Parallel Evolution of Copy-Number Variation across Continents in Drosophila melanogaster

Abstract

Genetic differentiation across populations that is maintained in the presence of gene flow is a hallmark of spatially varying selection. In Drosophila melanogaster, the latitudinal clines across the eastern coasts of Australia and North America appear to be examples of this type of selection, with recent studies showing that a substantial portion of the D. melanogaster genome exhibits allele frequency differentiation with respect to latitude on both continents. As of yet there has been no genome-wide examination of differentiated copy-number variants (CNVs) in these geographic regions, despite their potential importance for phenotypic variation in Drosophila and other taxa. Here, we present an analysis of geographic variation in CNVs in D. melanogaster. We also present the first genomic analysis of geographic variation for copy-number variation in the sister species, D. simulans, in order to investigate patterns of parallel evolution in these close relatives. In D. melanogaster we find hundreds of CNVs, many of which show parallel patterns of geographic variation on both continents, lending support to the idea that they are influenced by spatially varying selection. These findings support the idea that polymorphic CNVs contribute to local adaptation in D. melanogaster In contrast, we find very few CNVs in D. simulans that are geographically differentiated in parallel on both continents, consistent with earlier work suggesting that clinal patterns are weaker in this species.

Keywords: copy-number variation; natural selection.; population genetics.

Fig. 1.

Histograms of lengths of all CNVs differentiated along one or both coastlines in Drosophila melanogaster (black) and D. simulans (gray).

Fig. 2.

Density of differentiated CNVs across the Drosophila melanogaster genome. The numbers of CNVs differentiated along the US cline (black), the Australian cline (white), or both (gray, whether in the same or opposite directions) are shown for each 1-Mb window on each chromosome arm. Approximate locations of large chromosomal inversions (from Corbett-Detig et al. 2012) are shown as dashed lines.

Fig. 3.

Venn diagrams of differentiated CNVs detected in Drosophila melanogaster and D. simulans. (a) Drosophila melanogaster. Differentiated CNVs detected in the United States are represented by the gray circle, whereas those detected in Australia are in the white circle. The intersection represents all CNVs differentiated on both continents, whether in the same or opposite directions with respect to distance from the equator. The much lower number of CNVs differentiated only in Australia is likely due to the lack of paired-end reads from these samples. (b) Differentiated CNVs detected in D. simulans.