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Accelerated Diversification Explains the Exceptional Species Richness of Tropical Characoid Fishes

Melo, Bruno F, Sidlauskas, Brian L, Near, Thomas J, Roxo, Fabio F, Ghezelayagh, Ava, Ochoa, Luz E, Stiassny, Melanie L J, Arroyave, Jairo, Chang, Jonathan, Faircloth, Brant C, MacGuigan, Daniel J, Harrington, Richard C, Benine, Ricardo C, Burns, Michael D, Hoekzema, Kendra, Sanches, Natalia C, Maldonado-Ocampo, Javier A, Castro, Ricardo M C, Foresti, Fausto, Alfaro, Michael E, Oliveira, Claudio·2021·Systematic Biology
DOI 10.1093/sysbio/syab040
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Abstract

The Neotropics harbor the most species-rich freshwater fish fauna on the planet, but the timing of that exceptional diversification remains unclear. Did the Neotropics accumulate species steadily throughout their long history, or attain their remarkable diversity recently? Biologists have long debated the relative support for these museum and cradle hypotheses, but few phylogenies of megadiverse tropical clades have included sufficient taxa to distinguish between them. We used 1288 ultraconserved element loci spanning 293 species, 211 genera, and 21 families of characoid fishes to reconstruct a new, fossil-calibrated phylogeny and infer the most likely diversification scenario for a clade that includes a third of Neotropical fish diversity. This phylogeny implies paraphyly of the traditional delimitation of Characiformes because it resolves the largely Neotropical Characoidei as the sister lineage of Siluriformes (catfishes), rather than the African Citharinodei. Time-calibrated phylogenies indicate an ancient origin of major characoid lineages and reveal a much more recent emergence of most characoid species. Diversification rate analyses infer increased speciation and decreased extinction rates during the Oligocene at around 30 Ma during a period of mega-wetland formation in the proto-Orinoco-Amazonas. Three species-rich and ecomorphologically diverse lineages (Anostomidae, Serrasalmidae, and Characidae) that originated more than 60 Ma in the Paleocene experienced particularly notable bursts of Oligocene diversification and now account collectively for 68% of the approximately 2150 species of Characoidei. In addition to paleogeographic changes, we discuss potential accelerants of diversification in these three lineages. While the Neotropics accumulated a museum of ecomorphologically diverse characoid lineages long ago, this geologically dynamic region also cradled a much more recent birth of remarkable species-level diversity. [Biodiversity; Characiformes; macroevolution; Neotropics; phylogenomics; ultraconserved elements.]

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  • Although molecular phylogenetic studies have demonstrated frequent discordance between molecular data and morphological expectations, the monophyly of Siluriphysi has generally been maintained in traditional interpretations from early single-locus analyses to recent multiple genomic-scale loci, primarily to conform to morphological predictions.

    “Although numerous molecular phylogenetic studies have demonstrated frequent discordance between molecular data and morphological expectations, the monophyly of Siluriphysi has generally been maintained in traditional interpretations, from early single-locus analyses48 to recent multiple genomic-scale loci,49,50,51,52,53,54,55,56 primarily to conform to morphological predictions.”

    From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [56]

  • Some molecular phylogenetic studies failed to support Siluriphysi monophyly.

    “Nonetheless, some molecular phylogenetic studies (e.g., Figures S2, S4, and S5 in Hughes et al.’s study, and in Near et al.’s and Melo et al.’s studies)54,55,56 failed to support Siluriphysi monophyly.”

    From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [56]

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Metadata

Authors
Melo, B. F., Sidlauskas, B. L., Near, T. J., Roxo, F. F., Ghezelayagh, A., Ochoa, L. E., Stiassny, M. L. J., Arroyave, J., Chang, J., Faircloth, B. C., MacGuigan, D. J., Harrington, R. C., Benine, R. C., Burns, M. D., Hoekzema, K., Sanches, N. C., Maldonado-Ocampo, J. A., Castro, R. M. C., Foresti, F., Alfaro, M. E., & Oliveira, C.
Affiliations
  • Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University , Botucatu, SP 16818-689, Brazil
  • Wildlife and Conservation Sciences, Oregon State University Department of Fisheries, , Corvallis, OR 97331, USA
  • Yale University, New Haven Department of Ecology and Evolutionary Biology, , CT 06520, USA
  • Institute of Biosciences, São Paulo State University Sector of Zoology, , Botucatu, SP 18618-689, Brazil
  • Department of Ichthyology, American Museum of Natural History , New York, NY 10024, USA
  • Instituto de Biologiìa, Universidad Nacional Autónoma de México , Ciudad de México 04510, México
  • School of Biological Sciences, Monash University , Melbourne, VIC 3800, Australia
  • Department of Biological Sciences and Museum of Natural Science, Louisiana State University , Baton Rouge, LA 70803, USA
  • Cornell Lab of Ornithology, Cornell University Museum of Vertebrates , Ithaca, NY 14850, USA
  • Department de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana , Bogotá, DC Colombia (in memoriam)
  • Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo , Ribeirão Preto, SP 14040-901, Brazil
  • Department of Ecology and Evolutionary Biology, University of California , Los Angeles, CA 90095, USA
Venue
Systematic Biology
Publisher
Oxford University Press (OUP)
Published
2021-06-07
Volume
71
Issue
1
Pages
78-92
ISSN
  • 1063-5157
  • 1076-836X
DOI
10.1093/sysbio/syab040
Cited by
93
References
3
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Funders
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (16/11313-8, 18/24040-5, 14/05051-5, 15/00691-9, 14/06853-8, 18/23883-9, 14/26508-3)
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (404991/2018-1, 200159/2020-8, 307975/2019-3, 306054/2006-0)
  • National Science Foundation (1257898, DEB-165594, DEB-1601830, DEB-1242267)
  • Bingham Oceanographic Fund
  • Peabody Museum of Natural History, Yale University
  • National Institute of Health Predoctoral Training Program in Genetics (T32 GM 007499)
  • AMNH Axelrod Research Curatorship
  • Edward W. Rose Postdoctoral Fellowship
  • Cornell Lab of Ornithology
  • Programa de Pós-Graduação em Biologia Comparada da Universidade de São Paulo
  • NIH

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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