Temporal and spatial instability in neutral and adaptive (MHC) genetic variation in marginal salmon populations.
ABSTRACT: The role of marginal populations for the long-term maintenance of species' genetic diversity and evolutionary potential is particularly timely in view of the range shifts caused by climate change. The Centre-Periphery hypothesis predicts that marginal populations should bear reduced genetic diversity and have low evolutionary potential. We analysed temporal stability at neutral microsatellite and adaptive MHC genetic variation over five decades in four marginal Atlantic salmon populations located at the southern limit of the species' distribution with a complicated demographic history, which includes stocking with foreign and native salmon for at least 2 decades. We found a temporal increase in neutral genetic variation, as well as temporal instability in population structuring, highlighting the importance of temporal analyses in studies that examine the genetic diversity of peripheral populations at the margins of the species' range, particularly in face of climate change.
Project description:Global climate change is one of the major driving forces for adaptive shifts in migration and breeding phenology and possibly impacts demographic changes if a species fails to adapt sufficiently. In Western Europe, pied flycatchers (Ficedula hypoleuca) have insufficiently adapted their breeding phenology to the ongoing advance of food peaks within their breeding area and consequently suffered local population declines. We address the question whether this population decline led to a loss of genetic variation, using two neutral marker sets (mitochondrial control region and microsatellites), and one potentially selectively non-neutral marker (avian Clock gene). We report temporal changes in genetic diversity in extant populations and biological archives over more than a century, using samples from sites differing in the extent of climate change. Comparing genetic differentiation over this period revealed that only the recent Dutch population, which underwent population declines, showed slightly lower genetic variation than the historic Dutch population. As that loss of variation was only moderate and not observed in all markers, current gene flow across Western and Central European populations might have compensated local loss of variation over the last decades. A comparison of genetic differentiation in neutral loci versus the Clock gene locus provided evidence for stabilizing selection. Furthermore, in all genetic markers, we found a greater genetic differentiation in space than in time. This pattern suggests that local adaptation or historic processes might have a stronger effect on the population structure and genetic variation in the pied flycatcher than recent global climate changes.
Project description:Comparison of levels and patterns of genetic variation in natural populations either across loci or against neutral expectation can yield insight into locus-specific differences in the strength and direction of evolutionary forces. We used both approaches to test the hypotheses on patterns of selection on major histocompatibility (MH)-linked markers. We performed temporal analyses of class I and class II? MH-linked markers and eight microsatellite loci in two Atlantic salmon populations in Ireland on two temporal scales: over six decades and 9 years in the rivers Burrishoole and Delphi, respectively. We also compared contemporary Burrishoole and Delphi samples with nearby populations for the same loci. On comparing patterns of temporal and spatial differentiation among classes of loci, the class II? MH-linked marker was consistently identified as an outlier compared with patterns at the other microsatellite loci or neutral expectation. We found higher levels of temporal and spatial heterogeneity in heterozygosity (but not in allelic richness) for the class II? MH-linked marker compared with microsatellites. Tests on both within- and among-population differentiation are consistent with directional selection acting on the class II?-linked marker in both temporal and spatial comparisons, but only in temporal comparisons for the class I-linked marker. Our results indicate a complex pattern of selection on MH-linked markers in natural populations of Atlantic salmon. These findings highlight the importance of considering selection on MH-linked markers when using these markers for management and conservation purposes.
Project description:Observational data from the past century have highlighted the importance of interdecadal modes of variability in fish population dynamics, but how these patterns of variation fit into a broader temporal and spatial context remains largely unknown. We analyzed time series of stable nitrogen isotopes from the sediments of 20 sockeye salmon nursery lakes across western Alaska to characterize temporal and spatial patterns in salmon abundance over the past ?500 y. Although some stocks varied on interdecadal time scales (30- to 80-y cycles), centennial-scale variation, undetectable in modern-day catch records and survey data, has dominated salmon population dynamics over the past 500 y. Before 1900, variation in abundance was clearly not synchronous among stocks, and the only temporal signal common to lake sediment records from this region was the onset of commercial fishing in the late 1800s. Thus, historical changes in climate did not synchronize stock dynamics over centennial time scales, emphasizing that ecosystem complexity can produce a diversity of ecological responses to regional climate forcing. Our results show that marine fish populations may alternate between naturally driven periods of high and low abundance over time scales of decades to centuries and suggest that management models that assume time-invariant productivity or carrying capacity parameters may be poor representations of the biological reality in these systems.
