Large-Scale Genome Sampling Reveals Unique Immunity and Metabolic Adaptations in Bats

Authors

Diana D. Moreno Santillán, Texas Tech University
Tanya M. Lama, Stony Brook UniversityFollow
Yocelyn T. Gutierrez Guerrero, Instituto de Ecología, UNAM
Alexis M. Brown, Stony Brook University
Paul Donat, Stony Brook University
Huabin Zhao, Wuhan University
Stephen J. Rossiter, School of Biological and Chemical Sciences Queen Mary University of London
Laurel R. Yohe, Yale University
Joshua H. Potter, School of Biological and Chemical Sciences Queen Mary University of London
Emma C. Teeling, University College Dublin
Sonja C. Vernes, Max Planck Institute for Psycholinguistics
Kalina T.J. Davies, School of Biological and Chemical Sciences Queen Mary University of London
Eugene Myers, Max Planck Institute of Molecular Cell Biology and Genetics
Graham M. Hughes, University College Dublin
Zixia Huang, University College Dublin
Federico Hoffmann, College of Agriculture and Life Sciences
Angelique P. Corthals, John Jay College of Criminal Justice
David A. Ray, Texas Tech University
Liliana M. Dávalos, Stony Brook University

Document Type

Conference Proceeding

Publication Date

12-1-2021

Publication Title

Molecular Ecology

Abstract

Comprising more than 1,400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species, one generated in this study, encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defence receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defence response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance antiviral immune response while dampening inflammatory signalling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.

Keywords

adaptive immunity, gene family evolution, inflammatory pathway, innate immunity, metabolism, viral tolerance

Volume

30

Issue

23

First Page

6449

Last Page

6467

DOI

10.1111/mec.16027

ISSN

09621083

Comments

Peer reviewed accepted manuscript.

Recommended Citation

Moreno Santillán, Diana D.; Lama, Tanya M.; Gutierrez Guerrero, Yocelyn T.; Brown, Alexis M.; Donat, Paul; Zhao, Huabin; Rossiter, Stephen J.; Yohe, Laurel R.; Potter, Joshua H.; Teeling, Emma C.; Vernes, Sonja C.; Davies, Kalina T.J.; Myers, Eugene; Hughes, Graham M.; Huang, Zixia; Hoffmann, Federico; Corthals, Angelique P.; Ray, David A.; and Dávalos, Liliana M., "Large-Scale Genome Sampling Reveals Unique Immunity and Metabolic Adaptations in Bats" (2021). Biological Sciences: Faculty Publications, Smith College, Northampton, MA.
https://scholarworks.smith.edu/bio_facpubs/316