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.

Multiple genetic sources facilitate the northward range expansion of an intertidal oyster along China's coast

“…Untangling the genetic structure, population connectivity and genetic adaptation between the source and newly established population is crucial for understanding the mechanisms driving species distribution range expansion and biological invasion. Even for short‐time‐scale population distribution expansion, trends in rapid genetic adaptation can be detected (Wang et al, 2022). In the present study, our results indicate that multiple sources with divergent thermal adaptability facilitate the rapid northward distribution expansion of the southern species.…”

“…Characteristics in life history help the oyster C. sikamea expand further north than other southern species. The leading edge of the geographic distribution of C. sikamea has moved northward to $34 N (Appendix S1: Figure S1), one degree north of that of its counterpart N. yoldii, the first reported intertidal species experiencing northward distribution expansion along China's coast due to land reclamation (Wang et al, 2018(Wang et al, , 2022. Life history characteristics, including reproductive mode and period, and habitat specificity, have significant influences on shaping biogeographic patterns (Hu & Dong, 2022;Pappalardo et al, 2015;Wilson et al, 2009).…”

Thermal heterogeneity is an important factor for maintaining the genetic differentiation pattern of the pelagic barnacle Lepas anatifera in the northwest Pacific

“…The horizontal population differentiation or vertical differentiation of macrobenthos has been reported in previous studies (Bik et al, 2010;Ni et al, 2017;Pardo-Gandarillas et al, 2018;Sun et al, 2017Sun et al, , 2022Wang et al, 2022). However, studies of intraspecific population differentiation at both horizontal and vertical scales for epipelagic macrobenthos were still limited.…”

Single Nucleotide Polymorphism Markers with Applications in Conservation and Exploitation of Aquatic Natural Populations

“…In the studies of myosin heavy-chain proteins important for the muscle growth gene MYH in Pinctada fucata martensii had 18 out of 95 SNPs discovered in the exons region, were significantly associated with growth, of which 2 were confirmed in 2 populations [ 219 ]. In the studies of newly established populations of the marine snail Nerita yoldii north of the Yangtze River estuary, neutral SNPs confirmed that it consisted of founders and was distinct from the southern source population [ 220 ]. The new marginal population went through a bottleneck effect.…”