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

Abstract

Humoral and cellular immune responses provide animals with major defenses against harmful pathogens. While it is often assumed that immune genes undergo rapid diversifying selection, this assumption has not been tested in many species. Moreover, it is likely that different classes of immune genes experience different levels of evolutionary constraint, resulting in varying selection patterns. We examined the evolutionary patterns for a set of 91 canonical immune genes of North American monarch butterflies (Danaus plexippus), using as an outgroup the closely related soldier butterfly (D. eresimus). As a comparison to these immune genes, we selected a set of control genes that were paired with each immune for approximate size and genomic location. As a whole, these immune genes had a significant but modest reduction in Tajima's D relative to paired-control genes, but otherwise did not show distinct patterns of population genetic variation or evolutionary rates. When further partitioning these immune genes into four functional classes (recognition, signaling, modulation, and effector), we found distinct differences among these groups. Relative to control genes, recognition genes exhibit increased non-synonymous diversity and divergence, suggesting reduced constraints on evolution, and supporting the notion that coevolution with pathogens results in diversifying selection. In contrast, signaling genes showed an opposite pattern of reduced diversity and divergence, suggesting evolutionary constraints and conservation. Modulator and effector genes showed no statistical differences from controls. These results are consistent with patterns found in immune genes in fruit flies and Pieris butterflies, suggesting that consistent selective pressures on different classes of immune genes broadly govern the evolution of innate immunity among insects.

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Citation:

Tan WH, Talla V, Mongue AJ, de Roode JC, Gerardo NM, Walters JR. (2021). Population genomics reveals variable patterns of immune gene evolution in monarch butterflies (Danaus plexippus). Molecular ecology