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

Distribution 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 Nerita yoldii, 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 transcriptional plasticity in the new marginal
populations, potentially contributing to local adaptation. These results
suggest a new biogeographic pattern for the snail N.
yoldii has formed with the occurrence of demographic, physiologic
and genetic changes, and emphasize the roles of adaptation of marginal
populations during distribution range expansion.