Phylogeny, biology, and evolution of acanthopterygian fish clades

Abstract

The advent of molecular phylogenetics has rapidly transformed the understanding of relationships within Acanthopterygii, the spiny-rayed fishes. Acanthopterygii includes most of the marine fish diversity as well as several lineages in freshwater and contains such iconic groups as tunas, cichlids, seahorses, flatfishes, anglerfishes, and most fishes found on coral reefs. The robust and well-resolved phylogeny resulting from more than two decades of molecular studies includes some highly novel placements as well as unprecedented resolution of the lineages within Percomorpha. In this review, we highlight the patterns of morphology, ecology, biology, and biogeography within and among the major clades of Acanthopterygii using an evolutionary perspective that has been made possible by this emergent phylogenetic consensus. Our aim is to provide a comprehensive summary of each clade’s characteristics, serving as a reorientation for those familiar with previous conceptions of acanthopterygian phylogeny and as an introduction for those new to the biology, evolution, and biogeography of the major acanthopterygian groups.

Graphical abstract

Introduction

Acanthopterygii, the spiny-rayed fishes, contains 19,188 species classified in 313 taxonomic families (Fricke et al. 2023; Near and Thacker 2024) and includes most of the fish diversity in marine environments as well as a substantial fraction of species in fresh and brackish waters. Phylogenies based on analyses of morphological characters have provided insights into the evolutionary relationships of many acanthopterygian clades, but those efforts were unavoidably hampered by the incredible species diversity, the many instances of convergent phenotypic similarity, and the paucity of morphological characters informative at large phylogenetic scales (Lauder and Liem 1983; Johnson 1993; Johnson and Patterson 1993). In contrast, molecular data have provided an abundant source of phylogenetic characters applicable across the entire radiation, enabling resolution within and among the large clades that form the backbone of acanthopterygian phylogeny. Comprehensive efforts based on a variety of DNA sequence markers (Near et al. 2012b, 2013; Betancur-R et al. 2013, 2017; Faircloth et al. 2013; Alfaro et al. 2018; Hughes et al. 2018; Rabosky et al. 2018; Dornburg and Near 2021; Ghezelayagh et al. 2022) have largely converged on the same 16 major clades, with some ambiguity as to the relationships among lineages within those clades. This consilience among multiple studies has provided a consistent broader picture of higher-level fish relationships that is partially consistent with previous estimations based on morphology but also contains many novel groupings (Dornburg and Near 2021).

We recently published a monographic phylogenetic classification of ray-finned fishes (Actinopterygii) that reassessed the taxonomy of actinopterygians based on the relationships inferred primarily from molecular data (Near and Thacker 2024). In addition to providing a new taxonomy, our monograph discussed phylogenetic and taxonomic history of the major clades, listed species diversity, reviewed synonyms and known synapomorphic characters for each major clade, and provided summary phylogenetic trees for all extant family-rank taxonomic groups along with more than 285 fossil taxa. However, our monograph did not delve into the biology and ecology of these clades. In this review we cover the 16 major clades of Acanthopterygii; for each we list all the family-rank taxa and their common names, display the relationships of their living lineages with summary phylogenetic trees, and review their morphology, ecology, biology, and biogeography. We provide information on salinity tolerance, depth, and habitat preference, available details on their reproductive biology, and discuss the distribution of notable characteristics including bioluminescence, venom, air-breathing, mutualisms, endothermy, sound production, viviparity, and parental care. Our accounts reveal the phenotypic, ecological, geographic, and phylogenetic patterns within clades and serve as a review as well as a starting point for research exploring the evolution and biogeography of acanthopterygian fishes in their evolutionary context.

Following the classification of Near and Thacker (2024), we italicize all clade names and denote redundant family names (those containing a single genus) with asterisks in the taxon lists. We italicize all taxonomic names to facilitate their identification in the text, in accordance with the principles of rank-free phylogenetic nomenclature and recent taxonomic practice (deQuerioz and Cantino 2020; Thines et al. 2020; Brownstein et al. 2024). Common names for families are from the classification of Fricke et al. (2023); in rare cases where a common name is not given, we suggest one. All the phylogenetic trees shown here are derived from the hypothesis of Ghezelayagh et al. (2022) and the consensus trees shown in Near and Thacker (2024); we modify the trees presented in Near and Thacker (2024) to show only the living lineages, excluding fossil taxa. Species diversity estimates are those in Near and Thacker (2024) and are derived from the information given in Fricke et al. (2023), however, species counts are continually changing as groups are revised and new species are described.

The relationships among the 16 major acanthopterygian clades are shown in Fig. 1. Trachichthyiformes and Beryciformes resolve as sequential sister taxa to Percomorpha although Holocentridae has sometimes been placed outside Beryciformes (with ambiguous support; Betancur-R et al. 2013, 2017). Within Percomorpha the first major clade to diverge is Ophidiiformes, then Batrachoididae, followed by Gobiiformes and the clade containing Syngnathiformes and Scombriformes, although the relative placements of Gobiiformes and the clade containing Syngnathiformes and Scombriformes vary among phylogenetic analyses (Near et al. 2013; Betancur-R et al. 2013, 2017; Alfaro et al. 2018; Hughes et al. 2018; Dornburg and Near 2021; Ghezelayagh et al. 2022). Two large clades comprise the remainder of Percomorpha, one containing Atheriniformes, Blenniiformes, Synbranchiformes, and Carangiformes, and Eupercaria that includes Perciformes, Centrarchiformes, Labriformes, Acropomatiformes, and Acanthuriformes. These clades are resolved with broad agreement across molecular phylogenetic studies, although relationships within some of the clades are less confidently resolved.

Fig. 1

Phylogenetic relationships among the major clades of Acanthopterygii

Acanthopterygii (313 families and lineages, 19,188 species)

Trachichthyiformes (5 families, 71 species)

Anomalopidae (flashlight fishes), Anoplogasteridae* (fangtooths), Diretmidae (spinyfins), Monocentridae (pinecone fishes), Trachichthyidae (roughies).

Trachichthyiformes is a species-depauperate clade of robust, laterally compressed species with forked tails and often with small spines on the head and operculum; species of Monocentridae are covered with thick, ridged scales (Paxton 1999a, b, c). All Trachichthyiformes are marine, with a worldwide distribution from shallow nearshore habitats to the mesopelagic zone. Little is known about their reproduction, but it is likely they are broadcast spawners; spawning aggregations and pelagic eggs and larvae have been documented from a few species (Mace et al. 1990; Watson 1996a, b). Many species of Anomalopidae, Monocentridae, and Trachichthyidae possess cutaneous bioluminescent organs that host symbiotic bacteria, located under the eye in Anomalopidae, on the lower jaw in Monocentridae, and around the anus in Trachichthyidae (Davis et al. 2016a, b; Ghedotti et al. 2021). Anomalopidae and Monocentridae are associated with coral reefs, from shallow depths to 350 M and occur in schools (Paxton and Johnson 1999; Paxton 1999c). Anoplogastridae and Diretmidae are meso- to bathypelagic (200–3000 M; Paxton 1999a, b), and Trachichthyidae span the range from 2 to 1500 M (Moore and Paxton 1999a). Trachichthyidae is the most species-rich lineage, with 51 species; all other families have nine or fewer species (Fricke et al. 2023; Near and Thacker 2024). The stem age of Trachichthyiformes is estimated as 137.42 Ma (95% credible interval 129.12–147.3 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Trachichthyiformes are shown in Fig. 2.

Fig. 2

Phylogenetic relationships among the living lineages of Acanthopterygii, focusing on Trachichthyiformes, Beryciformes, Ophidiiformes, and Gobiiformes (representative Apogonoidei shown at left of tree; modified from Fig. 14 of Near and Thacker 2024)

Beryciformes (9 families, 213 species)

Berycoidei: Barbourisiidae* (Red Velvet Whalefish), Berycidae (alfonsinos), Cetomimidae (flabby whalefishes), Gibberichthyidae* (gibberfishes), Hispidoberycidae* (Spinyscale Pricklefish), Melamphaidae (bigscales), Rondeletiidae* (redmouth whalefishes), Stephanoberycidae (pricklefishes).

Holocentridae (squirrelfishes).

Species of Beryciformes are all marine, and except for Berycidae and Holocentridae, they occupy meso- to bathypelagic depths. The deepwater species are generally ovoid, with single dorsal fins and forked tails (Hastings et al. 2014). Unlike the deeper-dwelling beryciform lineages, Holocentridae and Berycidae are strong swimmers with large eyes and robust spines; they are nocturnal and range into shallower waters (25 to 1,300 M for Berycidae and 1 to 100 M in Holocentridae; Moore and Paxton 1999b). Berycidae and Holocentridae generally have red, yellow, or silvery coloration; red pigments appear black in deeper waters due to the differential filtration of longer wavelengths at depth. Holocentridae is the most species-rich lineage (90 species), followed by Melamphaidae (76 species) and Cetomimidae (27 species) (Fricke et al. 2023; Near and Thacker 2024).

The monophyly of Beryciformes is supported in some but not all molecular phylogenetic analyses of Acanthopterygii (Smith and Wheeler 2006; Alfaro et al. 2009; Santini et al. 2009; Near et al. 2012b, 2013; Davis et al. 2016a, b), and in particular, there are differing resolutions of Holocentridae (Betancur-R et al. 2013, 2017; Chen et al. 2014b; Dornburg et al. 2017; Hughes et al. 2018; Rabosky et al. 2018; Ghezelayagh et al. 2022). Species of Holocentridae are known from tropical reef and near-reef habitats in the Indo-Pacific and Atlantic and have been recorded in the Mediterranean as Lessepsian immigrants that transited the Suez Canal (Golani and Ben-Tuvia 1985; Farrag et al. 2018; Deef 2021). Phylogenetic reconstruction of biogeography that incorporates fossil taxa indicates that Holocentridae originated in the West Tethys reef biodiversity hotspot in the earliest Eocene, approximately 55 Ma, followed by multiple instances of divergence between the Western Atlantic and Eastern Pacific as well as the Indo-Pacific and Western Indian oceans as the West Tethys hotspot collapsed and the global center of reef fish diversity moved eastward to its present location in the Indo-Australian archipelago (Renema et al. 2008; Dornburg et al. 2014). Genetic connectivity among populations of cosmopolitan holocentrid species is generally high, with structure primarily evident only among ocean basins (Craig et al. 2007; Copus et al. 2022).

Beryciformes includes one of the most dramatic examples of sexual dimorphism and ontogenetic transformation known among fishes, in which the females, males, and larvae of some species of Cetomimidae exhibit morphologies so drastically different that they had previously been classified in different families. The connection between the forms was first suggested based on molecular data (Miya et al. 2003, 2005) and later confirmed based on the morphology of specimens of intermediate (transforming) larval stages (Johnson et al. 2009). Phylogenetic analysis calibrated with the earliest known holocentrid fossil places the origin of Holocentridae in the Paleocene (61.3 Ma), and the origin of Beryciformes in the Cretaceous (110.7 Ma) (Andrews et al. 2023). The stem age of Beryciformes is estimated as 132.91 Ma (95% credible interval 123.97–143.13 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Beryciformes are shown in Fig. 2.

Percomorpha (299 families and lineages, 18,904 species)

Ophidiiformes (3 families, 569 species)

Bythitoidei: Bythitidae (viviparous brotulas), Dinematichthyidae (dwarf brotulas).

Ophidiidae (cusk-eels and pearlfishes).

Ophidiiformes contains three lineages of demersal, almost exclusively marine fishes with a worldwide distribution in tropical and temperate habitats. Species of Bythitidae and Dinematichthyidae are livebearers with internal fertilization and intromittent organs present in males. This group also includes the pearlfishes in Ophidiidae, which lack the pelvic fins and girdle and are commensal with sea cucumbers, starfish, clams, and tunicates. They are generally slender, in most cases with the dorsal, caudal, and anal fins conjoined and the tail pointed, without a distinct caudal peduncle or fin (Hastings et al. 2014). Pelvic fins are often absent in species of Ophidiidae and some species have barbels on the chin. Scaled and scaleless species are found throughout Ophidiiformes. The livebearing lineages Bythitidae and Dinematichthyidae resolve as a clade that is the sister lineage of Ophidiidae (Betancur-R et al. 2013, 2017; Near et al. 2013; Møller et al. 2016). Ophidiidae contains 323 species; Bythitidae includes 129 species and Dinematichthyidae has 117 (Fricke et al. 2023; Near and Thacker 2024). An alternative taxonomy of Ophidiiformes includes the families Carapidae (37 species), Brotulidae (7 species), and Acanthonidae (3 species) (Wong and Chen 2024); however, we include these lineages in Ophidiidae (Near and Thacker 2024).

