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

One of the most essential question in ecology and evolutionary biology is how spatial distribution is limited in each species on the earth. Theoretically, asymmetric gene flow from core populations is suggested to increase poorly adapted immigrants in population at range edge. The genetic load due to the migration (i.e., migration load) should prevent adaptation to the local habitat, leading to decrease in distribution range via local extinction or the limit of range expansion to outside of current distribution. However, relatively few experimental studies have examined immigration's effects on fitness and natural selection within recipient populations. To demonstrate the influence of gene flow on distribution range, we performed field and laboratory observation, and population transcriptomics for the common river snail, Semisulcospira reinina. We found that river steepness is related to the lower distribution limit of S. reiniana in each river, with narrower distribution range in steeper river. Population transcriptomics analysis showed that gene flow was heavily asymmetric from upward populations to downward ones in a steep river, suggesting the greater migration load in steep river. The number of candidate genes putatively involved in adaptation to local habitat was less in a steep river than in a gentle river. Gene expression profiles also supported that individuals achieve local adaptations more properly in gentle river than steep one. Furthermore, laboratory experiments suggested the evolutionary difference among local populations in salinity tolerance was only found in gentle river. Our results provided the evidence that migration load owing to asymmetric gene flow along with stream disturbs local adaptation and then restricts distribution range of river snails.