Population genomics reveals complex patterns of immune gene evolution in monarch butterflies (Danaus plexippus)

• Type of Material: Article
• Authors: Wen-Hao Tan, Emory University; Andrew J. Mongue, University of Kansas; Jacobus De Roode, Emory University; Nicole Marie Gerardo, Emory University; James R. Walters, University of Kansas
• Language: English
• Date: 2019-04-26
• Publisher: Cold Spring Harbor Laboratory
• Publication Version: Preprint (Prior to Peer Review)
• Copyright Statement: The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): https://doi.org/10.1101/620013
• Title of Journal or Parent Work: bioRxiv
• Grant/Funding Information: This work was supported by National Science Foundation (NSF) grant IOS-1557724 to JCdR and NMG, and NSF grant DEB 1457758 to JRW.
• Keywords: Danaus; natural selection; ecological immunology; Lepidoptera; immunity
• Research Categories: Health Sciences, Immunology; Biology, Ecology

Abstract

Immune genes presumably rapidly evolve as pathogens exert strong selection pressures on host defense, but the evolution of immune genes is also constrained by trade-offs with other biological functions and shaped by the environmental context. Thus, immune genes may exhibit complex evolutionary patterns, particularly when organisms disperse to or live in variable environments. We examined the evolutionary patterns of the full set of known canonical immune genes within and among populations of monarch butterflies (Danaus plexippus), and relative to a closely related species (D. gilippus). Monarchs represent a system with a known evolutionary history, in which North American monarchs dispersed to form novel populations across the world, providing an opportunity to explore the evolution of immunity in the light of population expansion into novel environments. By analyzing a whole-genome resequencing dataset across populations, we found that immune genes as a whole do not exhibit consistent patterns of selection, differentiation, or genetic variation, but that patterns are specific to functional classes. Species comparisons between D. plexippus and D. gilippus and analyses of monarch populations both revealed consistently low levels of genetic variation in signaling genes, suggesting conservation of these genes over evolutionary time. Modulation genes showed the opposite pattern, with signatures of relaxed selection across populations. In contrast, recognition and effector genes exhibited less consistent patterns. When focusing on genes with exceptionally strong signatures of selection or differentiation, we also found population-specific patterns, consistent with the hypothesis that monarch populations do not face uniform selection pressures with respect to immune function.