Convergent deployment of ancestral functions during the evolution of mammalian flight membranes

Author:

Feigin Charles Y.12ORCID,Moreno Jorge A.1ORCID,Ramos Raul3ORCID,Mereby Sarah A.1ORCID,Alivisatos Ares1,Wang Wei4ORCID,van Amerongen Renée5ORCID,Camacho Jasmin6ORCID,Rasweiler John J.7ORCID,Behringer Richard R.8,Ostrow Bruce9ORCID,Plikus Maksim V.3ORCID,Mallarino Ricardo1ORCID

Affiliation:

1. Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA.

2. School of BioSciences, The University of Melbourne, Parkville, Victoria 3010, Australia.

3. Department of Developmental and Cell Biology, University of California Irvine, Irvine, CA 92697, USA.

4. Lewis Sigler Institute, Princeton University, Princeton, NJ 08544, USA.

5. Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, Netherlands.

6. Stowers Institute for Medical Research, Kansas City, MO 64110, USA.

7. Department of Obstetrics and Gynecology, State University of New York Downstate Medical Center, Brooklyn, NY 11203, USA.

8. Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

9. Department of Biology, Grand Valley State University, Allendale, MI 49401, USA.

Abstract

Lateral flight membranes, or patagia, have evolved repeatedly in diverse mammalian lineages. While little is known about patagium development, its recurrent evolution may suggest a shared molecular basis. By combining transcriptomics, developmental experiments, and mouse transgenics, we demonstrate that lateral Wnt5a expression in the marsupial sugar glider ( Petaurus breviceps ) promotes the differentiation of its patagium primordium. We further show that this function of Wnt5a reprises ancestral roles in skin morphogenesis predating mammalian flight and has been convergently used during patagium evolution in eutherian bats. Moreover, we find that many genes involved in limb development have been redeployed during patagium outgrowth in both the sugar glider and bat. Together, our findings reveal that deeply conserved genetic toolkits contribute to the evolutionary transition to flight in mammals.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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