Lunar Reproductive Timing Acts as a Magic Trait and May Recruit Additional Isolating Barriers in Sympatric Marine Midge Populations

Abstract

Population divergence with gene flow has proven more common than expected, but the underlying mechanisms are not fully understood. Magic traits (i.e. characters involved in both ecological adaptation and assortative mating) offer a tantalizing mechanism to explain the phenomenon, yet empirical demonstrations are rare. Moreover, speciation is assumed to involve genomic processes that couple multiple reproductive barriers, rather than being driven by a single barrier, and it re-mains unclear how magic traits interact with these processes. Here, we investigate the marine midge Clunio marinus, whose reproduction is timed to the extreme spring tide low tides during full moon or new moon. In Roscoff (Brittany, France) there are two sympatric chronotypes, i.e. subpopulations which reproduce only during full or new moons. Lunar reproductive timing is hypothesized to act as a magic trait, as it is both ecologically relevant and isolates reproduction in time. Based on wild-caught mating pairs and laboratory crosses, we show that lunar timing indeed is the major reproductive barrier (RI > 0.87). We also identify additional barriers which further increase reproductive isolation (total RI > 0.94). To explore the genomic basis of these barriers, we perform association testing on several high-FST loci. Two loci were associated with multiple barriers, and patterns of linkage disequilibrium suggest that these effects may arise from a combination of genetic link-age and pleiotropy. Together, our results indicate that lunar timing played a pivotal role in chronotype divergence, not only as a magic trait but also by promoting the recruitment of additional isolating barriers. We hypothesize that this recruitment is due to the polygenic and complex genetic architecture of lunar timing, highlighting the joint role of magic traits and genomic architecture in divergence with gene flow.