Evolution of circadian behavioral plasticity throughcis-regulatory divergence of a neuropeptide gene

Abstract

AbstractWidely-distributed species experience substantial environmental variation, which they often accommodate through behavioral plasticity. Although this ability is integral to fitness, we have little understanding of the mechanistic basis by which plasticity evolves. One factor that varies seasonally and by latitude is photoperiod (day length). Many organisms, including the cosmopolitanDrosophila melanogasterdisplay circadian plasticity, adjusting to fluctuating photoperiod by varying the timing of their activity to coincide with changing dawn/dusk intervals1. Here, we compareD. melanogasterwith the closely-related ecological specialistDrosophila sechellia, an equatorial island endemic that experiences minimal photoperiod variation, to investigate the molecular-genetic basis of circadian plasticity evolution2,3. We discover thatD. sechelliadisplays exceptionally little circadian plasticity compared toD. melanogasterand other non-equatorial drosophilids. Through a screen of circadian mutants inD. melanogaster/D. sechelliahybrids, we identify a role of the neuropeptide Pigment-dispersing factor (Pdf) in this loss. While the coding sequence ofPdfis conserved, we show thatPdfhas undergonecis-regulatory divergence in these drosophilids. We document species-specific temporal dynamic properties ofPdfRNA and protein expression, as well as Pdf neuron morphological plasticity, and demonstrate that modulating Pdf expression inD. melanogastercan influence the degree of behavioral plasticity. Furthermore, we find that thePdfregulatory region exhibits signals of selection across populations ofD. melanogasterfrom different latitudes. Finally, we provide evidence that plasticity confers a selective advantage forD. melanogasterat higher latitudes, whileD. sechellialikely suffers fitness costs through reduced copulation success outside its range. Our work definesPdfas a locus of evolution for circadian plasticity, which might have contributed to bothD. melanogaster’s global distribution andD. sechellia’s habitat specialization. Moreover, together with spatial changes in Pdf expression reported in high-latitude drosophilid species4,5, our findings highlight this neuropeptide gene as a hotspot for circadian plasticity evolution.