Accelerated Diversification Explains the Exceptional Species Richness of Tropical Characoid Fishes

Author:

Melo Bruno F1,Sidlauskas Brian L2,Near Thomas J3,Roxo Fabio F4,Ghezelayagh Ava3,Ochoa Luz E15,Stiassny Melanie L J6,Arroyave Jairo7,Chang Jonathan8,Faircloth Brant C9,MacGuigan Daniel J3,Harrington Richard C3,Benine Ricardo C4,Burns Michael D10,Hoekzema Kendra2,Sanches Natalia C1,Maldonado-Ocampo Javier A11,Castro Ricardo M C12,Foresti Fausto1,Alfaro Michael E13,Oliveira Claudio1

Affiliation:

1. Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University, Botucatu, SP 16818-689, Brazil

2. Department of Fisheries, Wildlife and Conservation Sciences, Oregon State University, Corvallis, OR 97331, USA

3. Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, USA

4. Sector of Zoology, Institute of Biosciences, São Paulo State University, Botucatu, SP 18618-689, Brazil

5. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Palmira, Valle del Cauca 763547, Colombia

6. Department of Ichthyology, American Museum of Natural History, New York, NY 10024, USA

7. Instituto de Biologiìa, Universidad Nacional Autónoma de México, Ciudad de México 04510, México

8. School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia

9. Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA

10. Cornell Lab of Ornithology, Cornell University Museum of Vertebrates, Ithaca, NY 14850, USA

11. Department de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Bogotá, DC Colombia (in memoriam)

12. Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Ribeirão Preto, SP 14040-901, Brazil

13. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA

Abstract

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.]

Funder

Fundação de Amparo à Pesquisa do Estado de São Paulo

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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