Project description:How expected increases in climate variability will affect species diversity depends on the role of such variability in regulating the coexistence of competing species. Despite theory linking temporal environmental fluctuations with the maintenance of diversity, the importance of climate variability for stabilizing coexistence remains unknown because of a lack of appropriate long-term observations. Here, we analyze three decades of demographic data from a Kansas prairie to demonstrate that interannual climate variability promotes the coexistence of three common grass species. Specifically, we show that (i) the dynamics of the three species satisfy all requirements of "storage effect" theory based on recruitment variability with overlapping generations, (ii) climate variables are correlated with interannual variation in species performance, and (iii) temporal variability increases low-density growth rates, buffering these species against competitive exclusion. Given that environmental fluctuations are ubiquitous in natural systems, our results suggest that coexistence based on the storage effect may be underappreciated and could provide an important alternative to recent neutral theories of diversity. Field evidence for positive effects of variability on coexistence also emphasizes the need to consider changes in both climate means and variances when forecasting the effects of global change on species diversity.
Project description:In some wild Atlantic salmon populations, rapid declines in numbers of wild returning adults has been associated with an increase in the prevalence of farmed salmon. Studies of phenotypic variation have shown that interbreeding between farmed and wild salmon may lead to loss of local adaptation. Yet, few studies have attempted to assess the impact of interbreeding at the genome level, especially among North American populations. Here, we document temporal changes in the genetic makeup of the severely threatened Magaguadavic River salmon population (Bay of Fundy, Canada), a population that might have been impacted by interbreeding with farmed salmon for nearly 20 years. Wild and farmed individuals caught entering the river from 1980 to 2005 were genotyped at 112 single-nucleotide polymorphisms (SNPs), and/or eight microsatellite loci, to scan for potential shifts in adaptive genetic variation. No significant temporal change in microsatellite-based estimates of allele richness or gene diversity was detected in the wild population, despite its precipitous decline in numbers over the last two decades. This might reflect the effect of introgression from farmed salmon, which was corroborated by temporal change in linkage-disequilibrium. Moreover, SNP genome scans identified a temporal decrease in candidate loci potentially under directional selection. Of particular interest was a SNP previously shown to be strongly associated with an important quantitative trait locus for parr mark number, which retained its genetic distinctiveness between farmed and wild fish longer than other outliers. Overall, these results indicate that farmed escapees have introgressed with wild Magaguadavic salmon resulting in significant alteration of the genetic integrity of the native population, including possible loss of adaptation to wild conditions.
Project description:Climate-induced phenological shifts can influence population, evolutionary, and ecological dynamics, but our understanding of these phenomena is hampered by a lack of long-term demographic data. We use a multi-decade census of 5 salmonid species representing 14 life histories in a warming Alaskan stream to address the following key questions about climate change and phenology: How consistent are temporal patterns and drivers of phenology for similar species and alternative life histories? Are shifts in phenology associated with changes in phenotypic variation? How do phenological changes influence the availability of resource subsidies? For most salmonid species, life stages, and life histories, freshwater temperature influences migration timing--migration events are occurring earlier in time (mean?=?1.7 days earlier per decade over the 3-5 decades), and the number of days over which migration events occur is decreasing (mean?=?1.5 days per decade). Temporal trends in migration timing were not correlated with changes in intra-annual phenotypic variation, suggesting that these components of the phenotypic distribution have responded to environmental change independently. Despite commonalities across species and life histories, there was important biocomplexity in the form of disparate shifts in migration timing and variation in the environmental factors influencing migration timing for alternative life history strategies in the same population. Overall, adult populations have been stable during these phenotypic and environmental changes (? ? 1.0), but the temporal availability of salmon as a resource in freshwater has decreased by nearly 30 days since 1971 due to changes in the median date of migration timing and decreases in intra-annual variation in migration timing. These novel observations advance our understanding of phenological change in response to climate warming, and indicate that climate change has influenced the ecology of salmon populations, which will have important consequences for the numerous species that depend on this resource.
Project description:Marginal populations are expected to provide the frontiers for adaptation, evolution and range shifts of plant species under the anticipated climate change conditions. Marginal populations are predicted to show genetic divergence from central populations due to their isolation, and divergent natural selection and genetic drift operating therein. Marginal populations are also expected to have lower genetic diversity and effective population size (Ne) and higher genetic differentiation than central populations. We tested these hypotheses using eastern white pine (Pinus strobus) as a model for keystone, long-lived widely-distributed plants. All 614 eastern white pine trees, in a complete census of two populations each of marginal old-growth, central old-growth, and central second-growth, were genotyped at 11 microsatellite loci. The central populations had significantly higher allelic and genotypic diversity, latent genetic potential (LGP) and Ne than the marginal populations. However, heterozygosity and fixation index were similar between them. The marginal populations were genetically diverged from the central populations. Model testing suggested predominant north to south gene flow in the study area with curtailed gene flow to northern marginal populations. Signatures of natural selection were detected at three loci in the marginal populations; two showing divergent selection with directional change in allele frequencies, and one balancing selection. Contrary to the general belief, no significant differences were observed in genetic diversity, differentiation, LGP, and Ne between old-growth and second-growth populations. Our study provides information on the dynamics of migration, genetic drift and selection in central versus marginal populations of a keystone long-lived plant species and has broad evolutionary, conservation and adaptation significance.
