Population genetics reveals divergent lineages and ongoing hybridization in a declining migratory fish species complex.

Deciphering the effects of historical and recent demographic processes responsible for the spatial patterns of genetic diversity and structure is a key objective in evolutionary and conservation biology. Using population genetic analyses, we investigated the demographic history, the contemporary genetic diversity and structure, and the occurrence of hybridization and introgression of two species of anadromous fish with contrasting life history strategies and which have undergone recent demographic declines, the allis shad (Alosa alosa) and the twaite shad (Alosa fallax). We genotyped 706 individuals from 20 rivers and 5 sites at sea in Southern Europe at thirteen microsatellite markers. Genetic structure between populations was lower for the nearly semelparous species A. alosa, which disperses greater distances compared to the iteroparous species, A. fallax. Individuals caught at sea were assigned at the river level for A. fallax and at the region level for A. alosa. Using an approximate Bayesian computation framework, we inferred that the most likely long term historical divergence scenario between both species and lineages involved historical separation followed by secondary contact accompanied by strong population size decline. Accordingly, we found evidence for contemporary hybridization and bidirectional introgression due to gene flow between both species and lineages. Moreover, our results support the existence of at least one distinct species in the Mediterrannean sea: A. agone in Golfe du Lion area, and another divergent lineage in Corsica. Overall, our results shed light on the interplay between historical and recent demographic processes and life history strategies in shaping population genetic diversity and structure of closely related species. The recent demographic decline of these species' populations and their hybridization should be carefully considered while implementing conservation programs.

Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar).

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater ('parr') stage to the migratory stage where they descend streams and enter salt water ('smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 °C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5 days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.

Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences.

Disentangling the effects of natural environmental features and anthropogenic factors on the genetic structure of endangered populations is an important challenge for conservation biology. Here, we investigated the combined influences of major environmental features and stocking with non-native fish on the genetic structure and local adaptation of Atlantic salmon (Salmo salar) populations. We used 17 microsatellite loci to genotype 975 individuals originating from 34 French rivers. Bayesian analyses revealed a hierarchical genetic structure into five geographically distinct clusters. Coastal distance, geological substrate and river length were strong predictors of population structure. Gene flow was higher among rivers with similar geologies, suggesting local adaptation to geological substrate. The effect of river length was mainly owing to one highly differentiated population that has the farthest spawning grounds off the river mouth (up to 900km) and the largest fish, suggesting local adaptation to river length. We detected high levels of admixture in stocked populations but also in neighbouring ones, implying large-scale impacts of stocking through dispersal of non-native individuals. However, we found relatively few admixed individuals suggesting a lower fitness of stocked fish and/or some reproductive isolation between wild and stocked individuals. When excluding stocked populations, genetic structure increased as did its correlation with environmental factors. This study overall indicates that geological substrate and river length are major environmental factors influencing gene flow and potential local adaptation among Atlantic salmon populations but that stocking with non-native individuals may ultimately disrupt these natural patterns of gene flow among locally adapted populations.

An examination of genetic diversity and effective population size in Atlantic salmon populations.

Effective population size (Ne) is an important parameter in the conservation of genetic diversity. Comparative studies of empirical data that gauge the relative accuracy of Ne methods are limited, and a better understanding of the limitations and potential of Ne estimators is needed. This paper investigates genetic diversity and Ne in four populations of wild anadromous Atlantic salmon (Salmo salar L.) in Europe, from the Rivers Oir and Scorff (France) and Spey and Shin (Scotland). We aimed to understand present diversity and historical processes influencing current population structure. Our results showed high genetic diversity for all populations studied, despite their wide range of current effective sizes. To improve understanding of high genetic diversity observed in the populations with low effective size, we developed a model predicting present diversity as a function of past demographic history. This suggested that high genetic diversity could be explained by a bottleneck occurring within recent centuries rather than by gene flow. Previous studies have demonstrated the efficiency of coalescence models to estimate Ne. Using nine subsets from 37 microsatellite DNA markers from the four salmon populations, we compared three coalescence estimators based on single and dual samples. Comparing Ne estimates confirmed the efficiency of increasing the number and variability of microsatellite markers. This efficiency was more accentuated for the smaller populations. Analysis with low numbers of neutral markers revealed uneven distributions of allelic frequencies and overestimated short-term Ne. In addition, we found evidence of artificial stock enhancement using native and non-native origin. We propose estimates of Ne for the four populations, and their applications for salmon conservation and management are discussed.

