Species' geographical ranges are often restricted due to niche limitation resulting in geographical isolation and reduced population size at range margins. Under the 'abundant center' paradigm, static marginal populations are thus expected to show higher genetic differentiation and lower genetic diversity than core populations. Low mate availability may also drive shifts towards higher propensity for selfing in geographically marginal populations. However, these predictions remain to be validated for contemporary range shifts occurring under current environmental change. This study is devoted to bridging this gap and assesses the spatial patterns of genetic structure and mating system across the geographical range of two coastal plant species characterized by contrasting contemporary range dynamics: the receding myrmecochorous Dune pansy (Viola tricolor subsp. curtisii) and the widespread expanding hydrochorous Rock samphire (Crithmum maritimum). Both species exhibited high propensity for selfing, with indications of inbreeding depression acting at early life stages. In Dune pansy, a biogeographical break was observed between core and marginal populations, with trailing-edge populations showing higher levels of genetic differentiation, reduced genetic diversity and higher levels of selfing estimated through progeny arrays. In contrast, genetic structuring was weak in Rock samphire and no clear spatial trends were observed in genetic diversity nor in mating system, likely the result of efficient long-distance seed dispersal by sea-surface currents. Our study highlights that key species differences in life-history traits related to dispersal and/or mate limitation modify the expectations of genetic diversity loss and mating system shift in contemporary range-expanding populations, as compared to historical core populations.
Identifying spatial patterns of genetic differentiation across a species range is critical to set up conservation and restoration decision-making. This is especially timely, since global change triggers shifts in species' geographic distribution and in the geographical variation of mating system and patterns of genetic differentiation, with varying consequences at the trailing and leading edges of a species' distribution. Using 454 pyrosequencing, we developed nuclear microsatellite loci for two plant species showing a strictly coastal geographical distribution and contrasting range dynamics: the expanding rock samphire (Crithmum maritimum, 21 loci) and the highly endangered and receding dune pansy (Viola tricolor subsp. curtisii, 12 loci). Population genetic structure was then assessed by genotyping more than 100 individuals from four populations of each of the two target species. Rock samphire displayed high levels of genetic differentiation (F = 0.38), and a genetic structure typical of a mostly selfing species (F ranging from 0.16 to 0.58). Populations of dune pansy showed a less pronounced level of population structuring (F = 0.25) and a genotypic structure more suggestive of a mixed-mating system when excluding two loci with heterozygote excess. These results demonstrate that the genetic markers developed here are useful to assess the mating system of populations of these two species. They will be tools of choice to investigate phylogeographical patterns and variation in mating system over the geographical distribution ranges for two coastal plant species that are subject to dynamic evolution due to rapid contemporary global change.
Anthropogenic changes drive shifts in species' geographic distributions and increase the occurrence of leading or trailing-edge marginal populations. Theoretical predictions and empirical observations indicate substantial changes in life-history traits in marginal populations, often involving dispersal and reproductive abilities. Using a common garden experiment, we studied the variation of life-history traits of populations sampled on spatial gradients extending from range-core to range-edge habitats for three expanding (miner's lettuce Claytonia perfoliata, Danish scurvygrass Cochlearia danica and rock samphire Crithmum maritimum) and one receding plant species (dune pansy Viola tricolor subs. curtisii). We monitored life-history traits related to dispersal, phenology, survival, reproductive output and selfing ability. Significant shifts in life-history traits between central and marginal populations strongly differed among species. Marginal populations of the three expanding species displayed modified seed weight in natura, suggesting increased dispersal abilities in leading-edge populations. Discarding unassessed maternal effects, this trait modification can be due to phenotypic plasticity or to genetic differentiation. In miner's lettuce, marginal expanding populations show advanced phenology and higher reproductive output, that may potentially influence their colonization ability. In rock samphire, life-history traits showed large intra-and inter-population variability that did not follow a core-to-edge geographic trend, except for seed size. Finally, the receding populations of the dune pansy displayed a shift towards a plant architecture maximizing survival but reducing individual reproductive success. Altogether, our results indicated a common trend for increased dispersal abilities in marginal populations of expanding species. However, shifts in species' distributions may drive idiosyncratic changes in other life-history traits, for which we observed no general evolutionary syndrome at range edges. These findings go along a stochastic view of trait evolution during range expansion, and question how to draw predictive projections of species' distribution shifts under current global change.
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