Whole-Genome Resequencing of Experimental Populations Reveals Polygenic Basis of Egg-Size Variation inDrosophila melanogaster

Abstract

Complete genome resequencing of populations holds great promise in deconstructing complex polygenic traits to elucidate molecular and developmental mechanisms of adaptation. Egg size is a classic adaptive trait in insects, birds, and other taxa, but its highly polygenic architecture has prevented high-resolution genetic analysis. We used replicated experimental evolution in Drosophila melanogaster and whole-genome sequencing to identify consistent signatures of polygenic egg-size adaptation. A generalized linear-mixed model revealed reproducible allele frequency differences between replicated experimental populations selected for large and small egg volumes at approximately 4,000 single nucleotide polymorphisms (SNPs). Several hundred distinct genomic regions contain clusters of these SNPs and have lower heterozygosity than the genomic background, consistent with selection acting on polymorphisms in these regions. These SNPs are also enriched among genes expressed in Drosophila ovaries and many of these genes have well-defined functions in Drosophila oogenesis. Additional genes regulating egg development, growth, and cell size show evidence of directional selection as genes regulating these biological processes are enriched for highly differentiated SNPs. Genetic crosses performed with a subset of candidate genes demonstrated that these genes influence egg size, at least in the large genetic background. These findings confirm the highly polygenic architecture of this adaptive trait, and suggest the involvement of many novel candidate genes in regulating egg size.

Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet inDrosophila

“…), and a generalized linear mixed model (GLMM) with binomial error structure and replicate population as a random effect (Jha et al. ). The binomial GLM model had a superior performance compared to the three other models in terms of detecting allele frequency differentiation and true discovery rate for both main effects and, importantly, the interaction.…”

“…To correct for this, we calculated P ‐values of permuted datasets to generate an empirical null distribution (equally overdispersed) that was subsequently used to estimate FDR of the observed data, following the procedure by Benjamini and Hochberg () (Jha et al. ).…”

Plant and Animal Reproductive Strategies: Lessons from Offspring Size and Number Tradeoffs

“…Economically important egg traits in chicken (yolk volume, egg weight) are known to have high heritability (Olsen and Knox, 1940;Shultz, 1953;Zhang et al, 2005). We know little about the genetic control of egg size and number in non-model animal taxa, and most of what we know comes from the common fruit fly Drosophila melanogaster, for which the egg size-number tradeoff is well-known (Mackay et al, 2012;Jha et al, 2015).…”

“…Based on data from controlled crosses, he concluded that egg size is polygenically controlled by genes on all four chromosomes. Jha et al (2015) adopted a whole-genome resequencing approach on replicated experimental-evolution lines selected for large and small egg sizes, respectively. Corroborating Warren's findings, Jha and colleagues report that egg size is polygenically controlled by at least 200 genes.…”

Ancestral population reconstitution from isofemale lines as a tool for experimental evolution

“…; Jha et al. ). Assuming that the reference population is not evolving during the experiment, this design permits the distinction between a generic adaptive response to the laboratory and adaptation to the experimental conditions of interest.…”