Importance of interindividual interactions in eco-evolutionary population dynamics: The rise of demo-genetic agent-based models.

The study of eco-evolutionary dynamics, that is of the intertwinning between ecological and evolutionary processes when they occur at comparable time scales, is of growing interest in the current context of global change. However, many eco-evolutionary studies overlook the role of interindividual interactions, which are hard to predict and yet central to selective values. Here, we aimed at putting forward models that simulate interindividual interactions in an eco-evolutionary framework: the demo-genetic agent-based models (DG-ABMs). Being demo-genetic, DG-ABMs consider the feedback loop between ecological and evolutionary processes. Being agent-based, DG-ABMs follow populations of interacting individuals with sets of traits that vary among the individuals. We argue that the ability of DG-ABMs to take into account the genetic heterogeneity-that affects individual decisions/traits related to local and instantaneous conditions-differentiates them from analytical models, another type of model largely used by evolutionary biologists to investigate eco-evolutionary feedback loops. Based on the review of studies employing DG-ABMs and explicitly or implicitly accounting for competitive, cooperative or reproductive interactions, we illustrate that DG-ABMs are particularly relevant for the exploration of fundamental, yet pressing, questions in evolutionary ecology across various levels of organization. By jointly modelling the effects of management practices and other eco-evolutionary processes on interindividual interactions and population dynamics, DG-ABMs are also effective prospective and decision support tools to evaluate the short- and long-term evolutionary costs and benefits of management strategies and to assess potential trade-offs. Finally, we provide a list of the recent practical advances of the ABM community that should facilitate the development of DG-ABMs.

Genotype-by-environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone.

Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation of native populations or hybridization. However, the mechanisms leading to these situations are not always explicitly documented and are thus rarely used to manage intraspecific diversity. In particular, genotype-by-environment (GxE) interactions can drive postzygotic reproductive isolation mechanisms that may result in a mosaic of diversity patterns, depending on the local environment. We test this hypothesis using a salmonid species (Salmo trutta) in the Mediterranean (MED) area, where intensive stocking from non-native Atlantic (ATL) origins has led to various outcomes of hybridization with the native MED lineage, going from MED resilience to total extirpation via full hybridization. We investigate patterns of offspring survival at egg stage in natural environments, based on parental genotypes in interaction with river temperature, to detect potential GxE interactions. Our results show a strong influence of maternal GxE interaction on embryonic survival, mediated by maternal effect through egg size, and a weak influence of paternal GxE interaction. In particular, when egg size is large and temperature is cold, the survival rate of offspring originating from MED females is three times higher than that of ATL females' offspring. Because river temperatures show contrast at small scale, this cold adaptation for MED females' offspring constitutes a potent postzygotic mechanism to explain small-scale spatial heterogeneity in diversity observed in MED areas where ATL fish have been stocked. It also indicates that management efforts could be specifically targeted at the environments that actively favor native intraspecific diversity through eco-evolutionary processes such as postzygotic selection.

Theory of environmental sex determination: Trending populations in stressful environments.

Species that have sex determined by environmental conditions during development (i.e., environmental sex determination [ESD]) are especially vulnerable to environmental change, including altered stress levels, habitat loss, and species translocations. These factors can produce multigenerational trends in population size and eco-evolutionary dynamics not captured by existing theory based on lifetime reproductive success (R0 ). Here, we extend ESD theory to use per capita growth rate r as a more appropriate measure of evolutionary success (fitness), and we demonstrate the importance of this change when males and females can differ in maturation times and when maturation times vary with local conditions (plasticity). In these cases, we show that primary and secondary sex ratios may be strongly biased; that optimal maturation times, when locally plastic, depend on the balance between mortality and growth effects; and that plasticity of maturation times can ameliorate fitness costs of increasing environmental stress.

Using Reciprocal Transplants to Assess Local Adaptation, Genetic Rescue, and Sexual Selection in Newly Established Populations.

Small populations establishing on colonization fronts have to adapt to novel environments with limited genetic variation. The pace at which they can adapt, and the influence of genetic variation on their success, are key questions for understanding intraspecific diversity. To investigate these topics, we performed a reciprocal transplant experiment between two recently founded populations of brown trout in the sub-Antarctic Kerguelen Islands. Using individual tagging and genetic assignment methods, we tracked the fitness of local and foreign individuals, as well as the fitness of their offspring over two generations. In both populations, although not to the same extent, gene flow occurred between local and foreign gene pools. In both cases, however, we failed to detect obvious footprints of local adaptation (which should limit gene flow) and only weak support for genetic rescue (which should enhance gene flow). In the population where gene flow from foreign individuals was low, no clear differences were observed between the fitness of local, foreign, and F1 hybrid individuals. In the population where gene flow was high, foreign individuals were successful due to high mating success rather than high survival, and F1 hybrids had the same fitness as pure local offspring. These results suggest the importance of considering sexual selection, rather than just local adaptation and genetic rescue, when evaluating the determinants of success in small and recently founded populations.

