engleski

Re-thinking a classic clinal trait: Pleiotropic consequences of thermally adaptive dopamine on pigmentation clines in Drosophila

Clinal variation is widely regarded as strong evidence for adaptation in natural populations. One of the best-studied clinal phenotypes is the latitudinal melanism cline in ectotherms. Owing to the repeatability of clinal pigmentation across species and continents, this trait is frequently considered as a classic example for an adaptive trait. Nevertheless, how selection operates on this trait is still debated. The thermal budget hypothesis, one popular explanation, suggests that pigmentation intensity modulates the use of sunlight for thermoregulation. Here, we challenge this hypothesis and show how misleading the evolutionary interpretation of phenotypic variation can be. Using highly replicated experimental evolution setup, we exposed natural Drosophila simulans populations to novel thermal environments. After more than 100 generations of adaptation to hot temperature, the key components of melanin metabolism evolved in the same direction as in natural clines. Because temperature adaptation was not mediated by exposure to sun, we searched for alternative explanations. Melanin, the key ingredient for pigmentation, is synthesized from dopamine, a highly pleiotropic neurotransmitter. Using RNA- seq, metabolomics, and transgenic and pharmacologic modulation of dopamine, we uncovered the adaptive role of dopamine levels. Temperature strongly modulates signaling activity and in our experiment and natural populations, evolution modulates dopaminergic signaling to maintain synaptic homeostasis. We demonstrate that the evolutionary modulation of dopaminergic signaling helps to maintain normal locomotion even at high temperatures. We conclude that the pigmentation cline in Drosophila is a pleiotropic read-out of adaptive changes in dopamine metabolism, rather than an adaptive phenotype. Our results demonstrate that pleiotropy is a major challenge for the interpretation of phenotypic variation in a causative evolutionary framework.

Drosophila simulans ; clinal pigmentation ; thermoregulation ; melanin ; dopaminergic signalling ; pleiotropy

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