Ophidiiformes includes several species known from abyssal depths, including Thermichthys hollisi (Bythitidae) found on hydrothermal vents in the Galapagos as well as Abyssobrotula galatheae and Holomycteronotus profundissimus (Ophidiidae), known from depths of 3000–8000 m worldwide (Møller et al. 2016). Species of the cosmopolitan bathydemersal and abyssal ophidiid genus Porogadus are segregated by depth in tropical and subtropical oceans and include species pairs in the Atlantic and Eastern Pacific split by the Isthmus of Panama (Schwarzhans and Møller 2021). Bythitidae also contains several paedomorphic lineages (Aphyonus, Barathronus, and their relatives) that are small, scaleless, blind, have reductions and simplifications throughout their skeletal, muscular, and sensory systems and inhabit deep waters. Taxonomic and revisionary work on this group is active, with many new species being described, particularly from museum collections (Schwarzhans et al. 2005; Schwarzhans and Møller 2007, 2011, 2021). The stem age of Ophidiiformes is estimated as 126.76 Ma (95% credible interval 116.96–135.68 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Ophidiiformes are shown in Fig. 2.

Batrachoididae (toadfishes; 84 species)

Species of Batrachoididae are distributed worldwide, mostly in nearshore marine environments but with a few freshwater species including one species of Thalassophryne in the Amazon River. Toadfishes are benthic, with flattened heads and tapering bodies, and they are generally found hidden on or buried in the substrate (Hastings et al. 2014). The distributions of toadfish genera are roughly equally split between the Eastern Pacific and Atlantic vs. the Indo-Pacific (Greenfield et al. 2008). Spines in the anterior dorsal fin and on the opercle are hollow and venomous in species of Daector (Eastern Pacific) and Thalassophryne (Western Atlantic) (Smith and Wheeler 2006). Pectoral fins are large, some bearing axillary pores and secretory glandular tissue. The function of this tissue is unknown, and analyses of secretions of the Western Atlantic Opsanus beta revealed no toxic or pheromonal function (Maina et al. 1998), although it has been suggested that the pectoral gland supplies venom to the opercular spines in Porichthys (Lopes-Ferreira et al. 2014).

Toadfishes have a unique mechanism of sound production in which contractions of swim bladder muscles are used to create grunts, whistles, and croaks that are used both as mating calls and warnings (Rice and Bass 2009). They are also among the few shallow-water bioluminescent species known, with cutaneous photophores arranged in several ventral rows in Porichthys. Species of Porichthys are facultatively bioluminescent; those in the northern extent of their range lack adequate luciferin sources in their diet and so do not luminesce like their southern conspecifics (toadfish luminescence is endogenous and does not involve hosting symbiotic luminescent bacteria). The light organs are under voluntary control by the toadfish. The photophores produce light of the same intensity as ambient downwelling light, consistent with a function of counterillumination (Harper and Case 1999).

Toadfish females lay demersal eggs in a nest that is constructed and guarded by the male. After hatching, the larvae remain benthic and do not have a planktonic dispersal phase. Species tend to have restricted, neighboring, minimally overlapping distributions (Greenfield et al. 2008), consistent with speciation in allopatry following uncommon dispersal events. Due to the age and restricted dispersal abilities of species in this clade, inference of biogeographic history among toadfishes is very likely to show high concordance with vicariant events such as the closure of the Isthmus of Panama, even on very fine scales. The stem age of Batrachoididae is estimated as 121.82 Ma (95% credible interval 113.37–130.94 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). The phylogenetic relationship of Batrachoididae within Percomorpha is shown in Fig. 2.

Gobiiformes (12 families, 2,740 species)

Apogonoidei: Apogonidae (cardinalfishes), Kurtidae* (nurseryfishes).

Gobioidei: Butidae (gudgeons), Eleotridae (sleepers), Gobiidae (gobies), Milyeringidae (cave gudgeons), Odontobutidae (Asian freshwater sleepers), Oxudercidae (mudskippers and allies), Rhyacichthyidae (loach gobies), Thalasseleotrididae (ocean sleepers), Xenisthmidae (collared wrigglers).

Trichonotidae* (sand divers).

Gobiiformes is a worldwide radiation of small, usually benthic fishes that inhabit inshore marine habitats as well as fresh and brackish waters. The species are generally less than 200 mm in length (often less than 100 mm in Gobiidae) but vary in their body shapes. Kurtidae and Apogonidae are laterally compressed and nektonic, Trichonotidae are eel-like and bury themselves in sand, and Eleotridae, Butidae, Oxudercidae, and Gobiidae are variously laterally compressed or more commonly cylindrical in shape and benthic, many with fused pelvic fins that function as an attachment disc. Within Gobiiformes, Apogonidae and Kurtidae are sister lineages, and Trichonotidae and Gobioidei form a clade (Thacker 2009; Near et al. 2013; Thacker et al. 2015; Betancur-R et al. 2017). The most species-rich lineages are Gobiidae (1387 species) and Oxudercidae (703 species); within those families, 19 clades have also been delineated (Thacker and Roje 2011; Agorreta et al. 2013; Thacker 2013).

Gobiiform species engage in complex reproductive behaviors that involve parental care by the male. Eggs are laid in a benthic nest (Gobioidei), carried on the forehead of the male (Kurtidae), or brooded in the oral cavity (Apogonidae) or gill chamber (Trichonotidae). The eggs are adhesive, and bear elaborate caps and filaments (Thacker et al. 2015). Within Gobiidae, several species are hermaphroditic, including protogyny or either sequential or bidirectional sex change (Cole 1990; Maxfield et al. 2012; Kuwamura et al. 2020). In Eleotridae, the freshwater genus Hypseleotris includes several wide-ranging species in Australia that interbreed and form a hemiclonal hybrid complex (Thacker et al. 2022). In this system, parental species persist alongside their hemiclone hybrids; hemiclones retain half of their genome in each generation without recombination and reproduce by mating with one of their sexual parental species and likely also with other hemiclone hybrids. At reproduction, the hemiclone passes the haploid genome from one parent only, with the other haploid genome supplied by the sexual parent species and then discarded in the next generation during gametogenesis (Unmack et al. 2019; Majtánová et al. 2021).

Paedomorphosis (small size coupled with juvenile morphology) and miniaturization (small size alone) are common in Gobiidae and Oxudercidae, with several species attaining adult lengths of only 17–25 mm (Giovannotti et al. 2007; Iwata et al. 2001; Kon and Yoshino 2002). Gobiidae includes some of the smallest vertebrates known, including the paedomorphic Schindleria brevipinguis (Watson and Walker 2004). Paedomorphic gobies feature comprehensive simplifications in the skeleton and soft tissues including drastic rearrangements in the gonads (Thacker and Grier 2005; La Mesa 2012). All the paedomorphic species are transparent and pelagic, resembling larval Gobiidae as mature adults. In Schindleria, few morphological characters are useful in distinguishing species, but many cryptic taxa have been delineated based on phylogenetic analysis of DNA sequences (Kon et al. 2007). Schindleria species also exhibit complex variation in the shapes of the male genital papillae, raising the possibility that fertilization is internal, and that genital variation may promote speciation among otherwise very similar forms. Schindleria species perform the diel migrations typical of fish larvae, descending in the day and rising to the surface at night. They are most abundant in near-reef habitats during the new moon when they aggregate, presumably to mate and possibly to deposit their eggs on or in the reef substrate (Thacker and Grier 2005; Robitzch et al. 2021).

Gobies frequently participate in mutualistic associations, ranging from simply occupying a living substrate such as a coral or a sponge to complex cleaning behaviors and intimate mutualisms with burrowing alpheid shrimp (Rüber et al. 2003; Herler et al. 2009; Duchene et al. 2013; Tornabene et al. 2013). The obligate mutualism between shrimp and gobies has evolved several times (Thacker et al. 2011) although there are many fewer shrimp than goby species that participate in the mutualism and there is not a strict pattern of cospeciation (Thompson et al. 2013). The mutualism features a tactile communication system in which the shrimp keeps its long antennae in contact with the goby’s flank and the goby communicates by means of body movements and tail flicks (Karplus and Thompson 2011). Gobies also communicate with fin-flaring displays and several Mediterranean goby species in Oxudercidae and Gobiidae produce clicking and humming sounds both for courtship and aggression. The sounds are likely produced with the buccal and opercular bones and muscles given that adult gobies do not have swim bladders (Malavasi et al. 2008).

Kurtidae and several species of Apogonidae inhabit estuaries and mangroves, but most species of Apogonidae are nocturnal and occupy coral reef habitats (Berra et al. 2007; Thacker and Roje 2009). Some reef Apogonidae possess a visceral bioluminescent system consisting of pouches elaborated from the gut; in some species the bioluminescent organs host symbiotic bacteria, in others they do not. Bioluminescence in Apogonidae is ventral and provides counterillumination, camouflaging the fish in low light conditions and potentially also used for attracting prey. Luminescent adaptations vary among species and have evolved several times within Apogonidae (Thacker and Roje 2009; Davis et al. 2016a, b).

Biogeography and phylogeography have been investigated for several gobiiform clades, in particular the divergences within and among species of Apogonidae, Eleotridae, and Gobiidae in the Caribbean and Eastern Pacific (Taylor and Hellberg 2005; Maxfield et al. 2012; Galván-Quesada et al. 2016; Tornabene et al. 2016; Thacker 2017; Piñeros et al. 2019; Huie et al. 2020; Thacker et al. 2023). In those groups, the closure of the Isthmus of Panama promoted both speciation and morphological diversification and revealed that gobies may exhibit phylogeographic differentiation on surprisingly small spatial scales as well as along depth gradients. Similarly, genetic structure within complexes of Indo-Pacific reef gobies (Eviota; Tornabene et al. 2015), mudskippers (Periopthalmus; Polgar et al. 2014) and gudgeons (Eleotris; Mennesson et al. 2018) indicates that new species, often cryptic, are arising both allopatrically and sympatrically in the Coral Triangle. Gobies comprise a large portion of the cryptobenthic reef fauna (Brandl et al. 2018): small fishes that are morphologically cryptic but vital to the biodiversity and functioning of reef environments (Brandl et al. 2019).

Phylogeographic studies of Australian and New Zealand freshwater Gobiidae, Eleotridae, and Apogonidae (Cook et al. 2017; Hammer et al. 2019; Mossop et al. 2015; Shelley et al. 2020a; Thacker et al. 2007, 2008) confirm that many cryptic species are present among freshwater lineages and indicate that currently isolated freshwater systems may have experienced periods of high connectivity in the past. Similarly, phylogenetic analyses of Oxudercidae in the marine and freshwaters of Europe and Western Asia have revealed previously unrecognized diversity, prompted taxonomic adjustments, and shown that independently derived freshwater lineages share convergent similarities in body form (Huyse et al. 2004; Vanhove et al. 2012; Thacker and Gkenas 2019; Thacker et al. 2019). Reconstruction of continental-scale biogeographic patterns in Gobiidae and Oxudercidae by Thacker (2015) inferred a Tethyan-Indo-Pacific origin for gobies, with seven independent invasions of the Americas along multiple routes over the course of the past 50 million years.

Gobies are notoriously hardy, often euryhaline, and excellent invaders both through natural pathways and human-mediated introductions (Neilson and Stepien 2009). Expansions in immune system gene families in both amphibious mudskippers and invasive round gobies are hypothesized to allow both groups to contend with unfamiliar pathogens in novel environments (You et al. 2014; Adrian-Kalchhauser et al. 2020). The stem age of Gobiiformes is estimated as 117.81 Ma (95% credible interval 108.89–126.63 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Gobiiformes are shown in Fig. 2.

Scombriformes (17 families and lineages, 287 species)

Amarsipidae* (Bagless Glassfish), Ariommatidae* (ariommatids), Arripidae* (Australian salmon), Bramidae (pomfrets), Caristiidae (manefishes), Centrolophidae (medusafishes), Chiasmodontidae (swallowers), Gempylidae (snake mackerels), Icosteidae* (Ragfish), Lepidocybium flavobrunneum (Escolar), Nomeidae (driftfishes), Pomatomidae* (Bluefish), Scombridae (mackerels, tunas and bonitos), Scombrolabracidae* (Longfin Escolar), Stromateidae (butterfishes), Tetragonuridae* (squaretails), Trichiuridae (cutlassfishes).

Scombriformes is a worldwide group of marine predators occupying open ocean habitats as well as the deep sea. Disparate molecular phylogenies all resolve Scombriformes as monophyletic but agree on little else beyond clades that include Gempylidae and Trichiuridae, Caristiidae and Bramidae, and a clade containing Stromateidae, Ariommatidae, and Nomeidae (Miya et al. 2013; Near et al. 2013; Betancur-R et al. 2017; Hughes et al. 2018; Friedman et al. 2019; Arcila et al. 2021; Ghezelayagh et al. 2022). The most species-rich lineages are Scombridae (52 species) and Trichiuridae (47 species; Fricke et al. 2023; Near and Thacker 2024).

