Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic or environmental SD, depending on the type of cue that triggers sexual differentiation. Mixed systems, in which SD is affected by genetic as well as environmental factors, are however more prevalent than previously thought. Such systems nonetheless remain understudied in the context of evolutionary stability and dynamics. We have developed a theoretical model to explore how environmental influences on SD genes can affect evolution of SD mechanisms. We found that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with worldwide latitudinal clines in the frequencies of various SD systems, involving multiple different genes. We found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms.