Rivers are fascinating ecosystems in which the eco‐evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater biodiversity patterns. Over the last 10 years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from southern France, and we broadened the scope of our findings using experiments, meta‐analyses, and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects not only community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that—in the studied river systems—stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity–ecosystem function relationships, and the setting of reliable conservation plans.
Background The brown trout ( Salmo trutta ) is an economically and ecologically important species for which population genetic monitoring is frequently performed. The most commonly used genetic markers for this species are microsatellites and mitochondrial markers that lack replicability among laboratories, and a large genome coverage. An alternative that may be particularly efficient and universal is the development of small to large panels of Single Nucleotide Polymorphism markers (SNPs). Here, we used Restriction site Associated DNA sequences (RADs) markers to identify a set of 12,204 informative SNPs positioned on the brown trout linkage map and suitable for population genetics studies. Then, we used this novel resource to develop a cost-effective array of 192 SNPs (96 × 2) evenly spread on this map. This array was tested for genotyping success in five independent rivers occupied by two main brown trout evolutionary lineages (Atlantic -AT- and Mediterranean -ME-) on a total of 1862 individuals. Moreover, inference of admixture rate with domestic strains and population differentiation were assessed for a small river system (the Taurion River, 190 individuals) and results were compared to a panel of 13 microsatellites. Results A high genotyping success was observed for all rivers (< 1% of non-genotyped loci per individual), although some initially used SNP failed to be amplified, probably because of mutations in primers, and were replaced. These SNPs permitted to identify patterns of isolation-by-distance for some rivers. Finally, we found that microsatellite and SNP markers yielded very similar patterns for population differentiation and admixture assessments, with SNPs having better ability to detect introgression and differentiation. Conclusions The novel resources provided here opens new perspectives for universality and genome-wide studies in brown trout populations. Electronic supplementary material The online version of this article (10.1186/s12864-019-5958-9) contains supplementary material, which is available to authorized users.
Genetic admixture between captive-bred and wild individuals has been demonstrated to affect many individual traits, although little is known about its potential influence on dispersal, an important trait governing the eco-evolutionary dynamics of populations. Here, we quantified and described the spatial distribution of genetic admixture in a brown trout (Salmo trutta) population from a small watershed that was stocked until 1999, and then tested whether or not individual dispersal parameters were related to admixture between wild and captive-bred fish. We genotyped 715 fish at 17 microsatellite loci sampled from both the mainstream and all populated tributaries, as well as 48 fish from the hatchery used to stock the study area. First, we used Bayesian clustering to infer local genetic structure and to quantify genetic admixture. We inferred first generation migrants to identify dispersal events and test which features (genetic admixture, sex and body length) affected dispersal parameters (i.e. probability to disperse, distance of dispersal and direction of the dispersal event). We identified two genetic clusters in the river basin, corresponding to wild fish on the one hand and to fish derived from the captive strain on the other hand, allowing us to define an individual gradient of admixture. Individuals with a strong assignment to the captive strain occurred almost exclusively in some tributaries, and were more likely to disperse towards a tributary than towards a site of the mainstream. Furthermore, dispersal probability increased as the probability of assignment to the captive strain increased, and individuals with an intermediate level of admixture exhibited the lowest dispersal distances. These findings show that various dispersal parameters may be biased by admixture with captive-bred genotypes, and that management policies should take into account the differential spread of captive-bred individuals in wild populations.
1. Intraspecific genetic diversity is heterogeneously distributed in natural landscapes and often forms repeatable spatial patterns. For instance, in rivers, genetic diversity increases towards downstream areas, whereas genetic differentiation increases in isolated upstream areas. Nonetheless, these patterns can be modified by human-induced perturbations, and documenting the extent to which human activities alter these natural patterns is important for conservation. Among the human pressures that affect freshwater biodiversity, stocking natural populations with captive-bred strains is a common practice worldwide that can strongly alter the genetic integrity of wild populations.2. The main objectives of this study were to document the spatial distribution of captive-bred ancestry in brown trout (Salmo trutta) populations from four French basins having been stocked according to different practices, and to quantify for each basin the effect of captive-bred ancestry on the spatial distribution of genetic diversity and differentiation. The four basins were sampled along their upstream-downstream gradient, and a total of 1,686 individuals were genotyped at 192 single nucleotide polymorphism loci.3. For all basins, individuals with a strong assignment to the captive strain were mostly found in upper reaches, although the average proportion of captive-bred ancestry varied strikingly among rivers (from 1.9 to 58.7%). Although spatial patterns of genetic differentiation were not affected by introgression and showed an expected increase with increasing distances from the river mouth in all basins, there was evidence that the classical pattern of downstream increase in genetic diversity was reversed when considering highly introgressed populations.4. These findings demonstrate that the stocking of captive-bred strains can strongly modify natural spatial patterns of diversity, even when stocking occurred many generations ago and has now ended. The study illustrates the major impacts of humans on intraspecific biodiversity patterns, and emphasizes the importance of conservation plans that take into account this artificial distribution of genetic diversity.Jérôme G. Prunier and Keoni Saint-Pé are co-first authors.
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