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Phylogeny and Tempo of Diversification in the Superradiation

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Phylogeny and Tempo of Diversification in the Superradiation Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes Thomas J. Neara,1, Alex Dornburga, Ron I. Eytana, Benjamin P. Keckb, W. Leo Smithc, Kristen L. Kuhna, Jon A. Moored, Samantha A. Pricee, Frank T. Burbrinkf, Matt Friedmang, and Peter C. Wainwrighte aDepartment of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, CT 06520; bDepartment of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996; cDivision of Fishes, The Field Museum, Chicago, IL 60605; dWilkes Honors College and Harbor Branch Oceanographic Institution, Florida Atlantic University, Jupiter, FL 33458; eDepartment of Evolution and Ecology, University of California, Davis, CA 95616; fBiology Department, College of Staten Island/City University of New York, Staten Island, NY 10314; and gDepartment of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom Edited by David M. Hillis, University of Texas at Austin, Austin, TX, and approved June 14, 2013 (received for review March 11, 2013) Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third “a bush at the top” of the teleost tree in reference to the his- of all living vertebrates. Despite their dominant role in aquatic torical lack of resolution of its basic phylogenetic intrarelation- ecosystems, the evolutionary history and tempo of acanthomorph ships (12). Studies using morphological and molecular datasets diversification is poorly understood. We investigate the pattern of offer alternative perspectives on the evolutionary relationships of lineage diversification in acanthomorphs by using a well-resolved acanthomorphs (6, 8, 13–15). Molecular phylogenies support the time-calibrated phylogeny inferred from a nuclear gene super- monophyly of several traditionally recognized taxonomic groups matrix that includes 520 acanthomorph species and 37 fossil age of percomorphs as well as the resolution of several novel clades constraints. This phylogeny provides resolution for what has been (13, 14, 16–19); however, a consistent and well-supported reso- classically referred to as the “bush at the top” of the teleost tree, and lution of the phylogenetic relationships among these major indicates acanthomorphs originated in the Early Cretaceous. Pale- groups has eluded the scientific community. ontological evidence suggests acanthomorphs exhibit a pulse of In addition to the uncertainty surrounding phylogenetic rela- morphological diversification following the end Cretaceous mass tionships, there are conflicting observations from molecular extinction; however, the role of this event on the accumulation of phylogenies and the fossil record regarding the temporal history EVOLUTION living acanthomorph diversity remains unclear. Lineage diversifica- of acanthomorph diversification (20). Recent analyses of lineage tion rates through time exhibit no shifts associated with the end diversification using time-calibrated molecular phylogenies Cretaceous mass extinction, but there is a global decrease in lineage identified an unnamed subclade of percomorphs, with an esti- fi diversi cation rates 50 Ma that occurs during a period when mor- mated age of ∼110 Ma (9–11, 19), as exhibiting a shift to an phological disparity among fossil acanthomorphs increases sharply. exceptionally high lineage diversification rate (10, 11). In con- fi fi Analysis of clade-speci c shifts in diversi cation rates reveal that trast, acanthomorph and percomorph species preserved in the the hyperdiversity of living acanthomorphs is highlighted by several fossil record show relatively little morphological disparity rapidly radiating lineages including tunas, gobies, blennies, snail- through the Late Cretaceous, but extensive expansion of mor- fishes, and Afro-American cichlids. These lineages with high diver- – fi phospace from the Cretaceous Paleogene (K-Pg) boundary to si cation rates are not associated with a single habitat type, such as the early Eocene (7). The signature of increased morphological coral reefs, indicating there is no single explanation for the success disparity in the fossil record of acanthomorphs was interpreted in of acanthomorphs, as exceptional bouts of diversification have the context of recovery from the K-Pg mass extinction event (7). occurred across a wide array of marine and freshwater habitats. These two results indicate that the timing of a shift to an in- creased lineage diversification rate in acanthomorphs is at least Actinopterygii | Cichlidae | Percomorpha | Teleostei 45 My older than the expansion of morphological disparity. However, the taxon sampling in the molecular time tree analyses fi ith more than 18,000 species, acanthomorph shes com- were designed to assess