COMMENTARY Resolving the ray-finned fish tree of life COMMENTARY Michael E. Alfaroa,1 The Challenge of Reconstructing Fish Phylogeny responsible for generating the trees in the first place When it comes to vertebrate evolutionary history, has emerged. In PNAS, Hughes et al. (12), use over our understanding of lobe-finned fishes—the branch 1,000 new markers using phylogenomic and tran- of the vertebrate tree leading to coelacanths plus scriptomic techniques to reconstruct the evolutionary the tetrapods (amphibians, turtles, birds, crocodiles, history of ray-finned fishes. Hughes et al.’s phylogeny lizards, snakes, and mammals)—far outstrips our reveals many key features of the backbone of the ray- knowledge of ray-finned fishes (Actinopterygii). Acti- finned fish tree of life and provides the most com- nopterygians exhibit extraordinary species richness prehensive evolutionary framework to date for this (>33,000 described species) and have evolved a stag- major radiation of vertebrates. gering diversity in morphology and ecology over their Phylogenomics has revolutionized evolutionary 400+ million y history. Ray-finned fishes include some reconstruction by vastly expanding both the number of the smallest vertebrates [the adult cyprinid Paedo- of loci that can be interrogated across nonmodel or- cypris progenetica measure just under 8 mm (1)], some ganisms, as well as the efficiency with which the data of the largest (adult ocean sunfish weigh more than may be collected (13). The most recent multilocus 2,000 kg), some of the longest (oarfishes may reach a studies that underlie our current understanding of the length of more than 13 m), some of the longest lived ray-finned fish tree of life are based upon 10– [rougheye rockfishes, Sebastes aleutianus, may live for 20 markers (e.g., refs. 9 and 11). These studies rep- more than 200 y (2)], and some of the shortest lived [the resent the culmination of decades of effort to identify coral reef pygmy goby, Eviota sigillata, has a maximum genes with reasonable phylogenetic performance, as lifespan of 59 d (3)]. In marine waters, ray-finned fishes well as the laborious effort to amplify and sequence include the tremendously diverse and ecologically rich each marker for each species (14). In contrast, modern coral reef fish families, such as wrasses, angelfishes, genome sequencing and transcriptomics enable butterfly fishes, and damselfishes, and they comprise rapid and cost-effective collection of genome-scale most important commercial and recreational fishing data for any species, shifting the challenge of phylo- stocks. Within freshwaters, ray-finned fishes have genetic analysis from intensive laboratory work to produced several ecologically dominant radiations, identifying the markers that are most appropriate for including cyprinids, characiforms, catfishes, and cichlids. the questions at hand. Efforts to reconstruct the phylogenetic history of this Hughes et al. (12) introduce a pipeline that expands group have proven extremely challenging (4, 5), especially the genomic resources for phylogenetic inference in within acanthomorphs (6, 7), a hyperdiverse subclade fishes by identifying and extracting 1,105 protein comprising almost two-thirds of all ray-finned fish species. coding genes from genomic alignments. Inferring the One of the major impediments to understanding ray-finned fish tree of life using phylogenomic data is higher-level ray-finned fish relationships has been the potentially confounded by two episodes of genomic lack of obvious morphological characters that unite expansion in the history of the group (15, 16): one at major lineages (reviewed in ref. 8). Within the last 5 y, the base of all vertebrates and the second at the base large-scale multilocus sequencing efforts have pro- of all teleost fishes (a group comprising over 99% of ray- duced novel insights in the ray-finned fish backbone finned fish species). Hughes et al. (12) show that naive phylogeny, including unexpectedly close relation- phylogenomic pipelines will likely recover a significant ships among morphologically disparate lineages (9– number of paralogs that in turn may mislead evolu- 11). Testing these new hypotheses is critical for un- tionary inferences at the tree-of-life scale. By filtering derstanding vertebrate evolutionary history, yet little out gene trees that fail to recover the monophyly evidence beyond the original set of nuclear markers of three major fish groups that emerged following aDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095 Author contributions: M.E.A. wrote the paper. The author declares no conflict of interest. Published under the PNAS license. See companion article on page 6249. 