Overall body shape in Scombriformes ranges from the elongate, ribbon-like profiles of Gempylidae and Trichiuridae to the stout forms of Scombridae and the laterally compressed ovoid shapes of Stromateidae and Ariommatidae. Dorsal fins are paired or single, with a series of small finlets following the dorsal and anal fins in Scombridae and Gempylidae; most have forked tails. Icosteidae and Chiasmodontidae are known from deeper waters and are drab and darkly colored (Hastings et al. 2014; Friedman et al. 2019). Scombriformes are pelagic and often found in schools, and some undertake long distance migrations across ocean basins (Miya et al. 2013), yielding high connectivity among populations (Thiesen et al. 2008; Barth et al. 2017). Most are predators of bony fish except for Centrolophidae, Nomeidae, Ariommatidae, Tetragonuridae, and Stromateidae which consume jellyfishes, siphonophores, salps and other small invertebrates (Miya et al. 2013; Friedman et al. 2019; some Nomeidae are commensal with siphonophores). Reproductive mode has only been observed in some of the scombriform lineages, but it is likely that they are all broadcast spawners. Lineages in which reproduction has been documented exhibit a prolonged spawning period containing one or two peaks; they form spawning aggregations in coastal waters and have high fecundity (Dadzie et al. 2008; Juan-Jordá et al. 2013; de Souza et al. 2021).

Scombridae species are endothermic, and most utilize a countercurrent circulation system that retains metabolic heat; Gasterochisma employs a slightly different mechanism in which a heater organ derived from eye muscles maintains warmth only in the brain (Block et al. 1993; Block and Finnerty 1994; Dickson and Graham 2004; Little et al. 2010; Wu et al. 2021). These adaptations have enabled tunas to perform long migrations in both tropical and temperate waters, migrate vertically in the water column, and maintain visual acuity in low-light conditions (Block et al. 1993; Dickson and Graham 2004).

Calibrated phylogenetic hypotheses of Scombriformes infer a crown age in the latest Cretaceous, approximately 65–73 Ma, and infer a rapid divergence of scombriform lineages around that time (Miya et al. 2013; Near et al. 2013; Friedman et al. 2019; Harrington et al. 2021; Ghezelayagh et al. 2022). Collar et al. (2022) examined the evolution of scombriform body shapes and showed that the ancestral (and most common) shape is the streamlined, torpedo-shaped form of tunas. Deeper, flat bodied shapes arose twice (in Stromateidae and Bramidae), and similarly, elongate morphologies developed independently in Gempylidae and Trichiuridae, each with different modifications to the vertebral column. The stem age of Scombriformes is estimated as 110.3 Ma (95% credible interval 101.51–120.65 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Scombriformes are shown in Fig. 3.

Fig. 3

Relationships among the living lineages of Scombriformes and Syngnathiformes (modified from Fig. 15 of Near and Thacker 2024)

Syngnathiformes (11 families, 690 species)

Aulostomidae* (trumpetfishes), Callionymidae (dragonets), Centriscidae (shrimpfishes), Dactylopteridae (flying gurnards), Draconettidae (slope dragonets), Fistulariidae* (cornetfishes), Macrorhamphosidae* (snipefishes), Mullidae (goatfishes), Pegasidae (sea moths), Solenostomidae* (ghost pipefishes), Syngnathidae (pipefishes and seahorses).

Syngnathiformes is a charismatic group of small-bodied species found in temperate and tropical habitats worldwide, mostly in shallow nearshore marine environments. They are characterized by having small mouths that are sometimes terminal and borne on a tubular snout and varying degrees of bony armor in the skin (Longo et al. 2017; Santaquiteria et al. 2021). Molecular phylogenetic and phylogenomic analyses agree in resolving two clades within Syngnathiformes, one composed of Pegasidae, Dactylopteridae, Mullidae, Callionymidae and Draconettidae and a second including Syngnathidae, Solenostomidae, Aulostomidae, Fistulariidae, Centriscidae, and Macrorhamphosidae (Near et al. 2013; Betancur-R et al. 2017; Longo et al. 2017; Santaquiteria et al. 2021; Ghezelayagh et al. 2022). The most species-rich lineages are Syngnathidae (328 species) and Callionymidae (201 species; Fricke et al. 2023; Near and Thacker 2024).

Syngnathiformes comprises two distinct clades with different characteristics and ecological adaptations. The first clade includes benthic lineages with varying degrees of body armor; Mullidae lack body scutes entirely, while Callionymidae and Draconettidae feature spines only on their heads and opercles. Dactylopteridae exhibit more extensive armor, with bony plates and spines on the head and scute-like scales covering the body. Pegasidae stand out as the most heavily armored species of Syngnathiformes, being completely covered in bony plates and characterized by an elongated rostrum. Both Pegasidae and Dactylopteridae share a notable feature of dramatically enlarged, wing-like pectoral fins. The second clade exhibits a more nektonic lifestyle and includes Syngnathidae, Solenostomidae, Aulostomidae, Fistulariidae, Centriscidae, and Macrorhamphosidae. This group displays remarkable morphological diversity, ranging from the elongated forms of Aulostomidae and Fistulariidae to the distinctively long-snouted Centriscidae and Macrorhamphosidae and the unique seahorses and pipefishes in Syngnathidae. Despite their varied appearances, members of this nektonic clade share several common characteristics. They all possess a long snout terminating in a small suctorial mouth and are generally weak swimmers. Armor configurations vary within this group: Aulostomidae have small scutes on the posterior head region, Fistulariidae display lines of scutes along their bodies, and Syngnathidae, Centriscidae, and Macrorhamphosidae feature extensive body armor composed of bony plates and rings. These distinctive morphological and ecological characteristics highlight the remarkable evolutionary adaptations within Syngnathiformes (Longo et al. 2017; Santaquiteria et al. 2021; Kawahara et al. 2008).

Species of Syngnathiformes employ a variety of reproductive strategies. Most syngnathiform species are pelagic spawners: Mullidae spawn in aggregations, Fistulariidae, Aulostomidae, and Dactylopteridae are pelagic spawners but the specific behavior is unknown, and the males engage in courting behaviors, pair with females, and rise into the water to spawn in species of Pegasidae, Callionymidae, Draconettidae, Centriscidae and Macrorhamphosidae (de Oliviera et al. 1993; Awata et al. 2010; Pavlov et al. 2011; Bariche et al. 2013; Zhang et al. 2020). Among species of Solenostomidae, the eggs are brooded by the female in a pouch supported by the pelvic fins. All species of Syngnathidae display male parental care of the eggs, ranging from brooding on an open patch of skin on the underside of the tail to protection of embryos in partially or completely enclosed brood pouches on the abdomen. The location of the brooding structure is diagnostic for the two major clades within Syngnathidae: tail brooders (nine pipefish genera) are distinct from trunk brooders (all other pipefish species, seahorses, seadragons, and pygmy pipedragons), and it is in the trunk-brooding seahorses that truly viviparous male pregnancies occur (Wilson and Orr 2011; Hamilton et al. 2017).

Species of Syngnathiformes are distributed worldwide, with the highest species diversity in the Indo-Pacific and with species of Syngnathidae particularly abundant on both the temperate and tropical coasts of Australia (Hamilton et al. 2017). Lineages within Syngnathiformes originated in the Tethys reef hotspot in the late Cretaceous roughly 87 Ma and from there populated the Indo-Pacific, with multiple invasions of the Atlantic and Eastern Pacific (Hamilton et al. 2017; Santaquiteria et al. 2021). Species of Syngnathidae are concentrated in the central Indo-Pacific and have undergone several long-distance dispersal events (Li et al. 2021; Stiller et al. 2022). The stem age of Syngnathiformes is estimated as 110.3 Ma (95% credible interval 101.51–120.65 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Syngnathiformes are shown in Fig. 3.

Atheriniformes (32 families and lineages, 2,126 species)

Atherinoidei: Atherinidae (Old World silversides), Atherinopsidae (New World silversides), Atherionidae* (pricklenose silversides), Bedotiidae (Malagasy rainbowfishes), Isonidae* (surf sardines), Melanotaeniidae (rainbowfishes), Phallostethidae (priapum fishes), Pseudomugilidae (blue eyes), Telmatherinidae (sailfin silversides).

Belonoidei: Adrianichthyidae (ricefishes), Belonidae (needlefishes), Euleptorhamphidae (ribbon halfbeaks), Exocoetidae (flyingfishes), Hemiramphidae (halfbeaks), “hyporhamphids” (Arrhamphus + Chriodorus + Hyporhamphus + Melapedalion), Zenarchopteridae (viviparous halfbeaks).

Cyprinodontoidei: Anablepidae (four-eyed fishes), Aphaniidae (Oriental killifishes), Aplocheilidae (Old World rivulins), Cubanichthyidae (island pupfishes), Cyprinodontidae (pupfishes), Fluviphylacidae* (American lampeyes), Fundulidae (topminnows and killifishes), Goodeidae (splitfins), Nothobranchiidae (African rivulins), Orestiidae (Andean killifishes), Pantanodontidae (spine killifishes), Poeciliidae (livebearers), Procatopodidae (African lampeyes), Profundulidae (Middle American killifishes), Rivulidae (rivulins), Valenciidae* (European killifishes).

Atheriniformes includes a variety of inshore marine and freshwater fishes, some of which are diadromous, that are generally small-bodied and live in shallow habitats. Species of Atheriniformes either lay demersal eggs with adhesive filaments, often mouthbrooded or guarded in a substrate nest, or are viviparous (Mabuchi et al. 2007; Wainwright et al. 2012). Atheriniformes is also characterized by a restricted spermatogonial testis type in which sperm are generated from spermatogonia only at the ends of the testicular lobes rather than throughout the entire organ (Uribe et al. 2014). The most species-rich lineages are Rivulidae (476 species), Nothobranchidae (314 species), and Poeciliidae (274 species) (Fricke et al. 2023; Near and Thacker 2024). Atheriniformes contains three subclades: Atherinoidei, Belonoidei, and Cyprinodontoidei (Near and Thacker 2024).

Atherinoidei and Belonoidei are most frequently found in inshore marine habitats, in contrast to the generally freshwater Cyprinodontoidei. Spcies of Atherinoidei are all small, laterally compressed, usually with an overall silvery coloration and sometimes with a black lateral stripe. They have two separate dorsal fins, with flexible spines in the first and at the start of the second. The unusual species of Phallostethidae have internal fertilization, in which the male clasps and inseminates the female by means of an elaborate copulatory organ modified from the pelvic girdle (Dyer and Chernoff 1996). Atherinopsidae includes beach-spawning grunion species in both the temperate Western Atlantic (Menidia) and Eastern Pacific (Leuresthes). The California grunion Leuresthes tenuis performs coordinated spawning rituals in which fishes swim up onto beaches at high tide during full or new moons, the female burrows tail-first into the sand and lays eggs and the male curls around the female and fertilizes the clutch. Eggs incubate into the sand for roughly two weeks until the eggs hatch and the larvae are carried out to sea by the next high tide (Martin and Swiderski 2001).

Atherinoidei includes several remarkable radiations of brightly colored fishes in Australia, New Guinea, Sulawesi (and neighboring islands) and Madagascar, including species in Bedotiidae, Melanotaeniidae, Telmatherinidae, and Pseudomugilidae (the atherinid genus Craterocephalus is also diverse in Australia and New Guinea). Phylogenetic hypotheses based on both morphological and molecular data resolve Atherinopsidae (distributed in the Americas) as sister to the remaining lineages, which are distributed in Europe, Africa, Asia, Australia, and the Indo-Pacific (Dyer and Chernoff 1996; Setiamarga et al. 2008; Bloom et al. 2012; Campanella et al. 2015; Betancur-R et al. 2017; Ghezelayagh et al. 2022), and in most phylogenetic analyses the colorful Indo-Pacific Bedotiidae, Melanotaenidae, Telmatherinidae, and Pseudomugilidae are resolved as the crown clade.

Belonoidei is distributed worldwide, mostly in marine habitats except for some freshwater Belonidae, Hemiramphidae, and Zenarchopteridae. Species of Adrianichthyidae occupy freshwater and brackish habitats in the Indo-Pacific region. Molecular phylogenies resolve well-supported relationships among the belonoid lineages and agree in resolving Adrianichthyidae as the sister taxon to a clade containing Belonidae plus Zenarchopteridae as then sister lineage of a clade containing Hemiramphidae and Exocoetidae (Lovejoy et al. 2004; Near et al. 2013; Betancur-R et al. 2017; Ghezelayagh et al. 2022). A phylogenomic analysis of Belonoidei resolves a paraphyletic Hemiramphidae, with separate resolution of three clades including Euleptorhamphus and Rhynchorhamphus (Euleptorhamphidae); Arrhamphus, Chriodorus, Hyporhamphus, and Melapedalion (“hyporamphids”; Near and Thacker 2024); and Hemiramphidae restricted to Hemramphus and Oxyporhamphus (Daane et al. 2021). Lovejoy et al. (2004) investigated the evolutionary and ontogenetic patterns of upper and lower jaw elongation among Belonidae, Hemiramphidae, Zenarchopteridae, and Exocoetidae and refuted the hypothesis that the halfbeaked condition in Hemiramphidae is a paedomorphic reduction of the symmetric jaw elongation in Belonidae. A phylogenomic analysis of Belonoidei revealed that aerial gliding in Exocoetidae is linked to elevated rates of evolution in genes associated with pectoral fin size and musculature, neuromuscular control of the propulsive caudal fin, corneal adaptations for vision in air, and enlargement of the semicircular canals (Daane et al. 2021).

