Distinct Genes with Similar Functions Underlie Convergent Evolution in Myotis Bat Ecomorphs

Author:

Morales Ariadna E12345ORCID,Burbrink Frank T2ORCID,Segall Marion267ORCID,Meza Maria18ORCID,Munegowda Chetan345ORCID,Webala Paul W9ORCID,Patterson Bruce D10ORCID,Thong Vu Dinh1112ORCID,Ruedi Manuel13ORCID,Hiller Michael345ORCID,Simmons Nancy B1ORCID

Affiliation:

1. Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History , New York , USA

2. Department of Herpetology, Division of Vertebrate Zoology, American Museum of Natural History , New York , USA

3. Centre for Translational Biodiversity Genomics , Frankfurt am Main, Hessen , Germany

4. Senckenberg Research Institute , Frankfurt am Main, Hessen , Germany

5. Faculty of Biosciences, Goethe-University , Frankfurt am Main, Hessen , Germany

6. Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205, Muséum National d’Histoire Naturelle, CNRS, SU, EPHE, UA, CP 50 , Paris , France

7. Department of Life Sciences, The Natural History Museum , London SW7 5BD , UK

8. Escuela de Biología, Universidad Industrial de Santander , Bucaramanga, Santander , Colombia

9. Department of Forestry and Wildlife Management, Maasai Mara University , Narok 20500 , Kenya

10. Negaunee Integrative Research Center, Field Museum of Natural History , Chicago , USA

11. Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology , 18 Hoang Quoc Viet Road, Cau Giay District, Hanoi , Vietnam

12. Graduate University of Science and Technology, Vietnam Academy of Science and Technology , 18 Hoang Quoc Viet Road, Cau Giay District, Hanoi , Vietnam

13. Department of Mammalogy and Ornithology, Natural History Museum of Geneva , Geneva 1208 , Switzerland

Abstract

Abstract Convergence offers an opportunity to explore to what extent evolution can be predictable when genomic composition and environmental triggers are similar. Here, we present an emergent model system to study convergent evolution in nature in a mammalian group, the bat genus Myotis. Three foraging strategies—gleaning, trawling, and aerial hawking, each characterized by different sets of phenotypic features—have evolved independently multiple times in different biogeographic regions in isolation for millions of years. To investigate the genomic basis of convergence and explore the functional genomic changes linked to ecomorphological convergence, we sequenced and annotated 17 new genomes and screened 16,426 genes for positive selection and associations between relative evolutionary rates and foraging strategies across 30 bat species representing all Myotis ecomorphs across geographic regions as well as among sister groups. We identify genomic changes that describe both phylogenetic and ecomorphological trends. We infer that colonization of new environments may have first required changes in genes linked to hearing sensory perception, followed by changes linked to fecundity and development, metabolism of carbohydrates, and heme degradation. These changes may be linked to prey acquisition and digestion and match phylogenetic trends. Our findings also suggest that the repeated evolution of ecomorphs does not always involve changes in the same genes but rather in genes with the same molecular functions such as developmental and cellular processes.

Funder

Gerstner Scholars Program

Gerstner Family Foundation

Gans Collections and Charitable Fund

H2020 Marie Skłodowska-Curie Actions

Vietnam Academy of Science and Technology

Publisher

Oxford University Press (OUP)

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