1Email: [email protected]. Published online May 30, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1807018115 PNAS | June 12, 2018 | vol. 115 | no. 24 | 6107–6109 Downloaded by guest on September 24, 2021 genomic expansion events (teleosts, euteleosts, and ostar- prior divergence-time studies show that this massive radiation iophysans), Hughes et al. arrive at a final marker set for their unfolded largely over the Late Cretaceous and some have dub- analyses with maximal power to accurately reconstruct actino- bed this period the “Second Age of Fishes” (9). However, some pterygian evolutionary history. fossil and phylogenomic studies implicate the mass extinction and recovery at the K-Pg (Cretaceous–Paleogene) boundary as major Can More Markers Help Resolve Controversial Nodes and forces that restructured marine fish communities (22) and fueled Questions About the Timing of Diversification? the rise of percomorphs (23, 24). Hughes et al. (12) show that the The growth of molecular phylogenetics has led to conflicting diversification within major percomorph groups predates the K–Pg perspectives on the evolutionary relationships among several of boundary. the most distinctive lineages on the ray-finned fish tree of life. The branching arrangement of the base of the teleost tree is one such ’ area of conflict, with morphological studies generally supporting Hughes et al. s phylogeny reveals many key the elopomorphs (eels and tarpon) and osteoglossomorphs (bony features of the backbone of the ray-finned fish tongues) as successive sister lineages to remaining teleosts (4). tree of life and provides the most comprehen- This result is recovered by some multilocus (11, 17) and phylo- genomic studies (18), while others support a sister group re- sive evolutionary framework to date for this lationship between elopomorphs and osteoglossomorphs (18). major radiation of vertebrates. The arrangement of the otophysans (a species-rich clade con- taining more than two-thirds of the world’s freshwater species, The underlying causes for the discrepancy in divergence times including characins, knifefishes, minnows, and catfishes), remains estimated by these studies is not immediately clear and could highly controversial, as morphological studies unambiguously reflect differences in the rates of evolution between coding and recover the monophyly of the characiformes (19), while molecular noncoding phylogenomic markers, differences in the treatment of studies generally render this group paraphyletic with respect to fossil constrained nodes, or differences in taxonomic sampling. other otophysan lineages (20; but see ref. 21). Hughes et al. (12) However, resolution of the timing of percomorph diversification is investigate the strength of support across the genome for alter- critical to evaluating explanations for the evolutionary success of native resolutions of contentious nodes through a recently de- the groups. If the modern percomorph fauna can be linked to veloped statistical pipeline (21). The authors (12) show that for at postextinction recovery, then the mass extinction at the K–Pg was least some controversial nodes, including teleosts and otophy- key to shaping diversity across major groups of both terrestrial and sans, conflict between morphological and molecular results ap- aquatic groups today. Alternatively, if diversification happened pears to be driven by noise in some gene partitions. When only over a broader window of time that predates the mass extinction, markers with strong phylogenetic signal are considered, the fa- percomorph diversity may be better understood as a conse- vored molecular and morphological topologies are the same. quence of lineage-specific factors relating to the ecological flex- Their analysis underscores the need to consider both the strength ibility of the group as a whole (9). of support for novel phylogenetic results and the distribution of The success of multilocus studies substantially improved the that support across gene partitions in the analysis of massive next- prospects of resolving higher-level relationships among ray- generation datasets. finned fishes. In PNAS, Hughes et al. (12) deliver a significant Another vexing phylogenetic problem in vertebrate evolu- advance on this front. Their phylogeny, the most robustly sup- tionary biology concerns the percomorphs, the largest acantho- morph subclade, with over 17,000 species. Recent multilocus ported hypothesis of relationship of ray-finned fishes to date, studies (8, 11) resolve the astonishing richness of this group into provides a stable framework for understanding actinopterygian nine major lineages, including Gobiaria (gobies), Pelagiaria evolutionary history as well as a road-map for fleshing-out re- ∼ (tunas), Syngnatharia (seahorses and pipefishes), Carangaria (jacks