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.
Highlights
Przeworski et al 2005; Pritchard and Di Rienzo 2010; The advent of whole-genome sequencing and inexpensive Pritchard et al 2010; Hernandez et al 2011; Burke 2012).genotyping has reinvigorated strategies for identifying genes Natural populations may experience selective forces undergoing adaptive change
To further prioritize these genes, we focused on specialized GO terms (FDR < 5%) that are relevant for egg development. These include regulation of cell size, female gamete generation, oogenesis, ovarian follicle cell development, germ cell migration, cell growth, and growth because these biological processes are likely to influence egg size. Combining genes in these GO terms yielded 95 candidates that are largely distinct from candidate genes within the differentiated blocks, indicating that SDV that do not fall in long-range linkage blocks can be targets of egg-size selection
Positive genetic correlations have been reported between ovariole number and thorax length (Bergland et al 2008)
Summary
Przeworski et al 2005; Pritchard and Di Rienzo 2010; The advent of whole-genome sequencing and inexpensive Pritchard et al 2010; Hernandez et al 2011; Burke 2012).genotyping has reinvigorated strategies for identifying genes Natural populations may experience selective forces undergoing adaptive change. One approach involves scan- that are locale-specific, further obscuring the adaptive phening along the genome to identify regions with patterns or notype to which selection is responding. In only a (Kawecki et al 2012) The key to this approach lies in the few cases, has it been possible to directly associate a control an investigator has in specifying the phenotype under phenotypic trait with molecular adaptations. The approach is seeing a resurgence in interest begenic adaptations that draw on standing variation may not be cause it is possible to affordably resequence samples detectable by scanning the genome to identify regions with from evolved and control populations.
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