Species of Cyprinodontoidei are distributed worldwide, mostly in fresh or brackish water, and are characterized by having small, terminal mouths and a single spineless dorsal fin placed far back on the body. Many species of Cyprinodontoidei feature pronounced sexual dimorphism, with the males brightly colored and sometimes with elaborately extended fins (Hastings et al. 2014). Lineages of Cyprinodontoidei have radiated extensively in freshwaters of the Western Hemisphere (Fundulidae, Profundulidae, Goodeidae, Anablepidae, Poeciliidae, and most Cyprinodontidae), with the remaining lineages known from Europe, North Africa, and Asia (Parenti 1981; Pohl et al. 2015; Bragança et al. 2018). Pupfishes (Cyprinodon) are distributed patchily in Southern and Western North America and islands in the Caribbean. They include the endangered Devil’s Hole Pupfish, Desert Pupfish, and Owens Pupfish, all restricted to small waterholes and springs in California, Nevada, Arizona, and Mexico, relicts of distributions in larger ancient drainages or potentially the products of vectored overland dispersal (Martin and Turner 2018). Pupfishes are highly tolerant of extremes in both salinity and temperature but are threatened by habitat degradation and reduction due to water diversion and introduction of non-native species. Analysis of Cyprinodon phylogeny and trait data indicates that accelerations in morphological change are correlated with transitions from generalist to specialist feeding strategies (including scale-eating, molluscivory, planktivory and piscivory) in two lineages known from inland lakes in Mexico and the Bahamas (Martin and Wainwright 2011).

Cyprinodontoidei also includes livebearing species with internal fertilization, independently evolved in Anablepidae, Poeciliidae, and Goodeidae (Parenti 1981; Ghedotti and Davis 2013; Reznick et al. 2017; Amorim and Costa 2018; Bragança et al. 2018). Phylogenies of Cyprinodontoidei consistently resolve two clades within the group, one containing Aplocheilidae, Nothobranchiidae, and Rivulidae as the sister clade to the remaining lineages (Pohl et al. 2015; Betancur-R et al. 2017; Bragança et al. 2018; Ghezelayagh et al. 2022). Resolution among the deeper nodes in the phylogeny is weak, but Goodeidae, Profundulidae, and Cubanichthyidae are resolved as a clade, as are Cyprinodontidae, Orestiidae, and Fundulidae. Poeciliidae and Anablepidae are sister lineages, but the interrelationships of Fluviphylacidae, Procatopodidae, Aphaniidae, and Valenciidae are less clear (Ghedotti and Davis 2013; Reznick et al. 2017; Amorim and Costa 2018). Within Poeciliidae, most genera are monophyletic, and they are resolved into four subclades (Hrbek et al. 2007; Reznick et al. 2017; Rodríguez-Machado et al. 2024).

The stem age of Atheriniformes is estimated as 96.2 Ma (95% credible interval 86.23–105.98 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Atheriniformes are shown in Fig. 4.

Fig. 4

Phylogenetic relationships among the living lineages of Ovalentaria, including Atheriniformes and Blenniiformes (modified from Fig. 16 of Near and Thacker 2024)

Blenniiformes (22 families and lineages, 3,814 species)

Ambassidae (Asiatic glassfishes), Cichlidae (cichlids), Congrogadidae (eelblennies), Embiotocidae (surfperches), Gobiesocidae (clingfishes), Grammatidae (gramma basslets), Mugilidae (mullets), Opistognathidae (jawfishes), Pholidichthyidae* (convict-blennies), Plesiopidae (roundheads), Polycentridae (leaffishes), Pomacentridae (damselfishes and anemonefishes), Pseudochromidae (dottybacks).

Blennioidei: Blenniidae (combtooth blennies), Calliclinus (Calliclinus blennies), Chaenopsidae (pikeblennies), Clinidae (kelp blennies), Cryptotremini (cryptotremines), Dactyloscopidae (sand stargazers), Labrisomidae (labrisomid blennies), Neoclini (fringeheads), Tripterygiidae (triplefins).

Blenniiformes is the most species-rich major clade of acanthopterygians. The most species-rich lineage of Blenniiformes is Cichlidae (1,755 species), distributed in freshwater habitats in Madagascar, India, Africa, and the Neotropics with notable adaptive radiations in African Rift Valley Lakes. The other lineages in Blenniiformes are mostly marine and feature a variety of colorful benthic and reef-associated groups including Pomacentridae (426 species), Pseudochromidae (131 species), Plesiopidae (52 species), Congrogadidae (24 species), Grammatidae (18 species), Opistognathidae (106 species), Gobiesocidae (191 species), and Blennioidei (948 species) (Fricke et al. 2023; Near and Thacker 2024). Most blenniiform species have elongate single dorsal fins. Body shapes vary widely among lineages, including laterally compressed ovoid Pomacentridae, eel-like Congrogadidae and Pholidichthyidae, and large-finned, brightly colored Opistognathidae, Grammatidae, Pseudochromidae, and Plesiopidae. Embiotocidae, Ambassidae, Cichlidae, and Polycentridae attain more typical rhomboid shapes, while Blennioidei are elongate and often have cirri on the head. Gobiesocidae are highly modified benthic species, with large heads and modified pelvic fins that function as an adhesive disc (Hastings et al. 2014). Species of Blenniiformes, in common with Atheriniformes, produce eggs with adhesive strands; eggs are guarded in demersal nests or mouthbrooded (by males in both cases), or are internally fertilized and retained by females (Mabuchi et al. 2007; Wainwright et al. 2012).

Phylogenetic hypotheses for this group, primarily based on molecular data (Setiamarga et al. 2008; Wainwright et al. 2012; Near et al. 2013; Betancur-R et al. 2017), have revealed unexpected phylogenetic relationships including the placement of Pholidichthyidae and Polycentridae as sequential sister lineages of Cichlidae. Cichlids are globally distributed in tropical freshwaters but most of their diversity is found in the Rift Valley Lakes of Eastern Africa where they form an exceptionally large adaptive radiation. Cichlids are sexually dimorphic with bright coloration and share a suite of pharyngeal modifications that increase feeding efficiency and versatility, characteristics that facilitate divergence in sympatry (Stiassny 1981; Wainwright et al. 2012; Ronco et al. 2021). There is also genomic evidence for historic hybridization and numerous insertion and deletion polymorphisms among cichlids, both of which are implicated as contributing to their history of rapid lineage diversification (Meier et al. 2017; Kautt et al. 2020; McGee et al. 2020; Svardal et al. 2020; Ronco et al. 2021). The elongate, marine reef-dwelling Pholidichthys is an unlikely sister lineage of Cichlidae, but that placement is consistently resolved in molecular phylogenies and supported by the morphology of the pharyngeal jaw apparatus (Wainwright et al. 2012). Molecular phylogenies also support the monophyly of a clade containing Blennioidei, Opistognathidae, and Gobiesocidae. Polycentridae and Nandidae, with which Blennioidei is grouped in traditional taxonomies of Acanthopterygii are not closely related; Collins et al. 2015). Among Embiotocidae, Grammatidae, and Gobiesocidae, molecular phylogenetics has provided insight into the evolution of habitat partitioning by depth (Baldwin et al. 2018; Longo et al. 2018; Conway et al. 2020). Phylogenetic relationships among and within the lineages of Blennioidei have been inferred using Sanger-sequenced mtDNA and nuclear genes (Lin and Hastings 2013), and other molecular studies have focused on Tripterygiidae (Miller et al. 2014) and Blenniidae (Hundt et al. 2014; Wagner et al. 2021; Vecchioni et al. 2022). Molecular phylogenetic analyses agree in resolving the circumglobal tropical groups Tripterygiidae and Blenniidae as diverging earliest, followed by the temperate Clinidae and with the primarily Neotropical lineages Labrisomidae, Calliclinus, Cryptotremini, Chaenopsidae, Neoclini, and Dactyloscopidae comprising the crown clade. Lin and Hastings (2013) resolve Calliclinus and the remainder of Cryptotremini as clades distinct from Labrisomidae and resolve Neoclini as separate from Chaenopsidae. The origin of Blennioidei is estimated at 60.3 Ma, with the Neotropical crown clade arising 37.6 Ma, when the Neotropics were becoming increasingly isolated from the Tethys-Indo-Pacific diversity hotspot (Lin and Hastings 2013). Blenniidae, the most species-rich blennioid lineage, is distributed worldwide, with most diversity in the tropics but also including significant radiations in temperate rocky intertidal regions as well as a small clade of freshwater species distributed throughout the islands and nearshore rivers of the Mediterranean coasts (Hundt et al. 2014; Wagner et al. 2021). The stem age of Blenniiformes is estimated as 96.2 Ma (95% credible interval 86.23–105.98 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Blenniiformes are shown in Fig. 4.

Carangiformes (32 families, 1,107 species)

Centropomidae* (snooks), Lactariidae* (false trevallies), Latidae (giant perches), Polynemidae (threadfins), Sphyraenidae* (barracudas).

Carangoidei: Carangidae (jacks), Coryphaenidae* (dolphinfishes), Echeneidae (remoras), Istiophoridae* (marlin), Leptobramidae* (beachsalmons), Menidae* (moonfishes), Nematistiidae* (roosterfishes), Rachycentridae* (Cobia), Toxotidae (archerfishes), Trachinotidae (pompanos), Xiphiidae* (swordfishes).

Pleuronectoidei: Achiridae (American soles), Achiropsettidae (southern flounders), Bothidae (lefteye flounders), Citharidae (largescale flounders), Cyclopsettidae (sand whiffs), Cynoglossidae (tonguefishes), Oncopteridae* (Remo flounders), Paralichthodidae* (peppered flounders), Paralichthyidae (sand flounders), Pleuronectidae (righteye flounders), Poeciliopsettidae (bigeye flounders), Psettodidae* (spiny turbots), Rhombosoleidae (South Pacific flounders), Samaridae (crested flounders), Scophthalmidae (turbots), Soleidae (soles).

Carangiformes typically occupy marine environments and include strong pelagic swimmers as well as benthic flatfishes. Carangiform lineages range in shape from fusiform to laterally compressed and the pelagic groups are often silvery, but the flatfishes are generally drably colored and have a remarkable ability to camouflage themselves against the substrate (Akkaynak et al. 2017). As far as is known, they are external spawners with pelagic eggs (Glass et al. 2023). Many of the lineages are species-depauperate, limited to one or a few species. The most species-rich clades in Carangiformes are three of the flatfish families, Soleidae (180 species), Bothidae (169 species), and Cynoglossidae (168 species), followed by Carangidae (152 species; Fricke et al. 2023; Near and Thacker 2024).

Phylogenies inferred from mitochondrial and nuclear sequences and genomic datasets are largely consistent in resolving three clades in Carangiformes (Harrington et al. 2016; Ribeiro et al. 2018; Girard et al. 2020; Ghezelayagh et al. 2022; Glass et al. 2023). The first, with slight variations in the phylogenetic relationships among its constituent lineages, includes Latidae, Centropomidae, Lactariidae and Sphyraenidae. Latidae (distributed in the Indo-West Pacific and Africa) and Centropomidae (inhabiting the tropical Western Atlantic and Eastern Pacific) are large-bodied, with separate dorsal fins and a forked or rounded tail. Lactariidae (Indian and Western Pacific oceans) and Sphyraenidae (worldwide subtropical and tropical marine) are marine predators.

Carangoidei is the sister of a clade containing Pleuronectoidei and Polynemidae (Harrington et al. 2016; Ribeiro et al. 2018; Girard et al. 2020; Ghezelayagh et al. 2022; Glass et al. 2023). Species of Carangoidei are entirely marine except for the fresh and brackish water species of Toxotidae, and include several large predators, most notably species of Coryphaenidae, Istiophoridae, and Xiphiidae. Carangidae and Trachinotidae include a variety of strong-swimming pelagic fishes, ranging in shape from fusiform to highly laterally compressed. Most have two dorsal fins, slender caudal peduncles, and deeply forked caudal fins; many additionally have scutes on the lateral line and caudal peduncle (Smith-Vaniz 1999). Scomberoides lysan (Trachinotidae) is venomous, delivering the venom with spines in the dorsal and anal fins (Halsted et al. 1972; Smith and Wheeler 2006). The unusual species of Toxotidae inhabit the fresh and brackish waters of the Indo-Pacific region and catch prey by spitting streams of water at insects on overhanging vegetation (Allen 1978); the water jet is generated by forcing water from the buccal cavity through a tube formed by the juxtaposition of several ridges and grooves elaborated from the bones and soft tissue of the oral cavity (Girard et al. 2022). Leptobramidae and Toxotidae resolve as a clade, and species of Leptobrama possess oral modifications similar to those in Toxotidae which they may use to push water onto the substrate and uncover buried prey (Girard et al. 2022).

Echeneidae are commensal, attaching to hosts such as sharks, turtles, whales, or larger fishes by means of a dorsal fin modified into an adherent disc (Friedman et al. 2013a). The commensalism is not permanent; the remora can attach or release the disk and is a capable swimmer but is usually attached to a host (O’Toole 2002; Friedman et al. 2013a). Carangoidei contains some of the largest and most spectacular pelagic fishes, the billfishes in Xiphiidae and Istiophoridae (Orrell et al. 2006). These migratory predators can reach body lengths of 3–5 M and have spear-like bills formed from fused extensions of the upper jaws (premaxillae). The bills are used for hunting by slashing through schools of smaller fish or squid and stunning or injuring them (Habegger et al. 2015). Billfishes are endothermic, but the endothermy is restricted to the eyes and brain and is accomplished with a thermogenic organ underneath the brain that is derived from external eye muscles in conjunction with a vascular countercurrent heat exchange system (Block et al. 1993; Block and Finnerty 1994; Dickson and Graham 2004; Wu et al. 2021).

