Seasonal evolution of Drosophila melanogaster abdominal pigmentation is associated with a multifarious selective landscape

Pigmentation has been widely studied by evolutionary biologists due to both ease of measure and relationship to fitness. Drosophila melanogaster pigmentation has represented a particularly useful avenue of investigation, as extensive genetic tools have enabled the characterization of the trait’s complex architecture. Drosophila pigmentation also varies predictably across space and time in wild populations, suggesting pigmentation is a component of adaptation to local environmental conditions. Despite this, the impact of D. melanogaster pigmentation on fitness, and the environmental factors that drive the evolution of pigmentation, are not well understood. To address this gap, we experimentally evolved replicated D. melanogaster populations in field mesocosms to determine whether and how pigmentation evolves in response to environmental variation. We found that pigmentation rapidly and predictably adapted to a direct manipulation of temperature, supportive of melanization playing a role in thermoregulation. However, we also determined that pigmentation responded adaptively to direct manipulations of numerous additional factors, including intraspecific competition, diet, and the microbiome. These findings suggest that the selective landscape acting on pigmentation is complex and multifaceted, and that patterns of melanization may be driven, at least in part, by indirect selection due to correlations with other fitness-related traits.