Etienne Prévost

Contrasting effects of climate change in continental vs. oceanic environments on population persistence and microevolution of Atlantic salmon

Facing climate change (CC), species are prone to multiple modifications in their environment that can lead to extinction, migration or adaptation. Identifying the role and interplay of different potential stressors becomes a key question. Anadromous fishes will be exposed to both river and oceanic habitat changes. For Atlantic salmon, the river water temperature, river flow and oceanic growth conditions appear as three main stressing factors. They could act on population dynamics or as selective forces on life-history pathways. Using an individual-based demo-genetic model, we assessed the effects of these factors (1) to compare risks of extinction resulting from CC in river and ocean, and (2) to assess CC effects on life-history pathways including the evolution of underlying genetic control of phenotypic plasticity. We focused on Atlantic salmon populations from Southern Europe for a time horizon of three decades. We showed that CC in river alone should not lead to extinction of Southern European salmon populations. In contrast, the reduced oceanic growth appeared as a significant threat for population persistence. An increase in river flow amplitude increased the risk of local extinction in synergy with the oceanic effects, but river temperature rise reduced this risk. In terms of life-history modifications, the reduced oceanic growth increased the age of return of individuals through plastic and genetic responses. The river temperature rise increased the proportion of sexually mature parr, but the genetic evolution of the maturation threshold lowered the maturation rate of male parr. This was identified as a case of environmentally driven plastic response that masked an underlying evolutionary response of plasticity going in the opposite direction. We concluded that to counteract oceanic effects, river flow management represented the sole potential force to reduce the extinction probability of Atlantic salmon populations in Southern Europe, although this might not impede changes in migration life history.

Female preference for male body size in brown trout, Salmo trutta: is big still fashionable?

The study of female preference for male traits is of primary importance for understanding the role of sexual selection in the evolution of natural populations. Female preference is usually investigated in controlled conditions to facilitate the manipulation of variables. However, such results are rarely confirmed in wild populations where many variables act together. Inferring the role of female preference in the outcome of reproduction thus requires field studies and a specific approach to behavioural data. We observed, over 2 years, the courtship behaviours of male and female brown trout in six populations distributed along a French watershed. We focused on behavioural items linked to female preference for male body size. We built a behavioural model describing the relationships between behaviour and female preference and estimated the parameters of the model using a Bayesian modelling approach. We found a significant preference for body size ratio: females tended to prefer males at least 1.45 times their own size. This preference varied between populations and was influenced by female size. Operational sex ratio had only a weak influence on female preference. Our model explained 44% of the observed variation in behaviour. Finally, because observed body size ratio at mating was generally greater than 1, we conclude that female preference plays a major role in the outcome of reproduction in wild populations of brown trout. These results are compared with existing knowledge and theory and their possible consequences at the population level are discussed.

Effect of water temperature and density of juvenile salmonids on growth of young‐of‐the‐year Atlantic salmon Salmo salar

A von Bertalanffy growth model for young-of the-year Atlantic salmon Salmo salar in a small French coastal stream was fitted using water temperatures and densities of juvenile salmonids (S. salar and brown trout Salmo trutta) as covariates influencing daily growth rate. The Bayesian framework was used as a template to integrate prior information from external data sets. The relative influence of the covariates on parr growth was quantified and results showed that growth of S. salar juveniles depended on both water temperatures and densities, but that most of the spatiotemporal variability of growth resulted from local spatiotemporal variations of 0+ age salmonid (S. salar and S. trutta) densities. Further analysis revealed that the fluctuations in young-of-the-year salmonid densities are likely to dominate the effects of potential future warming of water temperature due to climate change. It is concluded that factors that could affect salmonid densities might well have a greater effect on S. salar population dynamics than factors influencing water temperatures.

ASSESSING ADAPTIVE PHENOTYPIC PLASTICITY BY MEANS OF CONDITIONAL STRATEGIES FROM EMPIRICAL DATA: THE LATENT ENVIRONMENTAL THRESHOLD MODEL

Conditional strategies are the most common form of discrete phenotypic plasticity. In a conditional strategy, the phenotype expressed by an organism is determined by the difference between an environmental cue and a threshold, both of which may vary among individuals. The environmental threshold model (ETM) has been proposed as a mean to understand the evolution of conditional strategies, but has been surprisingly seldom applied to empirical studies. A hindrance for the application of the ETM is that often, the proximate cue triggering the phenotypic expression and the individual threshold are not measurable, and can only be assessed using a related observable cue. We describe a new statistical model that can be applied in this common situation. The Latent ETM (LETM) allows for a measurement error in the phenotypic expression of the individual environmental cue and a purely genetically determined threshold. We show that coupling our model with quantitative genetic methods allows an evolutionary approach including an estimation of the heritability of conditional strategies. We evaluate the performance of the LETM with a simulation study and illustrate its utility by applying it to empirical data on the size‐dependent smolting process for stream‐dwelling Atlantic salmon juveniles.