The most species-rich lineage of Carangiformes is the clade that contains Polynemidae and Pleuronectoidei. Flatfishes are characterized by the remarkable larval transformation of eye migration from one side of the head to the other, resulting in cranial asymmetry and enabling them to rest sideways on the substrate while keeping both eyes exposed. The placement of Polynemidae as the sister taxon to Pleuronectoidei is a result resolved in molecular phylogenies (Harrington et al. 2016; Girard et al. 2020; Ghezelayagh et al. 2022), a phylogenetic hypothesis that is also supported by morphological characters (Girard et al. 2020). Flatfishes are also united by many morphological traits beyond the ontogenetic migration of one eye around the midline, including extension of the dorsal fin onto the head and the presence of the recessus orbitalis, a sac behind the eyeball that can be filled with fluid causing the eyeballs to protrude above the surface of the head and above the substrate if the fish is buried (Chapleau 1993; Campbell et al. 2019). In contrast to the strong morphological evidence for flatfish monophyly, some molecular phylogenetic hypotheses resolve Psettodidae separately from the other flatfish lineages (Smith and Wheeler 2006; Li et al. 2011; Betancur-R et al. 2013; Campbell et al. 2013; Near et al. 2013; Lü et al. 2021). Others resolve Psettodidae as sister to all other flatfishes (Betancur-R and Orti 2014; Harrington et al. 2016; Betancur-R et al. 2017; Campbell et al. 2019; Girard et al. 2020; Evans et al. 2021; Duarte-Ribeiro et al. 2024), although in all molecular phylogenetic analyses the branch lengths connecting the internodes among flatfishes and their relatives are shallow.

The transformation from a symmetrical ancestor into asymmetric flatfishes was a rapid process that involved modular modifications of the skull, occurring near the K-Pg boundary at approximately 65.7 Ma and completing in no more than three million years (Friedman 2008; Harrington et al. 2016; Evans et al. 2021). Within Carangoidei, Frédérich et al. (2016) compared body shape change with reef association and detected a higher rate of morphological change following transition from reef to non-reef habitats. Glass et al. (2023) identified a widespread pattern of sympatry between sister species pairs, with sympatric species exhibiting a greater difference in both body size and depth preference, regardless of their time of divergence. Allopatric species pairs could mostly be attributed to vicariance, either due to the rise of the Isthmus of Panama or to the barrier imposed by cold current systems off the coast of South Africa. The stem age of Carangiformes is estimated as 98.87 Ma (95% credible interval 87.37–110.69 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Carangiformes are shown in Fig. 5.

Fig. 5

Phylogenetic relationships among the living lineages of Synbranchiformes and Carangiformes (modified from Fig. 17 of Near and Thacker 2024)

Synbranchiformes (9 families, 414 species)

Anabantoidei: Anabantidae (climbing gouramis), Channidae (snakeheads), Helostomatidae* (Kissing Gourami), Nandidae (Asian leaffishes), Osphronemidae (gouramis).

Synbranchoidei: Chaudhuriidae (earthworm eels), Indostomidae* (armored sticklebacks), Mastacembelidae (freshwater spiny eels), Synbranchidae (swamp eels).

Synbranchiformes is the most geographically restricted of the acanthopterygian clades, distributed almost exclusively in freshwater habitats of Asia and Africa except for a few species of Synbranchidae in Mexico, Central and South America, and the Indo-Australian archipelago. All species of Synbranchiformes utilize freshwater habitats except for synbranchids and some channids which can tolerate brackish water. Notably, all species have vascularized pouches in the buccal cavity (suprabranchial or labyrinth organs) that enable them to absorb oxygen from air, a great advantage in that they can occupy stagnant, swampy habitats with low oxygen by gulping air at the surface. Some species of Synbranchidae and Mastacembelidae are capable of burrowing into mud and surviving periods out of water; they as well as species of Channidae can disperse over land. The most species-rich lineages of Synbranchiformes are Osphronemidae (135 species), Channidae (57 species), and Mastacembelidae (93 species; Fricke et al. 2023; Near and Thacker 2024).

The morphology of synbranchiform species varies greatly, from the elongate eel-like forms of Synbranchidae, Mastacembelidae, and Chaudhuriidae through to the brightly colored, long-finned species in Osphronemidae, popular in the aquarium trade and extensively bred in captivity. Species of Nandidae are laterally compressed and rhomboid. The unusual Indostomus is small (3–4 cm in length) and cylindrical, with an elongated snout and scutes on the body. In many respects Indostomus resembles a slender stickleback (Gasterosteidae) and their body armor has a similar ontogenetic pattern (Britz and Johnson 2002), but they are distantly related (Kawahara et al. 2008). A general commonality among all the disparate synbranchiforms is the presence of an elongate, single dorsal fin, usually originating far back on the body (in Indostomus, the separate spinous dorsal fin consists of five isolated spines with small membranes, each supported by a bony scute). The anal fin is also elongate, and in some Osphronemidae the first pelvic fin rays are extended and filamentous. The exception to that fin morphology is the eel-like Synbranchidae, in which both the dorsal and anal fins are reduced to ridges on the body, the caudal fin is tiny or absent, and the pectoral and pelvic fins are both absent in adults (pectorals are transitorily present in the larvae). Pelvic fins are also absent in Mastacembelidae, Chaudhuriidae, and some Channidae (Favorito et al. 2005; Rüber et al. 2006; Hastings et al. 2014).

Species of Synbranchiformes usually engage in some form of egg guarding by the male involving mouthbrooding or the deposition of the eggs into bubble nests (Osphronemidae), plant or substrate nests (Indostomidae, Chaudhuriidae, Mastacembelidae, Nandidae), floating at the surface (Channidae), or in burrows (Synbranchidae); some species of Synbranchus are protogynous sequential hermaphrodites. Helostomidae and some Anabantidae are free spawners; other Anabantidae are bubble nesters or mouthbrooders (Britz 1997; Rüber et al. 2004b, 2006; Favorito et al. 2005; Li et al. 2006; Britz et al. 2020). Some species of Channa attain large sizes and high fecundities, and that coupled with their ability to breathe air, survive out of water for extended periods, and locomote on land makes them highly invasive when transplanted (Courtenay and Williams 2004).

The historical biogeography of Synbranchiformes is potentially tightly correlated to the movement of continents due to their nearly exclusive restriction to freshwater. Several lineages (Osphronemidae, Helostomatidae, Indostomidae, and Chaudhuriidae) are restricted to Southern Asia, while the others (Anabantidae, Channidae, Nandidae, Synbranchidae, and Mastacembelidae) have a disjunct distribution that includes both South Asia and Central Africa. One possible explanation for this pattern is that those lineages originated in Africa prior to the breakup of eastern Gondwana 120–130 Ma and then some species were rifted northward on the Indian/Malagasy plate and delivered to southern Asia between 35 and 50 Ma, although no species of Synbranchiformes are distributed in Madagascar today. However, time-calibrated phylogenies that are not constrained by this biogeographic scenario estimate younger dates for the origin and diversification of synbranchiform lineages and infer a Southeastern Asian origin for the group, followed by dispersal into India and Africa (Li et al. 2006; Adamson et al. 2010; Rüber et al. 2020; Harrington et al. 2023). Paleontological evidence likewise rejects the Gondwanan vicariance scenario (Capobianco and Friedman 2019). Two genera of Synbranchidae, Synbranchus and Ophisternon, separately invaded Central America from Africa in the Miocene 12.7–23 Ma (Perdices et al. 2005). Mastacembelidae originated in Asia and migrated to Africa in the Miocene approximately 15.4 Ma, then radiated extensively throughout Central Africa including the Congo Basin and the Rift Valley Lakes during the Miocene (Day et al. 2017). Within the South Asian genera Badis and Dario (Nandidae), the phylogeny is consistent with vicariant speciation in several clades due to river drainage rearrangement caused by the uplift of the Tibetan Plateau in the late Oligocene to Miocene (19–23 Ma; Rüber et al. 2004a). The stem age of Synbranchiformes is estimated as 98.87 Ma (95% credible interval 87.37–110.69 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Synbranchiformes are shown in Fig. 5.

Eupercaria (160 families and lineages, 7,073 species)

Perciformes (58 families and lineages, 3,200 species)

Acanthistiinae* (wirrahs), Anthiadidae (fairy basslets), Bembropidae (duckbill flatheads), Epinephelidae (groupers), Serranidae (sea basses).

Notothenioidei: Aethotaxis (Longfin Icedevil), Bathydraconidae (Antarctic dragonfishes), Bovichtidae (thornfishes), Channichthyidae (crocodile icefishes), Dissostichus (toothfishes), Eleginopsidae* (Patagonian Blennie), Gobionotothen (goby rockcods), Gvozdarus, Harpagiferidae (spiny plunderfishes), Nototheniidae (cod icefishes), Percophidae* (Brazilian Flathead), Pleuragrammatinae* (Antarctic Silverfish), Pseudaphritidae* (Congoli), Trematominae (notoperches).

Percoidei: Niphonidae* (Ara Grouper), Percidae (perches and darters), Trachinidae (weeverfishes).

Scorpaenoidei: Anoplomatidae (sablefishes), Bembridae (deepwater flatheads), Gasterosteidae (sticklebacks), Platycephalidae (flatheads), Triglidae (searobins).

• Cottoidea: Agonidae (poachers), Cottidae (sculpins), Cyclopteridae (lumpfishes), Hexagrammidae (greenlings), Jordaniidae (longfin sculpins), Liparidae (snailfishes), Psychrolutidae (marine sculpins), Rhamphocottidae (horsehead sculpins), Scorpaenichthyidae* (Cabezon), Trichodontidae (sandfishes), Zaniolepididae (combfishes)

• Scorpaenoidea: Congiopodidae (pigfishes), Hoplichthyidae* (spiny flatheads), Neosebastidae (gurnard scorpionfishes), Normanichthyidae* (Mote Sculpin), Plectrogeniidae (stinger flatheads), Scorpaenidae (scorpionfishes), Synanceiidae (stonefishes)

• Zoarcoidea: Anarhichadidae (wolffishes), Bathymasteridae (ronquils), Cebidichthyidae (monkeyface pricklebacks), Cryptacanthodidae* (wrymouths), Eulophiidae (spinous eelpouts), Lumpenidae (eel pricklebacks), Neozoarcidae (largemouth kissing eelpouts), Opisthocentridae (rearspined fin pricklebacks), Pholidae (gunnels), Ptilichthyidae* (Quillfish), Stichaeidae (pricklebacks), Zaproridae* (Prowfish), Zoarcidae (eelpouts)

Species of Perciformes are distributed globally in marine and freshwater environments, exhibiting significant presence in the nearshore marine areas of the Arctic and Antarctic as well as freshwater habitats across the Holarctic region. They include benthic and nektonic species, and body shapes are diverse, ranging from rhomboid to cylindrical and moderately elongate, with one or two dorsal fins and usually a forked or rounded tail (Hastings et al. 2014). Reproductive strategies include broadcast spawning, benthic deposition of eggs with parental care, and several instances of livebearing (Page et al. 1985; Yokoyama and Goto 2005; Hyde and Vetter 2007; Goto et al. 2014; La Mesa et al. 2020). Perciformes has had a long history as a catch-all taxon for lineages not morphologically distinct enough to be placed into other acanthopterygian groups (Dornburg and Near 2021; Near and Thacker 2024). Molecular phylogenies have been particularly effective at circumscribing Perciformes and resolving the relationships of the lineages within it (Smith and Wheeler 2004; Smith and Craig 2007; Smith and Busby 2014; Near et al. 2012b, 2015, 2018; Smith et al. 2018). The most species-rich lineages in this clade are Liparidae (448 species), Scorpaenidae (394 species), and Zoarcidae (314 species; Fricke et al. 2023; Near and Thacker 2024).

Perciformes includes several groups that encompass taxa traditionally placed in either Perciformes or Scorpaeniformes. Percoidei contains Percidae, a clade of 244 species distributed throughout the freshwater habitats in Eastern North America, Asia, and Europe, as well as its marine sister lineages Trachinidae and Niphonidae (Near et al. 2013, 2015). The most species-rich genus of Percidae is Etheostoma, containing more than 160 species of small benthic fishes distributed primarily in the Eastern United States, with a complex history of speciation within and exchange among river drainages (Near et al. 2011; Near and Keck 2013; Kim et al. 2023). Notothenioidei is comprised of the radiation of icefishes, dragonfishes, and plunderfishes in circum-Antarctic waters and their sister linages in Southern Hemisphere cold temperate habitats (Near et al. 2018). The ability of notothenioids to invade subzero polar waters is tied to the adaptation of antifreeze glycoproteins which bind to and encapsulate ice crystals in the blood, preventing their growth (Near et al. 2012a, 2015, 2018; Colombo et al. 2014).

