Population transcriptomics reveals the effect of gene flow on the evolution of range limits

One of the most important questions in evolutionary biology is how the spatial distribution of species is limited. Asymmetric gene flow from core populations is suggested to increase the number of poorly adapted immigrants in the populations at the range edge. Genetic load due to migration, i.e., migration load, should prevent adaptation to the local habitat, leading to decreases in distribution range via local extinction or the limiting range expansion. However, few experimental studies have examined the effects of immigration on fitness and natural selection within recipient populations. To investigate the influence of migration load on the evolution of distribution range, we performed field and laboratory observations as well as population transcriptomics for the common river snail, Semisulcospira reiniana. This species meets the conditions that migration from source populations can prevent local adaptation in a sink population because they inhabit the broader range of environments, including middle/upper reaches of a river and estuaries within a single river and they may be more vulnerable to being swept away by water currents due to lowered spontaneous (upward) locomotion activity. We found that river steepness was related to the lower distribution limit of S. reiniana, with a narrower distribution range in the steeper river. Population transcriptomic analysis showed that gene flow was heavily asymmetric from the upstream populations to downstream ones in the steep river, suggesting a greater migration load in the steep river. The number of genes putatively involved in adaptation to the local habitat was lower in the steep river than in the gentle river. Gene expression profiles suggested that individuals achieve better local adaptation in the gentle river. Laboratory experiments suggested that evolutionary differences in salinity tolerance among local populations were only found in the gentle river. Our results consistent with the hypothesis that migration load owing to asymmetric gene flow disturbs local adaptation and restricts the distribution range of river snails.