Balancing selection on immunity genes: review of the current literature and new analysis in Drosophila melanogaster

Abstract

Balancing selection has been widely assumed to be an important evolutionary force, yet even today little is known about its abundance and its impact on the patterns of genetic diversity. Several studies have shown examples of balancing selection in humans, plants or parasites, and many genes under balancing selection are involved in immunity. It has been proposed that host-parasite coevolution is one of the main forces driving immune genes to evolve under balancing selection. In this paper, we review the literature on balancing selection on immunity genes in several organisms, including Drosophila. Furthermore, we performed a genome scan for balancing selection in an African population of Drosophila melanogaster using coalescent simulations of a demographic model with and without selection. We find very few genes under balancing selection and only one novel candidate gene related to immunity. Finally, we discuss the possible causes of the low number of genes under balancing selection.

A genome-wide scan for genes under balancing selection in Drosophila melanogaster

“…Moreover, in the studies [36] and [37], the authors look for balancing selection only in a small part of the genome of D. melanogaster . We also find little overlap when we compare the results to our earlier study [8]: only one gene ( CG18208 ) is shared for the African candidate genes. This discrepancy might again be explained by our different methodology and different dataset.…”

“…Unckless et al [36] found evidence of alleles maintained by balancing selection in genes encoding antimicrobial peptides. Nonetheless, examples of genes under balancing selection in D. melanogaster are still scarce, and no genome-wide analysis for balancing selection has been done in this species with the exception of our own previous preliminary work [8]. Based on the availability of a wealth of NGS data we approached the difficulties of detecting balancing selection in the genome using two common statistics (high genetic diversity and intermediate-frequency polymorphism), without specifying a certain type of balancing selection.…”

“…Dobzhansky proposed the ‘balanced hypothesis’, which suggests that many genes are polymorphic and that these polymorphisms are maintained by heterozygote advantage [1]. However, systematic studies that have been carried out on various organisms have so far reported little evidence of balancing selection [2–8]. …”

“…They found 60 candidates genes under balancing selection in two human populations. Several Drosophila studies have also recently obtained encouraging results in this respect [8, 36, 37]. Based on whole-genome sequence data, it has been shown that some genes share non-synonymous polymorphisms between D. melanogaster and D. simulans [34].…”

“…Following our preliminary work [8], we used next-generation-sequencing (NGS) data to identify targets of balancing selection in a derived (European) and an ancestral (African) population. We searched for evidence of balancing selection based on two criteria: high levels of polymorphism compared to neutral expectations and a distortion of the SFS toward intermediate frequencies.…”