Project description:Species ranges are influenced by past climate oscillations, geographical constraints, and adaptive potential to colonize novel habitats at range limits. This study used Liriodendron chinense, an important temperate Asian tree species, as a model system to evaluate the roles of biogeographic history and marginal population genetics in determining range limits. We examined the demographic history and genetic diversity of 29 L. chinense populations using both chloroplast and nuclear microsatellite loci. Significant phylogeographic structure was recovered with haplotype clusters coinciding with major mountain regions. Long-term demographical stability was suggested by mismatch distribution analyses, neutrality tests, and ecological niche models (ENM) and suggested the existence of LGM refuges within mountain regions. Differences in genetic diversity between central and marginal populations were not significant for either genomic region. However, asymmetrical gene flow was inferred from central populations to marginal populations, which could potentially limit range adaptation and expansion of L. chinense.
Project description:In the main distribution area the genetic pattern of silver birch is dominated by two haplotypes: haplotype A located in the western and north-western Europe, and haplotype C in eastern and southeastern Europe, characterized by high levels of neutral genetic variability within populations, and low differentiation among populations. Information about the amount and structure of genetic variation in the southern marginal areas, representing rear populations left during the expansion of this species from southern glacial refugia, are lacking. The general aim of the study was to investigate the existence of the climatic characteristics typical of the environmental niche of the species, jointly to genetic organization, variation and gene flow, in marginal populations on the Italian Apennines and Greek Southern Rhodope and compare them with populations of the southern part of the main distribution range on the Alps and Balkans. Genetic analysis was performed using nuclear microsatellites loci on 311 trees sampled from 14 populations. Environmental analysis was performed on the multivariate analysis of derived climatic variables. The allelic pattern was analyzed to assess genetic diversity, population diversity and differentiation, population structure and gene flow. The geographic and environmental peripherality did not always match, with some Apennine sites at higher elevation enveloped in the environmental niche. In the peripheral populations on the Apennines, we observed a lower genetic diversity and higher differentiation, with evident genetic barriers detected around these sites. These characteristics were not shown in the marginal Greek populations. Unexpectedly, the southern Italian marginal populations showed genetic links with the Greek and central area of the distribution range. The Greek populations also showed evident gene flow with the Alpine and Balkan areas. The disparity of results in these two marginal areas show that it is not the geographic peripherality or even the ecological marginality that may shape the genetic diversity and structure of marginal populations, but primarily their position as part of the continuous range or as disjunct populations. This outcome suggests different considerations on how to manage their gene pools and the role that these rear populations can play in maintaining the biodiversity of this species.
Project description:Migratory salmon transit estuary habitats on their way out to the ocean but this phase of their life cycle is more poorly understood than other phases. The estuaries of large river systems in particular may support many populations and several species of salmon that originate from throughout the upstream river. The Skeena River of British Columbia, Canada, is a large river system with high salmon population- and species-level diversity. The estuary of the Skeena River is under pressure from industrial development, with two gas liquefaction terminals and a potash loading facility in various stages of environmental review processes, providing motivation for understanding the usage of the estuary by juvenile salmon. We conducted a juvenile salmonid sampling program throughout the Skeena River estuary in 2007 and 2013 to investigate the spatial and temporal distribution of different species and populations of salmon. We captured six species of juvenile anadromous salmonids throughout the estuary in both years, and found that areas proposed for development support some of the highest abundances of some species of salmon. Specifically, the highest abundances of sockeye (both years), Chinook in 2007, and coho salmon in 2013 were captured in areas proposed for development. For example, juvenile sockeye salmon were 2-8 times more abundant in the proposed development areas. Genetic stock assignment demonstrated that the Chinook salmon and most of the sockeye salmon that were captured originated from throughout the Skeena watershed, while some sockeye salmon came from the Nass, Stikine, Southeast Alaska, and coastal systems on the northern and central coasts of British Columbia. These fish support extensive commercial, recreational, and First Nations fisheries throughout the Skeena River and beyond. Our results demonstrate that estuary habitats integrate species and population diversity of salmon, and that if proposed development negatively affects the salmon populations that use the estuary, then numerous fisheries would also be negatively affected.