INVESTIGATING EVOLUTIONARY TRADE-OFFS IN WILD POPULATIONS OF ATLANTIC SALMON (SALMO SALAR): INCORPORATING DETECTION PROBABILITIES AND INDIVIDUAL HETEROGENEITY

Evolutionary trade‐offs among demographic parameters are important determinants of life‐history evolution. Investigating such trade‐offs under natural conditions has been limited by inappropriate analytical methods that fail to address the bias in demographic estimates that can result when issues of detection (uncertain detection of individual) are ignored. We propose a new statistical approach to quantify evolutionary trade‐offs in wild populations. Our method is based on a state‐space modeling framework that focuses on both the demographic process of interest as well as the observation process. As a case study, we used individual mark–recapture data for stream‐dwelling Atlantic salmon juveniles in the Scorff River (Southern Brittany, France). In freshwater, juveniles face two life‐history choices: migration to the ocean and sexual maturation (for males). Trade‐offs may appear with these life‐history choices and survival, because all are energy dependent. We found a cost of reproduction on survival for fish staying in freshwater and a survival advantage associated with the “decision” to migrate. Our modeling framework opens up promising prospects for the study of evolutionary trade‐offs when some life‐history traits are not, or only partially, observable.

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.

Invasion Dynamics of a Fish-Free Landscape by Brown Trout (Salmo trutta)

Metapopulation dynamics over the course of an invasion are usually difficult to grasp because they require large and reliable data collection, often unavailable. The invasion of the fish-free freshwater ecosystems of the remote sub-Antarctic Kerguelen Islands following man-made introductions of brown trout (Salmo trutta) in the 1950s is an exception to this rule. Benefiting from a full long term environmental research monitoring of the invasion, we built a Bayesian dynamic metapopulation model to analyze the invasion dynamics of 85 river systems over 51 years. The model accounted for patch size (river length and connections to lakes), alternative dispersal pathways between rivers, temporal trends in dynamics, and uncertainty in colonization date. The results show that the model correctly represents the observed pattern of invasion, especially if we assume a coastal dispersal pathway between patches. Landscape attributes such as patch size influenced the colonization function, but had no effect on propagule pressure. Independently from patch size and distance between patches, propagule pressure and colonization function were not constant through time. Propagule pressure increased over the course of colonization, whereas the colonization function decreased, conditional on propagule pressure. The resulting pattern of this antagonistic interplay is an initial rapid invasion phase followed by a strong decrease in the invasion rate. These temporal trends may be due to either adaptive processes or environmental gradients encountered along the colonization front. It was not possible to distinguish these two hypotheses. Because invasibility of Kerguelen Is. freshwater ecosystems is very high due to the lack of a pre-existing fish fauna and minimal human interference, our estimates of invasion dynamics represent a blueprint for the potential of brown trout invasiveness in pristine environments. Our conclusions shed light on the future of polar regions where, because of climate change, fish-free ecosystems become increasingly accessible to invasion by fish species.

Digging through model complexity: using hierarchical models to uncover evolutionary processes in the wild

The growing interest for studying questions in the wild requires acknowledging that eco‐evolutionary processes are complex, hierarchically structured and often partially observed or with measurement error. These issues have long been ignored in evolutionary biology, which might have led to flawed inference when addressing evolutionary questions. Hierarchical modelling (HM) has been proposed as a generic statistical framework to deal with complexity in ecological data and account for uncertainty. However, to date, HM has seldom been used to investigate evolutionary mechanisms possibly underlying observed patterns. Here, we contend the HM approach offers a relevant approach for the study of eco‐evolutionary processes in the wild by confronting formal theories to empirical data through proper statistical inference. Studying eco‐evolutionary processes requires considering the complete and often complex life histories of organisms. We show how this can be achieved by combining sequentially all life‐history components and all available sources of information through HM. We demonstrate how eco‐evolutionary processes may be poorly inferred or even missed without using the full potential of HM. As a case study, we use the Atlantic salmon and data on wild marked juveniles. We assess a reaction norm for migration and two potential trade‐offs for survival. Overall, HM has a great potential to address evolutionary questions and investigate important processes that could not previously be assessed in laboratory or short time‐scale studies.

Evidence for long-term change in length, mass and migration phenology of anadromous spawners in French Atlantic salmon Salmo salar

This study provides new data on Atlantic salmon Salmo salar life-history traits across France. Using a long-term recreational angling database (1987-2013) covering 34 rivers in three regions (genetic units), a decline in individual length, mass and a delayed adult return to French rivers was reported. Temporal similarities in trait variations between regions may be attributed to common change in environmental conditions at sea. The relative rate of change in phenotypic traits was more pronounced in early maturing fish [1 sea-winter (1SW) fish] than in late maturing fish (2SW fish). Such contrasted response within populations highlights the need to account for the diversity in life histories when exploring mechanisms of phenotypic change in S. salar. Such detailed life-history data on returning S. salar have not previously been reported from France. This study on French populations also contributes to reducing the gap in knowledge by providing further empirical evidence of a global pattern in S. salar across its distribution range. Results are consistent with the hypothesis that the observed changes in life-history traits are primarily associated with environmental changes in the North Atlantic Ocean. They also emphasize the presence of less important, but still significant contrasts between region and life history.