Scorpaenoidei is most species-rich perciform subclade, with 2,208 species classified into Scorpaenoidea, Cottoidea, Zoarcoidea, Gasterosteidae, and three additional families (Ghezelayagh et al. 2022; Near and Thacker 2024). Most are marine, but the freshwater sculpin (Cottidae) radiations in Western North America and Eurasia are notable counterexamples (Smith and Wheeler 2004; Goto et al. 2014; Smith and Busby 2014). Species of Sebastes in the Eastern Pacific comprise a cold-temperate radiation of livebearers that cooccur across gradients of depth, temperature, and habitat (Hyde and Vetter 2007). Zoarcoidea species are marine, and many are small, elongate, and cryptic, sheltering on or in complex benthic habitats in cold temperate regions and the poles (Hotaling et al. 2021). Within Scorpaenoidea, many species bear spines on the head and opercles and in the fins, some of which are equipped with venom glands (Smith and Wheeler 2004, 2006).

The stem age of Perciformes is estimated as 93.73 Ma (95% credible interval 81.7–107.69 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Perciformes are shown in Fig. 6.

Fig. 6

Relationships among the living lineages of Perciformes (modified from Fig. 18 of Near and Thacker 2024)

Centrarchiformes (20 families, 304 species)

Percalates (Australian basses).

Centrarchoidei: * Aplodactylidae* (marblefishes), Centrarchidae (sunfishes and freshwater basses), Cheilodactylidae* (fingerfins), Chironemidae* (kelpfishes), Cirrhitidae (hawkfishes), Enoplosidae* (Oldwife), Latridae (trumpeters), Parascorpididae* (Jutjaw), Percichthyidae (temperate basses), Sinipercidae (Chinese perches).

Terapontoidei: * Caesioscorpididae* (Blowhole Perch), Dichistiidae* (galjoens), Girellidae (nibblers), Kuhliidae* (flagtails), Kyphosidae (sea chubs), Microcanthidae (stripeys), Oplegnathidae* (knifejaws), Scorpididae (halfmoons), Terapontidae (grunters).

Centrarchiformes comprises a clade of species distributed in nearshore marine habitats in the Atlantic, Pacific, and Indian Oceans, with freshwater lineages (Centrarchidae, Percichthyidae, Sinipercidae, Terapontidae) in North America, Australia, New Guinea, South America, and East Asia. Several groups (Aplodactylidae, Caesioscorpididae, Cheilodactylidae, Chironemidae, Enoplosidae, Latridae, Percalates, Percichthyidae, Terapontidae) are known exclusively from the Southern Hemisphere, particularly in and around Australia. Others are restricted to temperate North America (Centrarchidae) or East Asia (Sinipercidae), with the remaining lineages (Cirrhitidae, Dichistiidae, Girellidae, Kuhliidae, Kyphosidae, Microcanthidae, Oplegnathidae, Parascorpididae, Scorpididae) distributed widely in temperate and tropical oceans (Burridge and Smolenski 2004; Davis et al. 2012; Knudsen and Clements 2013; Chen et al. 2014a; Arratia and Quezada-Romegialli 2019; Ludt et al. 2019).

The body of centrarchiform species is usually ovoid or disc-shaped, generally with a single dorsal fin (often with a notch between the spinous and rayed portions) and a forked or truncate tail. Most species of Centrarchiformes are predators of other fishes and invertebrates, but dietary diversity in the clade includes durophagous (e.g., Oplegnathus) and herbivorous species (e.g., Aplodactylus, Kyphosidae, Hephaestus, and Scortum) (Davis et al. 2016a, b; Maschette et al. 2020; Johnson and Clements 2022). Parental care through nest guarding is widespread in the freshwater lineages Percichthyidae and Centrarchidae (Growns 2004; Neff and Knapp 2009). Centrarchiformes are economically important as many species are the targets of commercial and recreational fisheries (Long et al. 2015; Taylor et al. 2019). The most species-rich lineages in this clade are Terapontidae (62 species), Centrarchidae (47 species), and Cirrhitidae (35 species); most of the lineages contain 20 or fewer species (Fricke et al. 2023; Near and Thacker 2024).

Centrarchiformes were first resolved as a clade in molecular phylogenetic analyses in the first wave of studies with an inclusive taxon sampling of percomorph lineages that used mitochondrial and nuclear gene sequences (Near et al. 2012b, 2013; Betancur-R et al. 2013; Chen et al. 2014b; Sanciangco et al. 2016). There are three major lineages of Centrarchiformes: (1) Percalates, resolved as the sister lineage of all other Centrarchiformes (Fig. 18; Near et al. 2012b; Chen et al. 2014b; Lavoué et al. 2014; Ghezelayagh et al. 2022); (2) Terapontoidei, including Girellidae, Scorpididae, Parascorpis typus, Dichistius, Microcanthidae, Caesioscorpis theagenes, Oplegnathus, Kyphosidae, Kuhlia, and Terapontidae (Yagishita et al. 2002, 2009; Knudsen and Clements 2016; Sanciangco et al. 2016; Betancur-R et al. 2017; Knudsen et al. 2019; Ghezelayagh et al. 2022); and (3) Centrarchoidei, including Enoplosus armatus, Percichthyidae, Centrarchidae, Sinipercidae, Cirrhitidae, Latridae, Chironemus, Cheilodactylus, and Aplodactylus (Li et al. 2010; Near et al. 2012b, 2013; Sanciangco et al. 2016; Betancur-R et al. 2017; Song et al. 2017; Ghezelayagh et al. 2022). The seven species of North American freshwater Elassoma (pygmy sunfishes) are classified in Centrarchidae based on molecular phylogenetic analyses (Near et al. 2012c; Chen et al. 2014a, b; Ghezelayagh et al. 2022).

The two largest radiations within Centrarchiformes, Centrarchidae and Terapontidae, occur in freshwater. Centrarchidae are widely distributed in the rivers of the Eastern United States, and freshwater Terapontidae (genera Amniataba, Bidyanus, Hannia, Hephaestus, Lagusia, Leiopotherapon, Pingala, Scortum, Syncomistes, and Variichthys) inhabit Australia, New Guinea, and parts of Southeast Asia, with the highest diversity in the Kimberly region of Northwestern Australia (Near et al. 2004, 2005; Shelley et al. 2019, 2020b; Near and Kim 2021). In both Centrarchidae and Terapontidae, the availability of time-calibrated phylogenies has enabled macroevolutionary studies investigating topics that include the role of dietary specialization on phenotypic evolution and diversification (Collar et al. 2005, 2009; Davis et al. 2012, 2016a, b), the evolution of post-zygotic reproductive isolation (Bolnick and Near 2005; Bolnick et al. 2006, 2008), and the patterns of allopatric speciation among adjacent geographic regions (Sandel et al. 2014; Shelley et al. 2020c; Kim et al. 2022a). Species discovery and delimitation in Centrarchiformes remains an active area of research, particularly using molecular data (Shelley et al. 2020b; Kim et al. 2022a, b). The stem age of Centrarchiformes is estimated as 83.17 Ma (95% credible interval 75.25–92.76 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Centrarchiformes are shown in Fig. 7.

Fig. 7

Phylogenetic relationships among the living lineages of crown Eupercaria, focusing on Centrarchiformes, Labriformes, and Acropomatiformes (modified from Fig. 19 of Near and Thacker 2024)

Labriformes (7 families, 887 species)

Ammodytidae (sand lances), Centrogenyidae* (False Scorpionfish), Cheimarrichthyidae* (New Zealand Torrentfish), Labridae (wrasses and parrotfishes), Leptoscopidae (southern sandfishes), Pinguipedidae (sandperches), Uranoscopidae (stargazers).

Labriformes are exclusively marine, except for the amphidromous Cheimarrichthys fosteri. The clade includes many reef-dwelling species as well as several lineages that are benthic or burrow in sand. Labriformes comprises two clades, one containing Labridae as sister to Centrogenyidae and a second including Ammodytidae, Cheimarrichthyidae, Leptoscopidae, Pinguipedidae, and Uranoscopidae. Labridae range in shape from oblong to elongate and cylindrical, generally with either rounded or truncate caudal fins (Hastings et al. 2014). Labridae (680 species) is the most species-rich lineage, followed by Pinguipedidae (100 species) and Uranoscopidae (59 species; Fricke et al. 2023; Near and Thacker 2024).

Labridae includes some of the most brightly colored and charismatic reef fishes, including the fairy wrasses (Cirrhilabrus), flasher wrasses (Paracheilinus), rainbow wrasses (Coris), cleaner wrasses (Labroides), the parrotfish genera Scarus and Sparisoma, and the many species of Halichoeres and Thalassoma (Westneat and Alfaro 2005; Kazancioglu et al. 2009; Tea et al. 2022). Labridae are characterized by the presence of a complex of oral and pharyngeal jaw specializations (pharyngognathy) resulting in a robust, mobile, and versatile feeding apparatus that enables them to consume a wide variety of prey, including the fused oral teeth and pharyngeal mills with which parrotfishes grind coral and other hard substrates which they then excrete as sand (Westneat 1995; Mabuchi et al. 2007; Kazancioglu et al. 2009; Price et al. 2011; Wainwright et al. 2012). The labrid sister lineage Centrogenyidae shares some of the pharyngeal jaw modifications found in Labridae but it is benthic and has mottled coloration that resembles a scorpionfish, likely an adaptation for camouflage or possibly to mimic the venomous Scorpaena (Ghezelayagh et al. 2022). Most Labridae and Centrogenyidae are less than 25 cm in length although some wrasse species may be much larger, including the Humphead Wrasse (Cheilinus undulatus) and the Green Humphead Parrotfish (Bolbometopon muricatum) in tropical Indo-Pacific waters, and the California Sheephead (Semicossyphus pulcher) in the temperate Eastern Pacific. Both Labridae and Centrogenyidae have single continuous dorsal fins with distinct spinous and rayed portions.

The sister lineage of the clade that includes Labridae and Centrogenyidae includes several groups whose species are benthic and often burrow into sand substrates, plus the New Zealand endemic Cheimarrichthyidae which are amphidromous and inhabit fast-flowing streams (Scrimgeour and Eldon 1989). Species of Uranoscopidae and Leptoscopidae have dorsally placed eyes and bury themselves in sand. They are ambush predators and some species of Uranoscopidae have a lure modified from the buccal tissue that they use for prey attraction. Species of Uranoscopidae additionally bear paired venomous spines behind the opercles, and some species have electrogenic organs in their heads; both the spines and electric shocks are used for hunting and defense (Kishimoto 2001; Smith and Wheeler 2006). Species of Leptoscopidae inhabit the coastal waters of Australia and New Zealand and are also benthic ambush predators. Species of Ammodytidae are distributed worldwide but most are distributed in the cold temperate North Pacific and North Atlantic. They are also burrowers, with long slender bodies lacking swim bladders and pelvic fins, and species of Ammodytes spend part of the year dormant under the sand (Robards and Piatt 1999). Species of Pinguipedidae are benthic but do not burrow, they are active predators distributed worldwide in reef and sandy habitats. Species of Cheimarrichthyidae are known only from New Zealand and are benthic and specialized for life in fast-flowing streams. Species of Leptoscopidae and Ammodytidae have continuous dorsal fins; those in Pinguipedidae and Uranoscopidae have a distinct anterior spined portion, and Cheimarrichthyidae have the anterior dorsal spines each separate at the origin of the fin (McDowall 1973).

Within Labridae, most species are sequential protogynous hermaphrodites, but not all individuals are born female; some are primary males. Among the primary females, some will transition after attaining their adult sizes and the color morphs of these secondary males are different from those of primary males and females (Warner and Robertson 1978; Kazancioglu and Alonso 2010; Choat et al. 2012; Kuwamura et al. 2020). Generally, labrid species are broadcast spawners with various types of group spawning, but temperate species in Centrolabrus, Labrus, and Symphysodus engage in nest building and egg guarding by the male (Hanel et al. 2002). The reproductive strategies among Uranoscopidae, Leptoscopidae, and Ammodytidae are not as well known, but those that have been observed are benthic spawners with planktonic larvae (eggs are also planktonic in Uranoscopus; Çoker et al. 2008) and no parental care (Robards and Piatt 1999; Han et al. 2012). Pinguipedidae are also benthic spawners and at least some species of Parapercis are protogynous hermaphrodites, with large males controlling a territory inhabited by a harem of females (Walker et al. 2007; Villanueva-Gomila et al. 2015). Cheimarrichthyidae are amphidromous, spawning in freshwater with larvae swept out to sea then returning to freshwater as juveniles (McDowall 1973; Scrimgeour and Eldon 1989). Many species of reef-dwelling Labridae engage in cleaning behaviors, obligately or facultatively, and the various types of cleaning strategy have evolved repeatedly within the group (Baliga and Law 2016). The stem age of Labriformes is estimated as 81.03 Ma (95% credible interval 73.25–89.3 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Labriformes are shown in Fig. 7.

