Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group
John T. Clarke a,b,1, Graeme T. Lloyd c, and Matt Friedman b,2
Author Affiliations
aDepartment of Earth and Environmental Science, University of Pennsylvania, Philadelphia, PA 19104-6316;
bDepartment of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom;
cDepartment of Biological Sciences, Faculty of Science, Macquarie University, North Ryde, NSW 2109, Australia
Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved August 19, 2016 (received for review May 6, 2016)
Significance
The success of teleost fishes, which represent roughly half of all vertebrate species, has attracted attention since Darwin. Numerous scenarios invoke elevated diversification in teleosts facilitated by supposed key innovations, yet claims of teleost exceptionalism are profoundly biased by the evolutionary “snapshot” of living fishes. Analysis of 160 million y (Permian–Early Cretaceous) of evolution in neopterygian fishes reveals that anatomical diversification in Mesozoic teleosts as a whole differed little from their “living fossil” holostean sister group. There is some evidence for evolutionary heterogeneity within teleosts, with early evolving lineages showing the greatest capacity for evolutionary innovation in body shape among Mesozoic neopterygians, whereas members of the modern teleost radiation show higher rates of shape evolution.
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.
neopterygian phylogeny genome duplication fossil record morphological diversification
Footnotes
1To whom correspondence should be addressed. Email: j.clarke.paleo@gmail.com.
2Present address: Museum of Paleontology and Department of Earth and Environmental Science, University of Michigan, Ann Arbor, MI 48108-1079.
Author contributions: J.T.C. and M.F. designed research; J.T.C. performed research; G.T.L. contributed new reagents/analytic tools; J.T.C. and G.T.L. analyzed data; and J.T.C., G.T.L., and M.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1607237113/-/DCSupplemental.
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