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.2016 Oct 11;113(41):11531-11536.
doi: 10.1073/pnas.1607237113. Epub 2016 Sep 26.

Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group

Affiliations

Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group

John T Clarke et al. Proc Natl Acad Sci U S A..

Abstract

Since Darwin, biologists have been struck by the extraordinary diversity of teleost fishes, particularly in contrast to their closest "living fossil" holostean relatives. Hypothesized drivers of teleost success include innovations in jaw mechanics, reproductive biology and, particularly at present, genomic architecture, yet all scenarios presuppose enhanced phenotypic diversification in teleosts. We test this key assumption by quantifying evolutionary rate and capacity for innovation in size and shape for the first 160 million y (Permian-Early Cretaceous) of evolution in neopterygian fishes (the more extensive clade containing teleosts and holosteans). We find that early teleosts do not show enhanced phenotypic evolution relative to holosteans. Instead, holostean rates and innovation often match or can even exceed those of stem-, crown-, and total-group teleosts, belying the living fossil reputation of their extant representatives. In addition, we find some evidence for heterogeneity within the teleost lineage. Although stem teleosts excel at discovering new body shapes, early crown-group taxa commonly display higher rates of shape evolution. However, the latter reflects low rates of shape evolution in stem teleosts relative to all other neopterygian taxa, rather than an exceptional feature of early crown teleosts. These results complement those emerging from studies of both extant teleosts as a whole and their sublineages, which generally fail to detect an association between genome duplication and significant shifts in rates of lineage diversification.

Keywords: fossil record; genome duplication; morphological diversification; neopterygian; phylogeny.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Phenotypic variation in early crown neopterygians. (A) Total-group holosteans. (B) Stem-group teleosts. (C) Crown-group teleosts. Taxa illustrated to scale.
Fig. 2.
Fig. 2.
(A) Morphospace of Permian–Early Cretaceous crown Neopterygii. (B) One supertree subjected to our paleontological (Upper) and molecular (Lower) timescaling procedures to illustrate contrasts in the range of evolutionary timescales considered. Colors of points (A) and branches (B) indicate membership in major partitions of neopterygian phylogeny. Topologies are given in Datasets S4 and S5. See Dataset S6 for source trees.
Fig. S1.
Fig. S1.
Morphospace of 398 Permian–Early Cretaceous Neopterygii. Three major axes of shape variation are presented. Silhouettes and accompanying arrows illustrate the main anatomical correlates of these principal axes, as described in Table S3. Actual fossil specimens represented in the dataset are also displayed to visualize the extremities of morphospace axes. Fossil taxa as follows: (a)Bavarichthys incognitus; (b)Ellimmichthys longicostatus; (c)Turbomesodon relegans; (d)Allothrissops salmoneus; (e)Pholidophorus germanicus; (f)Macrosemius fourneti.
Fig. S2.
Fig. S2.
Morphospace of 398 Permian–Early Cretaceous Neopterygii, illustrating the major clades of (A) teleosts and (B) holosteans.
Fig. S3.
Fig. S3.
Comparisons of size rates between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Identical taxon sampling leads the CS and pruned SL datasets to yield near identical results. Although the larger SL dataset results often differ slightly, the overall conclusion from each pairwise comparison (i.e., which outcome is the most likely in an overall majority of trees) is identical in all but one comparison (E, under molecular timescales).
Fig. S4.
Fig. S4.
Comparisons of size innovation between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Comparisons of size innovation are presented forK value distributions of the three datasets resemble each other closely.
Fig. 3.
Fig. 3.
Comparisons of phenotypic rate and innovation between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, and (C) crown teleosts and stem teleosts. Rate results are conveyed with pie charts, where the proportion of sampled supertrees in support of significantly higher rates (as determined from two-wayP values with α = 0.05) in a given neopterygian partition are color coded to match that partition; white sections correspond to supertrees indicating no significant rate differences. Violin plots capturing the distribution ofK values obtained from 100 sampled supertrees allow for investigation of innovation. HigherK values suggest greater phylogenetic signal, and correspondingly, greater innovation, in contrast to the iterative “rediscovery” of similar phenotypes (Methods).K interpretations are contextualised with rate in Table S1.
Fig. S5.
Fig. S5.
Comparisons of phenotypic rate and innovation between (A) holosteans and crown teleosts; (B) holosteans and stem teleosts. Rate results are conveyed with pie charts, where the proportion of sampled supertrees in support of significantly higher rates (as determined from two-wayP values with α = 0.05) in a given neopterygian partition are color-coded to match that partition; white sections correspond to supertrees indicating no significant rate differences. Violin plots capturing the distribution ofK values obtained from 100 sampled supertrees allow for investigation of innovation. HigherK values suggest greater phylogenetic signal, and correspondingly, greater innovation, in contrast to the iterative “rediscovery” of similar phenotypes (Methods).K interpretations are contextualized with the rate in Table S1.
Fig. S6.
Fig. S6.
Landmark scheme used to quantify shape. Fixed landmarks are marked by red circles; semilandmarks are marked by black circles with white fill. Red circles containing a white asterisk act as anchor points for the semilandmarks in-between. Fixed landmarks document: 1) anterior tip of the upper jaw (premaxilla); 2) the central, ventral surface of the orbit; 3) the center of the orbit; 4) the central, dorsal surface of the orbit; 5) the dorsal surface of the skull immediately above the eye; 6) postero-dorsal tip of braincase; 7) anterior insertion of dorsal fin; 8) posterior insertion of dorsal fin; 9) dorsal surface representation of the last vertebral centra; 10) ventral surface representation of the last vertebral centra; 11) posterior insertion of anal fin; 12, anterior insertion of anal fin; 13) anterior insertion of the pelvic fin; 14) anterior insertion of the pectoral fin; 15) lower jaw joint. Landmarked specimen isAmiopsis lepidota (SMNS 80251) from the Staatliches Museum für Naturkunde, Stuttgart.
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