Demographic, physiological and genetic factors linked to the poleward range expansion of the snail Nerita yoldii along the shoreline of China.

Abstract

Species range shift is one of the most significant consequences of climate change in the Anthropocene. A comprehensive study, including demographic, physiological and genetic factors linked to poleward range expansion, is crucial for understanding how the expanding population occupies the new habitat. In the present study, we investigated the demographic, physiological and genetic features of the intertidal gastropod Nerita yoldii, which has extended its northern limit by ~200 km over the former biogeographical break of the Yangtze River Estuary in recent decades. Data from neutral single nucleotide polymorphisms (SNPs) showed that the new marginal populations formed a distinct cluster established by a few founders. Demographic modelling analysis revealed that the new marginal populations experienced a strong genetic bottleneck followed by recent demographic expansion. Successful expansion that overcame the founder effect might be attributed to its high capacity for rapid population growth and multiple introductions. According to the non-neutral SNPs under diversifying selection, there were high levels of heterozygosity in the new marginal populations, which might be beneficial for adapting to the novel thermal conditions. The common garden experiment showed that the new marginal populations have evolved divergent transcriptomic and physiological responses to heat stress, allowing them to occupy and survive in the novel environment. Lower transcriptional plasticity was observed in the new marginal populations. These results suggest a new biogeographical pattern of N. yoldii has formed with the occurrence of demographic, physiological and genetic changes, and emphasize the roles of adaptation of marginal populations during range expansion.