Paper

Drosophila melanogaster pigmentation demonstrates adaptive phenotypic parallelism over multiple timescales

Greenblum, Sharon I, Petrov, Dmitri A, Rajpurohit, Subhash, Bitter, Mark C, Behrman, Emily L, Schmidt, Paul, Betancourt, Nicolas J, Berner, Mary Catherine, Rhodes, Jessica A, Berardi, Skyler, Bergland, Alan O

2024

Overview

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than fifteen generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.Competing Interest StatementThe authors have declared no competing interest.Footnotes* Edits were made to the interpretation of genomic analysis results.

• Publisher: Cold Spring Harbor Laboratory Press,Cold Spring Harbor Laboratory
• Subject: Adaptation / Alleles / Demography / Drosophila melanogaster / Environmental changes / Evolution & development / Evolutionary Biology / Evolutionary genetics / Frequency dependence / Gene frequency / Genetic diversity / Genomic analysis / Insects / Phenotypes / Phenotypic variations / Pigmentation / Polygenic inheritance / Population genetics