patterns of diversification among more – Wprise almost one-third of living vertebrates (1 3). Acan- inclusive vertebrate lineages, and did not target specific acan- fi thomorphs, or spiny-rayed shes, are present in nearly all marine thomorph clades that may have diversified around the K-Pg (10, and freshwater habitats from tropical coral reefs, freezing waters 11). Despite these important observations, it is not known how around Antarctica, alpine mountain lakes, and hadal trenches in ’ the K-Pg mass extinction event affected the accumulation of the deepest parts of the world s oceans known to harbor animal lineage diversity in acanthomorphs, or if there are global shifts in life (2). Acanthomorphs exhibit substantial morphological dispar- rates of lineage origination coincident with the increase of mor- ity, with body plans as diverse as flatfishes, pufferfishes, sword- fi fl fi phological disparity following the K-Pg. shes, seahorses, and ying shes (3), and adult body sizes that We investigated the timing and tempo of acanthomorph di- range from among the smallest of all vertebrates to the largest versification by using a time-calibrated molecular phylogeny inferred bony fishes (4, 5). In addition, acanthomorphs include some of the most economically and scientifically important fish species, such as cods, tunas, sticklebacks, and cichlids. Investigating the Author contributions: T.J.N., A.D., R.I.E., W.L.S., J.A.M., M.F., and P.C.W. designed re- processes that have resulted in the success of acanthomorphs is search; T.J.N., A.D., R.I.E., B.P.K., W.L.S., K.L.K., J.A.M., S.A.P., F.T.B., M.F., and P.C.W. key to understanding the origins of the rich biodiversity of living performed research; T.J.N., A.D., R.I.E., B.P.K., K.L.K., S.A.P., F.T.B., M.F., and P.C.W. ana- vertebrates. lyzed data; and T.J.N., A.D., R.I.E., and P.C.W. wrote the paper. Resolution of the phylogenetic relationships among acantho- The authors declare no conflict of interest. morphs, particularly the species-rich Percomorpha, has ranked This article is a PNAS Direct Submission. among the most important and vexing problems in vertebrate Freely available online through the PNAS open access option. – biology (3, 6 9). High species richness in particular has posed Data deposition: The sequences reported in this paper have been deposited in the a challenge to investigating relationships of the group. For ex- GenBank database (accession nos. KF139346–KF141634). ample, Percomorpha contains more than 17,000 species, has 1To whom correspondence should be addressed. E-mail: [email protected]. been shown to exhibit exceptional species richness relative to This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. other lineages of jawed vertebrates (10, 11), and is described as 1073/pnas.1304661110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1304661110 PNAS Early Edition | 1of6 Downloaded by guest on September 23, 2021 by using 10 nuclear genes sampled from 579 species that included the molecular phylogeny with the teleost fossil record provides im- 520 acanthomorphs, representing all major lineages and tradition- portant insights into the timing and tempo of acanthomorph di- ally recognized taxonomic orders and suborders (2). The analyses of versification. A set of time-calibrated phylogenies were estimated diversification rates through time in acanthomorphs are analyzed in using Bayesian methods and 37 well-justified fossil-based prior age the context of the K-Pg mass extinction event and the timing of constraints that included 33 acanthomorph taxa, of which 24 were morphological expansion detected in the fossil record. We also in- percomorphs (SI Text), ranging from Early Cretaceous (∼134 Ma) to vestigate clade-specific shifts in diversification rates, which identify Miocene (∼12 Ma) in age. The estimated ages of Acanthomorpha, several percomorph lineages that exhibit exceptionally high rates of between 133 and 152 Ma, and Percomorpha, between 109 and 120 lineage accumulation. Our results provide a phylogenetic and tem- Ma (Table S1), are consistent with those implied by the fossil record poral perspective from which to investigate the evolutionary pro- and previous molecular clock analyses (7, 9–11, 25). Major non- cesses that resulted in the origin of one of the most species rich percomorph acanthomorph lineages, such as the Beryciformes, clades of living vertebrates. originate in the Cretaceous (Figs. 1 A and B and 2A). However, we find no clear signature of lineage origination centered on the K-Pg Results and Discussion because many percomorph lineages predate or postdate the age of The supermatrix of 10 combined nuclear genes is 84.5% com- the mass extinction event (Figs. 1A and 2A and Table S1). For plete, with the proportion of missing taxa among the 10 genes example,
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