Acropomatiformes (21 lineages, 306 species)

Acropomatidae (lanternbellies), Banjosidae* (banjofishes), Bathyclupeidae (deepsea herrings), Champsodontidae* (gapers), Creediidae (sand burrowers), Dinolestidae* (Long-finned Pike), Epigonidae (deepwater cardinalfishes), Glaucosomatidae* (pearl perches), Hemerocoetidae (Indo-Pacific duckbills), Howellidae (oceanic basslets), Lateolabracidae* (Asian seaperches), Malakichthyidae (temperate ocean-basses), Ostracoberycidae* (shellskin alfonsinos), Pempheridae (sweepers), Pentacerotidae (armorheads), Polyprionidae* (wreckfishes), Schuettea (moonyfishes), Scombropidae* (gnomefishes), Stereolepididae* (giant sea basses), Symphysanodontidae* (slopefishes), Synagropidae (splitfin ocean-basses).

Acropomatiformes is a recently identified group that includes 21 lineages, most of which contain only one or a few species (Davis et al. 2016a, b; Ghezelayagh et al. 2022; Smith et al. 2022). Species of Acropomatiformes inhabit nearshore and offshore marine habitats worldwide, frequently in deeper waters. They are generally schooling fishes; nearshore groups are often nocturnal (Pempheridae, Glaucosomatidae, Malakichthyidae, Dinolestidae) and several groups are bathypelagic or bathydemersal. Species of Acropomatidae, Ostracoberycidae, Symphysanodontidae, Polyprionidae, Banjosidae, Pentacerotidae, Bathyclupeidae, Synagropidae, Champsodontidae, and Malakichthyidae occur from depths of roughly 200–500 M. Species of Epigonidae and Howellidae are the deepest-dwelling acropomatiforms and can be found below 1200 M (Smith et al. 2022). Most species are laterally compressed with an ovoid to rhomboid body, a forked tail, and one or two dorsal fins (Smith et al. 2022). Some attain very large sizes (Polyprion may be as large as 2 M), others are small and burrow in sand (Creedidae, Hemerocoetidae). The most species-rich lineages of Acropomatiformes are Pempheridae (85 species) and Epigonidae (48 species; Fricke et al. 2023; Near and Thacker 2024).

Reproductive patterns are known for only a few of the acropomatiform lineages and are characterized by pelagic spawning in seasonal aggregations (Koeda et al. 2012; Coulson et al. 2016; Allen et al. 2020). Given their similar ecologies, it is likely that most of the lineages are aggregate spawners, apart from the benthic Creedidae and Hemerocoetidae. Stereolepis gigas, the Giant Sea Bass known from the kelp forests of the Eastern Pacific, aggregates to spawn in summer and produces low-frequency booming sounds by compressing the swim bladder and drumming on it with its ribs (Allen et al. 2020). These sounds are used in aggressive interactions but may also be part of courting and spawning behaviors. Several species of Pempheridae, Acropomatidae, Epigonidae, and Howellidae are bioluminescent (Thacker and Roje 2009; Davis et al. 2016a, b; Ghedotti et al. 2018; Smith et al. 2022), with light organs derived from pockets of the gut that include elaborate epithelial folds, creating chambers that host symbiotic luminescent bacteria. The fishes take up luminescent bacteria from ocean water and the light they produce is transmitted ventrally through transparent musculature (Davis et al. 2016a, b; Ghedotti et al. 2018).

The phylogenetic relationships among groups within Acropomatiformes are still uncertain; several studies have included many of the acropomatiform lineages and some of the resolved relationships are consistent, but resolution among the deepest branches and nodes of the phylogeny are poorly supported (Near et al. 2013; Thacker et al. 2015; Betancur-R et al. 2017; Satoh 2018; Oh et al. 2021). Smith et al. (2022) placed the enigmatic genus Hemilutjanus within Malakichthyidae and provided evidence that the genus Schuetta is also part of Acropomatiformes, although with uncertain phylogenetic resolution. The stem age of Acropomatiformes is estimated as 80.09 Ma (95% credible interval 73.1–88.58 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Acropomatiformes are shown in Fig. 7.

Acanthuriformes (54 families, 2,376 species)

Callanthiidae (splendid perches), Caproidae (boarfishes), Cepolidae (bandfishes), Chaetodontidae (butterflyfishes), Dinopercidae (cavebasses), Drepaneidae* (sicklefishes), Emmelichthyidae (rovers), Ephippidae (spadefishes and batfishes), Gerreidae (mojarras), Haemulidae (grunts), Leiognathidae (ponyfishes), Lethrinidae (emporer snappers), Lobotidae (tripletails and tigerperches), Lutjanidae (snappers), Malacanthidae (tilefishes), Monodactylidae (moonies), Moronidae (temperate basses), Nemipteridae (threadfin breams and spinycheeks), Pomacanthidae (angelfishes), Priacanthidae (bigeyes), Scatophagidae (scats), Sciaenidae (croakers and drums), Siganidae* (rabbitfishes), Sillaginidae (sillagos), Sparidae (porgys and seabreams).

Acanthuroidei: Acanthuridae (surgeonfishes and unicornfishes), Luvaridae* (Louvar), Zanclidae* (Moorish Idol).

Lophioidei: Antennariidae (Fibonacci frogfishes), Caulophrynidae (fanfins), Centrophrynidae* (Prickly Seadevil), Ceratiidae (seadevils), Chaunacidae (sea toads), Diceratiidae (doublespine seadevils), Gigantactinidae (whipnose seadevils), Himantolophidae* (footballfishes), Linophrynidae (leftvent seadevils), Lophichthyidae* (Boschma’s Frogfish), Lophiidae (goosefishes), Melanocetidae* (black seadevils), Neoceratiidae* (Spiny Seadevil), Ogcocephalidae (batfishes), Oneirodidae (dreamers), Thaumatichthyidae (wolftrap seadevils).

Tetraodontoidei: Aracanidae (deepwater boxfishes), Balistidae (triggerfishes), Diodontidae (porcupinefishes and burrfishes), Molidae (ocean sunfishes), Monacanthidae (filefishes), Ostraciidae (boxfishes), Tetraodontidae (puffers), Triacanthidae (triplespines), Triacanthodidae (spikefishes), Triodontidae* (Threetooth Puffer).

Acanthuriformes contains many of the larger-bodied shore and reef fishes including well-known food fish species of Lutjanidae, Haemulidae, Sparidae, and Sciaenidae, as well as Tetraodontoidei and its sister clade Lophioidei. Their body shape is generally either laterally compressed, robust, and often oblong or rounded in profile with a single dorsal fin, or else globose, rectangular, or trapezoidal, as seen in Tetraodontoidei and Lophioidei (Hastings et al. 2014). The unusual shapes in Tetraodontoidei are complemented by the presence of thickened skin ornamented in many species with scales modified into plates or spines. Species of Tetraodontidae and Diodontidae can inflate their bodies by rapidly suctioning water into the stomach as a defense mechanism (Matsuura 2015b); in Diodontidae, this causes the strong spines covering the body to project outwards. Acanthuriformes also includes the reef fish groups Acanthuridae, Chaetodontidae, Pomacanthidae, and Zanclidae, as well as the viscerally bioluminescent, sexually dimorphic Leiognathidae (Sparks and Dunlap 2004; Chakrabarty et al. 2011) and venomous Siganidae (Smith and Wheeler 2006). All inhabit marine environments except for a few lineages in fresh and brackish water. The most species-rich lineages in Acanthuriformes are Sciaenidae (298 species), Tetraodontidae (193 species), and Sparidae (164 species; Fricke et al. 2023; Near and Thacker 2024).

Reproductive patterns among acanthuriform lineages, where documented, generally involve high fecundity and pelagic spawning in small to large aggregations, often with courtship behaviors and in a few lineages with subsequent parental care of the eggs. The spawning aggregations may involve thousands of individuals migrating to spawning grounds, occur in synchrony with lunar or seasonal cycles, and be specifically triggered to time of day by light levels (Colin and Clavijo 1988; Myrberg et al. 1988). Species of Tetraodontoidei also aggregate to spawn, particularly the larger pelagic species such as molas and sunfishes (Hellenbrecht et al. 2019). Species of Tetraodontidae, Monacanthidae, and Balistidae spawn in pairs or small harems on the substrate, in some cases depositing eggs in or on the sand, in others building and guarding complex radial sand nests (Kawase 2002; Matsuura 2015a; Kawase et al. 2017). Sequential hermaphroditism, generally protogynous or protandrous but sometimes bidirectional, is common among species of Pomacanthidae, Nemipteridae, Lethrinidae, Sparidae, and Balistidae (Kuwamura et al. 2020). Species of Lophioidei are all sexually dimorphic, with males much smaller than females (Pietsch 2009; Pietsch et al. 2013; Pietsch and Arnold 2020). Reproduction in Lophioidei ranges from free spawning onto the substrate or into the water column, to benthic egg guarding in a nest, and in a few frogfish species, brooding of the eggs in the pectoral fins, a pocket formed by curling the dorsal, caudal, and anal fins, or on the flanks of the female (Mori et al. 2022). Eggs are laid in a gelatinous mass (Pietsch and Arnold 2020). The deep sea anglerfishes are known for the extreme and unique system of miniaturized, parasitic males which attach to and fuse with the much larger females, acting as an external testis. This strategy is present in species of Ceratiidae, Linophrynidae, and Neoceratiidae (Pietsch 2009; Brownstein et al. 2024).

Phylogenies of Acanthuriformes have been inferred as part of larger molecular phylogenetic studies (Holcroft and Wiley 2008; Betancur-R et al. 2013; Hughes et al. 2018; Ghezelayagh et al. 2022) and they agree in resolving Caproidae as the sister lineage of a crown clade containing Lophioidei and Tetraodontoidei. The remaining acanthuriform lineages are resolved in a pectinate pattern with shallow internodes along the backbone of the phylogeny. Clades consistently resolved in molecular phylogenetic analyses with the densest taxon sampling include a clade containing Acanthuridae, Luvaridae, and Zanclidae (Acanthuroidei); the resolution of Chaetodontidae and Leiognathidae as sister taxa; and a clade containing Nemipteridae, Lethrinidae, and Sparidae (Betancur-R et al. 2013; Ghezelayagh et al. 2022). The phylogenetic resolution of Gerreidae is particularly controversial, with Ghezelayagh et al. (2022) placing it as the sister lineage to all other Acanthuriformes, however Betancur-R et al. (2013) and Hughes et al. (2018) resolved it outside of Acanthuriformes. The most detailed phylogenetic work has been in studies focusing on the relationships of Acanthuridae, Chaetodontidae, Leiognathidae, Pomacanthidae, Lutjanidae, Haemulidae, Sciaenidae, Nemipteridae, Lethrinidae, and Sparidae.

Time-calibrated phylogenetic relationships within the reef-associated Acanthuridae, Chaetodontidae, and Pomacanthidae estimate the origin of Acanthuridae at 54 Ma in the Eocene (Sorenson et al. 2013). Similarly, the colorful, disc shaped Chaetodontidae have an Eocene origin, with slightly different root age estimates (50–54 Ma) obtained in different studies (Fessler and Westneat 2007; Bellwood et al. 2009), followed by intrafamilial divergences throughout the Miocene approximately 14–24 Ma and young endemic species in the Red and Arabian Seas arising with the invasion of deeper reef habitats (Cowman and Bellwood 2011; DiBattista et al. 2018). Relaxed molecular clock analyses of Pomacanthidae place the origin of the group in the Eocene (52 Ma in Gaither et al. 2014), with diversification among lineages spanning the Oligocene and Miocene. Biogeographic reconstructions indicate a Pacific origin for Pomacanthidae, with lineage diversification coinciding with the Miocene Terminal Tethyan Event and fragmentation of Indo-Pacific reef habitats as well as repeated independent invasions of the Atlantic and Eastern Pacific along different routes (Bellwood et al. 2004; Baraf et al. 2019). Species of Pomacanthidae as well as Chaetodontidae, Acanthuridae, Balistidae and Tetraodontidae hybridize in the Eastern Indian Ocean at both Christmas and Cocos-Keeling Islands, areas of secondary contact between fishes inhabiting the Indian and Pacific Oceans (Hobbs et al. 2009; Hobbs and Allen 2014; DiBattista et al 2016). Pairs of species in Acanthuriformes dominate the hybrid combinations found in those areas, although some Labridae (Labriformes), Pomacentridae (Blenniiformes), and Serranidae (Perciformes) also hybridize there (Hobbs and Allen 2014).

Molecular phylogenetic hypotheses for Sparidae, Lethrinidae, and Nemipteridae have facilitated an untangling of long-standing taxonomic issues and identifying convergence among morphological characters (Chiba et al. 2009; Hung et al. 2017; Chen and Borsa 2020). Phylogenetic studies of Lutjanidae, Haemulidae, and Sciaenidae have also addressed taxonomic questions (Sanciangco et al. 2011; Lo et al. 2017; Veneza et al. 2019; da Silva et al. 2023) as well as inferring divergence times. Compared to other acanthuriform lineages, relatively old stem (~ 62 Ma) and crown (~ 54 Ma) ages are inferred for species of Lutjanidae, which occupy habitats ranging from estuaries, through shallow reef and near-reef habitats, to shelf habitats of 200 M depth or more (Frédérich and Santini 2017), and so are less tightly dependent on reef habitats than species of Acanthuridae, Chaetodontidae, or Pomacanthidae.

