Population-Based Resequencing of Experimentally Evolved Populations Reveals the Genetic Basis of Body Size Variation in Drosophila melanogaster

Abstract

Body size is a classic quantitative trait with evolutionarily significant variation within many species. Locating the alleles responsible for this variation would help understand the maintenance of variation in body size in particular, as well as quantitative traits in general. However, successful genome-wide association of genotype and phenotype may require very large sample sizes if alleles have low population frequencies or modest effects. As a complementary approach, we propose that population-based resequencing of experimentally evolved populations allows for considerable power to map functional variation. Here, we use this technique to investigate the genetic basis of natural variation in body size in Drosophila melanogaster. Significant differentiation of hundreds of loci in replicate selection populations supports the hypothesis that the genetic basis of body size variation is very polygenic in D. melanogaster. Significantly differentiated variants are limited to single genes at some loci, allowing precise hypotheses to be formed regarding causal polymorphisms, while other significant regions are large and contain many genes. By using significantly associated polymorphisms as a priori candidates in follow-up studies, these data are expected to provide considerable power to determine the genetic basis of natural variation in body size.

Life history evolution and cellular mechanisms associated with increased size in high‐altitude Drosophila

“…Size is a complex trait at the genetic level, and many hundreds of genes may affect growth in Drosophila melanogaster (Turner et al. 2011). The developmental complexity of size – different structures and tissues grow at different rates, begin and end growth at different times, involving an interplay between cell growth, proliferation, and death – can also make size variation extremely difficult to study in even the most tractable laboratory models, let alone in naturally occurring populations of organisms.…”

A Genome-Wide Scan for Evidence of Selection in a Maize Population Under Long-Term Artificial Selection for Ear Number

“…However, the recent reduction in the cost of DNA sequencing and single-nucleotide polymorphism (SNP) detection (reviewed by Metzker 2010) now allows genomewide characterization of allelic variants. Accordingly, multiple experiments utilizing high-density SNP or sequence data to identify selected sites in both naturally and artificially selected populations and in both sexual and asexual species have been conducted (e.g., Akey et al 2002;Parts et al 2011;Bigham et al 2010;Turner et al 2011). The goals of these experiments ranged from localizing selected sites for unknown traits in natural populations (Voight et al 2006) to identifying quantitative trait loci for specific traits in experimentally derived populations or crosses (Parts et al 2011).…”

“…Methods for identifying selection in these artificially selected populations may include any of the methods utilized for natural populations, but a benefit of these types of studies is that samples of the progenitor population are frequently available, which allows for direct measurement of allele frequency changes. Separation of selection vs. genetic drift effects has been performed by comparing allele frequencies to simulations of drift (Wisser et al 2008) and by developing significance tests based on replicated or control populations (Parts et al 2011;Turner et al 2011).…”

Investigating Natural Variation inDrosophilaCourtship Song by the Evolve and Resequence Approach

“…While this may be true for variation associated with a small number of large-effect alleles, a much larger number of lines may be necessary to attain sufficient statistical power when phenotypic variation is caused by many smaller-effect alleles (Long and Langley 1999). For this reason, we propose that population-based resequencing of artificially selected populations provides a powerful compliment to GWAS in D. melanogaster (Nuzhdin et al 2007;Burke et al 2010;Earley and Jones 2011;Turner et al 2011;Zhou et al 2011). This approach is not limited by the creation and maintenance of large sets of inbred lines and could therefore be leveraged in other species of Drosophila, other insects, annual plants, and any other system where large populations can be manipulated over multiple generations (Johansson et al 2010;Parts et al 2011).…”