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

<p><span>Distribution </span><span>range expansion is one of the most significant consequences of climate change in the Anthropocene. During range expansion, the former biogeographic barrier can be broken and then a new biogeographic pattern might appear. A comprehensive study, including demographic pattern, physiological performance and genetic features, is crucial for understanding how the expanding population occupies and survives in the new habitat, within which it formerly did not occur. In the present study, we investigated the demographic, physiological, and genetic features of the intertidal gastropod </span><span><em>Nerita yoldii</em>, which has extended its northern limit by ~200 km into areas that are warming up faster than the historical distribution over the former biogeographic break of the Yangtze River Estuary (YRE) during recent decades. The neutral SNPs data showed that the new marginal populations formed a distinct cluster established by a few founders. Demographic modeling analysis revealed that the new marginal populations experienced strong genetic bottlenecks followed by recent demographic expansion. Successful expansion that overcomes the founder effect (reduced genetic variation) might be attributed to its high capacity of 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. Our study also reveals a fast loss of </span><span>transcriptional</span><span> plasticity in the new marginal populations, potentially contributing to local adaptation. These results suggest a new biogeographic pattern for the snail <em>N. yoldii</em> has formed with the occurrence of demographic, physiologic and genetic changes, and emphasize the roles of adaptation of marginal populations during distribution range expansion.</span></p>