Rapid evolution of abdominal pigmentation in Drosophila melanogaster
Authors: Skyler Berardi 1; Subhash Rajpurohit 1,2; Seth Rudman 1,3; Tess Grainger 1,4; Mary Catherine Berner 1; Nicolas Betancourt 1; Paul Schmidt 1
Affiliations: 1) Dept. of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA; 2) Biological and Life Sciences, Ahmedabad University, Ahmedabad, India; 3) School of Biological Sciences, Washington State University, Vancouver, WA, USA; 4) Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada
Keywords: Ecological & conservation genetics
Climatic conditions vary dramatically across spatiotemporal scales, and understanding how populations adapt to this heterogeneity remains a fundamental goal of evolutionary biology. Elucidating the mechanisms of polygenic adaptation is critical to our understanding of how populations evolve in response to rapid environmental change. In this study, we leveraged Drosophila melanogaster as a model to tease apart the roles of demography, migration, and selection on the evolutionary dynamics of a complex, fitness-associated trait: pigmentation. The extent of abdominal melanization is highly variable both within and among species of Drosophila; in D. melanogaster, it exhibits latitudinal and altitudinal clines on multiple continents, suggesting that pigmentation is an important component of local adaptation to climate. We first examined patterns of pigmentation across a latitudinal cline on the east coast of North America, which was not previously characterized. We sampled flies from six natural populations ranging from 25.28°N to 42.45°N, and we measured patterns of pigmentation after generations of culture in a common garden, laboratory environment. We found that abdominal melanization increases predictably with latitude, consistent with previously documented patterns on other continents. This supports the hypothesis that phenotypic clines are driven by local adaptation to climate. We further explored the dynamics of these putatively adaptive patterns by probing whether seasonal trends are concordant with this latitudinal trend. We sampled flies from an orchard in southeastern Pennsylvania in the spring and fall across six years. We found that populations in the spring exhibit a higher degree of abdominal melanization, which then declines predictably and in parallel across seasonal time in the six replicate years. Finally, we seeded replicate outdoor mesocosms in southeastern Pennsylvania with an outbred panel of flies collected in the spring from local orchards across multiple years. This enabled us to further test the hypothesis that selection drives the observed seasonal patterns by eliminating the confounding effects of gene flow and cryptic population structure. The trend we had observed in the wild Pennsylvanian population was recapitulated: abdominal melanization decreased across seasonal time, and this pattern was repeated over several years in our mesocosms. Together, these findings implicate adaptive tracking as a key driver of the phenotypic response of populations to rapid environmental change.