Relaxed molecular clock analyses estimate an origin of Haemulidae in the Eocene (55 to 42 Ma) followed by radiation of the relatively species-rich lineages in the Oligocene, 25 to 30 Ma (Tavera et al. 2018). Species of Haemulidae also occupy a variety of habitats, including soft bottomed sand or mud as well as harder substrates including rocks and reef. The soft bottom habitat is ancestral for Haemulidae, with invasions of rocky and reef habitats occurring in three clades independently (Price et al. 2012). A time-calibrated molecular phylogeny of Sciaenidae reveals repeated transitions between marine, estuarine and freshwaters with an estimated crown age of 27.3 Ma (Oligocene) for the group, with divergences among major lineages taking place throughout the Miocene (Lo et al. 2015). Sciaenidae is inferred to have originated in the Eastern Pacific or Western Atlantic, followed by eastward expansion into the Eastern Atlantic and Indo-Pacific; the Indo-Pacific is the current area of greatest species diversity of sciaenids (Lo et al. 2015). Haemulidae and Sciaenidae are closely related and both produce sounds, although the mechanisms of sound generation differ. Haemulidae grunt by grinding their pharyngeal teeth (Tavera et al. 2018) and Sciaenidae croak or drum using vibration of muscles against the swim bladder, which functions as a resonance chamber (Lo et al. 2015).

The crown clade in Acanthuriformes consists of Tetraodontoidei and Lophioidei. This clade includes the globose Tetraodontidae, Triodontidae, and Diodontidae; the laterally compressed, rhomboid Balistidae, Monacanthidae, Triacanthodidae, Triacanthidae, and Molidae; the rectangular Aracanidae and Ostraciidae; the shallow benthic Antennariidae, Lophichthyidae, and Ogcocephalidae; the deep water benthic Lophiidae; and twelve lineages of deep sea anglerfishes, mostly spherical to oblong, drably colored, with reduced eyes and weak ossification (Pietsch 2009; Hastings et al. 2014). All Lophioidei (except for Neoceratias) are equipped with a highly modified first dorsal spine used for attracting prey, placed on the midline near the eyes and composed of a line (illicium) and a terminal lure (esca). The escas of Antennariidae, Lophichthyidae, Lophiidae, and Ogcocephalidae range in size from small knobs to enlarged frilly or worm-shaped structures; the escas of the deep sea anglerfishes also range from small to elaborate and are bioluminescent, hosting symbiotic bacteria (Pietsch 2009; Pietsch and Arnold 2020). Species of Antennariidae are ambush predators, covered with skin flaps and patterns that make them highly camouflaged on the substrate (Arnold and Pietsch 2012). They use their illicium to attract prey which they then consume with extremely rapid suction (Pietsch and Arnold 2020). Relationships among lineages within Lophioidei have been inferred in comprehensive molecular phylogenies (Miya et al. 2010; Near et al. 2013; Betancur-R et al. 2017; Rabosky et al. 2018; Ghezelayagh et al. 2022; Hart et al. 2022), and those studies generally concur in recovering Lophiidae as sister to the remaining families, a close relationship between Antennariidae (encompassing the lineages Brachionichthyidae, Tetrabrachiidae, Histiophrynidae, Rhycheridae, and Tathicarpidae as used in Hart et al. 2022) and Ogcocephalidae, and Chaunacidae as sister to the deep sea anglerfish lineages.

Phylogenies of Tetraodontoidei mostly agree in recovering several clades: sister lineages of Triacanthidae and Triacanthodidae; Diodontidae and Tetraodontidae; Balistidae and Monacanthidae; and Aracanidae and Ostraciidae. Phylogenies differ on the resolutions among those clades, and in the placements of Triodontidae and Molidae (Alfaro et al. 2007; Near et al. 2013; Santini et al. 2013; Matsuura 2015b; Betancur-R et al. 2017; Arcila and Tyler 2017; Ghezelayagh et al. 2022; Troyer et al. 2022). The stem age of Acanthuriformes is estimated as 80.09 Ma (95% credible interval 73.1–88.58 Ma) based on Bayesian analysis of ultraconserved element sequence data (Ghezelayagh et al. 2022). Phylogenetic relationships among the living lineages of Acanthuriformes are shown in Fig. 8.

Fig. 8

Phylogenetic relationships among the living lineages of Acanthuriformes (modified from Fig. 20 of Near and Thacker 2024)

Discussion

The phylogenetic pattern of acanthopterygian evolution is characterized by a mosaic distribution of notable traits with few broad trends. Features such as cutaneous and visceral bioluminescence, venom, specializations in the oral and pharyngeal jaws, complex mutualisms, muscular electrogenesis and thermogenesis, sound production, and various reproductive and parental care behaviors have arisen repeatedly throughout the entire radiation (Hanel et al. 2002; Little et al. 2010; Wainwright et al. 2012; Davis et al. 2016a, b; Smith et al. 2016). Acanthopterygian lineages have evolved in concert with their habitats and shifting continental landscapes, in particular the multiple transitions between shallow and deep seas, tropical and polar latitudes, marine and freshwater, and the long coevolution of fishes on reefs (Cowman and Bellwood 2011, 2013a, 2013b; Brandl et al. 2018; Rabosky et al. 2018; Capobianco and Friedman 2019; Miller et al. 2022). Of the 16 acanthopterygian clades, five are exclusively marine (Beryciformes, Trachichthyiformes, Scombriformes, Labriformes, Acropomatiformes,), five are primarily marine with a few freshwater lineages (Ophidiiformes, Batrachoididae, Syngnathiformes, Carangiformes, Acanthuriformes), five have significant representation in both marine and freshwater (Gobiiformes, Atheriniformes, Blenniiformes, Perciformes, and Centrarchiformes) and Synbranchiformes is unique in almost exclusively occupying freshwater habitats. Synbranchiformes is also the only acanthopterygian clade that does not have a worldwide distribution, inhabiting primarily Asia, Africa, Australia, and islands of the Indo-Pacific, with only a few lineages in the Neotropics. All acanthopterygian clades are found in tropical and temperate habitats, but in polar regions the primary representatives are several lineages of Perciformes. Arctic and Antarctic habitats each host a variety of Cottoidea and Zoarcoidea, and in Antarctic seas the primary acanthopterygian representatives are the icefishes, dragonfishes and plunderfishes in Notothenioidei (Near et al. 2012a; Rabosky et al. 2018).

Acanthopterygian clades have radiated globally throughout their history, successfully dispersing by means of nearly every potential aquatic pathway. Biogeographic analyses of acanthopterygian groups usually infer multiple invasion events into and out of newly occupied regions, with even sporadic long-distance dispersal events becoming likely over long timescales. The only biogeographic pattern that has been refuted for acanthopterygian clades is that of Gondwanan vicariance, potentially manifesting as sister group splits between freshwater lineages in South America and Africa or evolutionary links between Africa, Asia, and Australia due to Gondwanan breakup and northward rafting of the Indian subcontinent. Although that mechanism is likely responsible for distributions of older linages such as Lepidosireniformes, Osteoglossiformes, and certain Ostariophysi, the acanthopterygian lineages are simply too young (Friedman et al. 2013b; Capobianco and Friedman 2019; Adamson et al. 2010; Harrington et al. 2023). Ghezelayagh et al. (2022) dates the origin of Acanthopterygii at 145 Ma in the earliest Cretaceous, with the major acanthopterygian clades arising throughout the Cretaceous between 137 and 80 Ma. With all of the major acanthopterygian clades established prior to the Cretaceous/Paleogene boundary, evolution within those clades would primarily be affected by Cenozoic events such as the Paleocene-Eocene Thermal Maximum (a period of global elevated temperatures and ocean acidification around 55 Ma), global cooling and collapse of the West Tethys coral reef hotspot (late Eocene/early Oligocene, approximately 33 Ma) and eastward movement of the center of coral reef diversity into the Coral Triangle, the Terminal Tethyan Event separating the Mediterranean/Atlantic from the Indian Ocean due to the collision of Africa with Eurasia (12–18 Ma), the closure of the Isthmus of Panama separating the Western Atlantic from the Eastern Pacific (3.1 Ma), and the sea level fluctuations induced by glaciation cycles throughout the Pleistocene (Renema et al. 2008; Cowman and Bellwood 2011, 2013a, 2013b; Price et al. 2015; Thacker 2015, 2017; Arcila and Tyler 2017; Shelley et al. 2020c).

Species diversity among acanthopterygian clades varies widely. Blenniiformes (3,814 species) is the most species-rich, followed by Perciformes (3,200 species), Gobiiformes (2,740 species), Acanthuriformes (2,376 species) and Atheriniformes (2,126 species) (Fig. 9). The most species-depauperate lineages are Trachichthyiformes (71 species) and Batrachoididae (84 species), followed by Beryciformes (213 species) and Scombriformes (287 species). No phylogenetic pattern in diversity is apparent; high and low species diversity clades are interspersed throughout the phylogeny.

Fig. 9

Percentage of total species diversity in each acanthopterygian clade

The phylogenetic relationships of Acanthopterygii inferred based on molecular data accord in many respects with those derived from morphology (Lauder and Liem 1983; Johnson 1993; Johnson and Patterson 1993) but they include several notable differences. The reallocation of Lophioidei from Paracanthopterygii into crown group Acanthuriformes as sister to Tetraodontoidei is the most dramatic and yields a novel framework for evaluating the evolution of both body shape and depth preferences among anglerfishes and pufferfishes (Dornburg and Near 2021; Miller et al. 2022, 2023; Brownstein et al. 2024). Similarly, Atheriniformes has historically been placed outside Percomorpha but modern analyses resolve it as sister to Blenniiformes (Lauder and Liem 1983). A long-held placement of tunas and billfishes as sisters was disconfirmed with the resolution of Xiphiidae and Istiophoridae in Carangiformes, prompting a reinterpretation of the evolution of endothermy (Orrell et al. 2006; Little et al. 2010). Carangiformes also contains Pleuronectoidei, the flatfishes, and the juxtaposition of these groups contextualizes the unique modifications of flatfish evolution (Harrington et al. 2016, 2021).

The molecular revolution in acanthopterygian phylogeny has provided detailed resolution of relationships and yielded a rich and comprehensive portrait of acanthopterygian evolution. Although some uncertainties remain such as the placements of Ovalentaria and the clade containing Scombriformes and Syngnathiformes, the interrelationships of clades within Eupercaria, and the resolution of lineages within Perciformes, Acanthuriformes, Scombriformes, and Belonoidei, the overall pattern of acanthopterygian phylogeny is consistent and well-resolved (Near et al. 2012b, 2013; Betancur-R et al. 2013, 2017; Faircloth et al. 2013; Alfaro et al. 2018; Hughes et al. 2018; Rabosky et al. 2018; Dornburg and Near 2021; Ghezelayagh et al. 2022). In particular, the resolution of lineages previously assigned to Perciformes into nearly every other major acanthopterygian clade is a remarkable advance in the phylogenetics of vertebrates (Dornburg and Near 2021; Near and Thacker 2024). Understanding of the components and interrelationships of large clades including Acanthuriformes, Perciformes, and Blenniiformes, as well as identification of previously unrecognized groups such as Acropomatiformes, is foundational for inferences of evolutionary processes and patterns across Acanthopterygii. With this clear structuring of acanthopterygian diversity, centuries of morphological descriptions may be reinterpreted in an evolutionary context as well as augmented with modern techniques that provide detailed resolution of anatomical structures such as CT scanning.

Future investigations into acanthopterygian evolution will rely on a consilience of data from paleontology, morphology, and molecular phylogenetics. With the relationships established by molecular phylogenies, calibrations and phylogenetic refinements provided by the inclusion of fossils, and phylogenetically informed techniques to infer patterns of biogeography, phenotypic trait evolution, and global biogeography, a comprehensive, detailed portrait of acanthopterygian fish evolution is developing (Thacker 2015; Rabosky et al. 2018; Ghezelayagh et al. 2022; Brownstein et al. 2024). However, molecular data are finite; as techniques that enable the near-complete sequencing of genomes become more available, the inference of molecular phylogeny may reach an inflection point beyond which no further resolution may be obtained. Molecular data are also susceptible to convergence in functionally critical genes as well as saturation, particularly over deep timescales (Duarte-Ribeiro et al. 2024). Even with extensive phylogenomic data, some areas of the acanthopterygian tree will likely remain poorly resolved, and some polytomies are likely accurate representations of rapid diversification. Potential solutions could include increase in the use of fossil taxa, both as cross-checks on the sequence of lineage appearance as well as direct inclusion of fossil species in tip-dating analyses. Analysis of genome morphology (gene order, chromosomal configuration, and synteny patterns) may also hold promise in revealing evolutionary relationships over long timescales. Research into fish phylogeny and evolution is currently at a tipping point due to a convergence of centuries of morphological work with vast advances in molecular phylogenetics, analysis techniques, fossil discoveries and the extraction of new data from old fossils. It is from the integration of all these data types that a complete portrait of spiny-rayed fish evolution, distribution, and diversification will emerge.