Evolutionary genetics and dynamics of wing morphs in aphid males

Thesis (Ph. D.)--University of Rochester. Department of Biology, 2019.Organisms display remarkable morphological diversity in Nature, yet so much remains to understand the genetic basis of these variations. One prominent example of intraspecific morphological differences is wing dimorphism, displayed by a diverse group of insects including the aphids. In wing-dimorphic species, flight-capable and flight-incapable morphs are produced within single populations. The trade-offs between dispersal and reproductive abilities of these two alternative morphs have been extensively studied. However, little is known about the underlying genetic mechanism. This thesis first focuses on the genetic basis of the pea aphid (Acyrthosiphon pisum) wing dimorphism, wherein males exhibit one of two alternative morphologies that differ dramatically in a set of correlated traits besides the presence or absence of wings. This dimorphism is controlled by a single uncharacterized locus on the X chromosome called aphicarus (api for short). We localized api to a 130kb region of the pea aphid genome spanning two scaffolds and later closed the gap between these scaffolds using long-read sequencing technique. We discovered a previously unidentified 120kb, autosomal originated DNA region inserted into the wingless allele through comparative phylogenetic analysis. Two candidate genes, an aphid-specific gene and a follistatin paralog emerged as good candidates though expression analysis. We also identified the signatures of a selective sweep of these two candidate genes using pool-seq data of samples from natural populations. Comparison of the api region across host-specific pea aphid biotypes revealed that the two alleles were likely present prior to biotype diversification 16,000 years ago. In addition, we studied the evolution of male wing morph across aphid phylogeny and investigated the potential influence of four ecological factors. We estimated more wing losses than wing gains in different aphid lineages through ancestral state reconstruction. We found significant statistical support for the correlation of host alternation and host breadth, but not host plant type (woody or herbaceous) and ant tending, with male wing morphs. In addition, we observed consistent api allele frequency differences among three pea aphid biotypes (alfalfa, clover, and pea) across different locations, further suggesting the influence of host plant on male wing morph evolution