A hierarchical bayesian model to quantify uncertainty of stream water temperature forecasts.

Providing generic and cost effective modelling approaches to reconstruct and forecast freshwater temperature using predictors as air temperature and water discharge is a prerequisite to understanding ecological processes underlying the impact of water temperature and of global warming on continental aquatic ecosystems. Using air temperature as a simple linear predictor of water temperature can lead to significant bias in forecasts as it does not disentangle seasonality and long term trends in the signal. Here, we develop an alternative approach based on hierarchical Bayesian statistical time series modelling of water temperature, air temperature and water discharge using seasonal sinusoidal periodic signals and time varying means and amplitudes. Fitting and forecasting performances of this approach are compared with that of simple linear regression between water and air temperatures using i) an emotive simulated example, ii) application to three French coastal streams with contrasting bio-geographical conditions and sizes. The time series modelling approach better fit data and does not exhibit forecasting bias in long term trends contrary to the linear regression. This new model also allows for more accurate forecasts of water temperature than linear regression together with a fair assessment of the uncertainty around forecasting. Warming of water temperature forecast by our hierarchical Bayesian model was slower and more uncertain than that expected with the classical regression approach. These new forecasts are in a form that is readily usable in further ecological analyses and will allow weighting of outcomes from different scenarios to manage climate change impacts on freshwater wildlife.

Understanding admixture patterns in supplemented populations: a case study combining molecular analyses and temporally explicit simulations in Atlantic salmon.

Genetic admixture between wild and introduced populations is a rising concern for the management of endangered species. Here, we use a dual approach based on molecular analyses of samples collected before and after hatchery fish introduction in combination with a simulation study to obtain insight into the mechanisms of admixture in wild populations. Using 17 microsatellites, we genotyped pre- and post-stocking samples from four Atlantic salmon populations supplemented with non-native fish to estimate genetic admixture. We also used individual-based temporally explicit simulations based on realistic demographic and stocking data to predict the extent of admixture. We found a low admixture by hatchery stocks within prestocking samples but moderate to high values in post-stocking samples (from 12% to 60%). The simulation scenarios best fitting the real data suggested a 10-25 times lower survival of stocked fish relative to wild individuals. Simulations also suggested relatively high dispersal rates of stocked and wild fish, which may explain some high levels of admixture in weakly stocked populations and the persistence of indigenous genotypes in heavily stocked populations. This study overall demonstrates that combining genetic analyses with simulations can significantly improve the understanding of admixture mechanisms in wild populations.

Changes in the genetic structure of Atlantic salmon populations over four decades reveal substantial impacts of stocking and potential resiliency.

While the stocking of captive-bred fish has been occurring for decades and has had substantial immediate genetic and evolutionary impacts on wild populations, its long-term consequences have only been weakly investigated. Here, we conducted a spatiotemporal analysis of 1428 Atlantic salmon sampled from 1965 to 2006 in 25 populations throughout France to investigate the influence of stocking on the neutral genetic structure in wild Atlantic salmon (Salmo salar) populations. On the basis of the analysis of 11 microsatellite loci, we found that the overall genetic structure among populations dramatically decreased over the period studied. Admixture rates among populations were highly variable, ranging from a nearly undetectable contribution from donor stocks to total replacement of the native gene pool, suggesting extremely variable impacts of stocking. Depending on population, admixture rates either increased, remained stable, or decreased in samples collected between 1998 and 2006 compared to samples from 1965 to 1987, suggesting either rising, long-lasting or short-term impacts of stocking. We discuss the potential mechanisms contributing to this variability, including the reduced fitness of stocked fish and persistence of wild locally adapted individuals.