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LARGE-SCALE GENOME SAMPLING REVEALS UNIQUE IMMUNITY AND METABOLIC ADAPTATIONS IN BATS
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  • Diana Moreno Santillan,
  • Tanya Lama,
  • Yocelyn Gutiérrez Guerrero,
  • Alexis Brown,
  • Paul Donat,
  • Huabin Zhao,
  • Stephen Rossiter,
  • Laurel Yohe,
  • Joshua Potter,
  • Emma Teeling,
  • Sonja Vernes,
  • Kalina Davies,
  • Eugene Myers,
  • Graham Hughes,
  • Zixia Huang,
  • Federico G. Hoffmann,
  • Angelique Corthals,
  • David Ray,
  • Liliana Davalos
Diana Moreno Santillan
Texas Tech University

Corresponding Author:dianad.mosa@gmail.com

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Tanya Lama
Stony Brook University
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Yocelyn Gutiérrez Guerrero
Universidad Nacional Autonoma de Mexico
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Alexis Brown
Stony Brook University
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Paul Donat
Stony Brook University
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Huabin Zhao
Wuhan University
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Stephen Rossiter
Queen Mary University of London
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Laurel Yohe
Yale University
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Joshua Potter
Queen Mary University of London
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Emma Teeling
University College Dublin
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Sonja Vernes
Max Planck Institute for Psycholinguistics
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Kalina Davies
Queen Mary University of London
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Eugene Myers
Max-Planck-Institute of Molecular Cell Biology and Genetics
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Graham Hughes
University College Dublin
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Zixia Huang
University College Dublin
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Federico G. Hoffmann
Mississippi State University
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Angelique Corthals
John Jay College of Criminal Justice
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David Ray
Texas Tech University
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Liliana Davalos
Stony Brook University
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Abstract

Comprising more than 1400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity given small body size, 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 encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune system 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 defense receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defense 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 anti-viral immune response while dampening inflammatory signaling. 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.
30 Dec 2020Submitted to Molecular Ecology
04 Jan 2021Submission Checks Completed
04 Jan 2021Assigned to Editor
04 Jan 2021Reviewer(s) Assigned
20 Apr 2021Review(s) Completed, Editorial Evaluation Pending
28 Apr 2021Editorial Decision: Revise Minor
27 May 2021Review(s) Completed, Editorial Evaluation Pending
27 May 20211st Revision Received
03 Jun 2021Editorial Decision: Accept