Abstract
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.
Highlights
One of the most important questions in evolutionary biology is how the spatial distribution of species is limited
In some of the quite steep rivers, no S. reiniana were observed up to 50 km from the estuary, while we found that the lower distribution limit was from 10 to 35 km from the estuary in other rivers
We demonstrated a relationship between river steepness and the lower distribution limit of a river snail using field data and population transcriptomic data, focusing on SNPs in transcripts and gene expression levels
Summary
One of the most important questions in evolutionary biology is how the spatial distribution of species is limited. The failure of adaptation along the environmental gradient due to migration load is suggested to be the predominant process at a small spatial scale and in species with higher dispersal ability[8,15]. A previous study assessed the phenotypic traits of a stickleback, Gasterosteus aculeatus, population inhabiting a pond and its inlet and outlet rivers and showed that the population in the outlet (downstream) of the pond exhibits a phenotype intermediate between that of the river- and pond-adapted fish, whereas the upstream population has a phenotype optimized for the river e nvironment[23] This inconsistency between the optimal and realized phenotype resulted from frequent immigration from the pond population, following the water flow. The extent of asymmetric gene flow is affected by the geographic and physical features of each river since passive movement is caused by environmental factors, such as frequency of floods, nature of the substratum, and the velocity and steepness of the river[18,28]
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