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

Abstract

Humoral and cellular immune responses provide animals with major defences 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 (Danaus 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, signalling, modulation, and effector), we found distinct differences among these groups. Relative to control genes, recognition genes exhibit increased nonsynonymous diversity and divergence, suggesting reduced constraints on evolution, and supporting the notion that coevolution with pathogens results in diversifying selection. In contrast, signalling 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.

Signatures of Adaptation, Constraints, and Potential Redundancy in the Canonical Immune Genes of a Key Pollinator

“…For example, positive selection produces genomic regions of reduced diversity through “selective sweeps,” whereby selected beneficial alleles, as well as neighboring sites, can increase in frequency within a population to the point of fixation ( Nielsen et al 2005 ). Recent studies on insects have applied population genetic approaches to investigate the genetic variability of immune genes, as well as to determine the different forms of selection acting upon them ( Palmer et al 2018 ; Tan et al 2021 ). However, with a few exceptions, studies employing genome-wide population genomic techniques to better understand how selection has acted on different functional classes of the immune system are still lacking, especially for nonmodel organisms within the field of genetics (but see Tan et al 2021 ).…”

“…Recent studies on insects have applied population genetic approaches to investigate the genetic variability of immune genes, as well as to determine the different forms of selection acting upon them ( Palmer et al 2018 ; Tan et al 2021 ). However, with a few exceptions, studies employing genome-wide population genomic techniques to better understand how selection has acted on different functional classes of the immune system are still lacking, especially for nonmodel organisms within the field of genetics (but see Tan et al 2021 ).…”

Activation of immune pathways in common bed bugs, Cimex lectularius, in response to bacterial immune challenges - a transcriptomics analysis

“…Evolutionary biology studies revealed that genes associated with the canonical immune system often evolve most rapidly, both within and between species ( 1 , 2 ). With the growing number of insect genomes and transcriptomes being sequenced, it has become evident that duplication and loss of immune genes are likely caused by host-pathogen interactions ( 1 , 2 ). Moreover, certain species react to various pathogenic challenges with a diverse array of specific responses (see below).…”

The Effect of Developmental Pleiotropy on the Evolution of Insect Immune Genes

“…Genetic pleiotropy arises when a single gene product contributes to multiple discrete phenotypic traits, and many components of immune pathways appear to be pleiotropic. Since the discovery of the Toll pathway, for example, numerous studies (and indeed Nobel prizes) have recognized its conserved dual role in development and innate immune system signaling ( Lemaitre et al 1997 ; DiAngelo et al 2009 ; Anthoney et al 2018 ) and proposed that this could impose constraints on immune system evolution ( Obbard et al 2009 ; Tan et al 2021 ). More broadly, a recent study estimated that approximately 17% of human genes affect multiple discrete phenotypic traits, and functional enrichment analysis of this pleiotropic gene set revealed immune system functions to be among the most over-represented processes ( Sivakumaran et al 2011 ).…”