Fluctuating Dynamics of Mate Availability Promote the Evolution of Flexible Choosiness in Both Sexes.

AbstractThe evolution of choosiness has a strong effect on sexual selection, as it promotes variance in mating success among individuals. The context in which choosiness is expressed, and therefore the associated gain and cost, is highly variable. An overlooked mechanism by current models is the rapid fluctuations in the availability and quality of partners, which generates a dynamic mating market to which each individual must optimally respond. We argue that the rapid fluctuations of the mating market are central to the evolution of optimal choosiness. Using a dynamic game approach, we investigate this hypothesis for various mating systems (characterized by different adult sex ratio and latency period combinations), allowing feedback between the choosiness and partner availability throughout a breeding season while taking into account the fine variation in individual quality. Our results indicate that quality-dependent and flexible choosiness usually evolve in both sexes for various mating systems and that a significant amount of variance in choosiness is observed, especially in males, even when courtship is costly. Accounting for the fluctuating dynamics of the mating market therefore allows envisioning a much wider range of choosiness variation in natural populations and may explain a number of recent empirical results regarding choosiness in the less common sex or its variance within sexes.

New insights into methylmercury induced behavioral and energy-related gene transcriptional responses in European glass eel (Anguilla anguilla).

The effect of methylmercury (MeHg) was investigated in glass eel migration behavior and metabolism. To migrate up estuary, glass eels synchronize their swimming activity to the flood tide and remain on or in the substratum during ebb tide. Following seven days of exposure to MeHg (100 ng L-1), glass eels migration behavior was expressed by their swimming synchronization to the water current reversal every 6.2 h (mimicking the alternation of flood and ebb tides) and their swimming activity level. In relation to their behavior, we then analyzed the energy-related gene expression levels in individual head, viscera and muscle. Results showed that MeHg decreased the number of glass eels synchronized to the change in water current direction and their swimming activity level. This last effect was more pronounced in non-synchronized fish than in synchronized ones, supporting the idea that non-synchronized glass eels could be more vulnerable to stress. As regard the expression of energy-related genes, no significant difference was observed between control and MeHg-exposed fish. In contrast, when the swimming activity levels were plotted against transcriptional responses, positive correlations were evidenced in viscera and especially in the head of exposed glass eels but not in control. Finally, it is noteworthy that non-synchronized glass eels displayed lower expression level of metabolism genes than their synchronized counterpart, but only in the head. Altogether, these results support the interest of focusing on the head to investigate the facultative migration behavior in glass eels and the effect of environmental stressors on this rhythmic behavior.

A reassessment of the carnivorous status of salmonids: Hepatic glucokinase is expressed in wild fish in Kerguelen Islands.

Salmonids belong to a high trophic level and are thus considered as strictly carnivorous species, metabolically adapted for high catabolism of proteins and low utilisation of dietary carbohydrates. However they conserved a "mammalian-type" nutritional regulation of glucokinase encoding gene and its enzymatic activity by dietary carbohydrates which remains puzzling regarding their dietary regime. The present study investigates the hypothesis that this conservation could be linked to a real consumption by trout of this nutrient in their natural habitat. To do so, brown trout were sampled in the sub-Antarctic Kerguelen Islands, a site presenting oligotrophic hydrosystems and no local freshwater fish fauna prior the introduction of salmonids fifty years ago. Qualitative and quantitative analysis of carbohydrate content within Kerguelen trout stomachs demonstrate that these animals are fed on food resources containing digestible carbohydrates. Additionally, glycaemia and more particularly gck mRNA level and gck enzymatic activity prove that Kerguelen trout digest and metabolise dietary carbohydrates. Physiological and molecular analyses performed in the present study thus strongly evidence for consumption of dietary carbohydrates by wild trout in natural environments. Investigating differences between Kerguelen individuals, we found that smaller individuals presented higher glycaemia, as well as higher carbohydrates contents in stomach. However no relationship between scaled mass index and any physiological indicator was found. Thus it appears that Kerguelen trout do not turn to carbohydrate diet because of a different condition index, or that the consumption of carbohydrates does not lead to a generally degraded physiological status. As a conclusion, our findings may explain the evolutionary conservation of a "mammalian-type" nutritional regulation of gck by dietary carbohydrates in these carnivorous fish.

Modeling of autophagy-related gene expression dynamics during long term fasting in European eel (Anguilla anguilla).

Autophagy is an evolutionary conserved cellular self-degradation process considered as a major energy mobilizing system in eukaryotes. It has long been considered as a post-translationally regulated event, and the importance of transcriptional regulation of autophagy-related genes (atg) for somatic maintenance and homeostasis during long period of stress emerged only recently. In this regard, large changes in atg transcription have been documented in several species under diverse types of prolonged catabolic situations. However, the available data primarily concern atg mRNA levels at specific times and fail to capture the dynamic relationship between transcript production over time and integrated phenotypes. Here, we present the development of a statistical model describing the dynamics of expression of several atg and lysosomal genes in European glass eel (Anguilla anguilla) during long-term fasting at two temperatures (9 °C and 12 °C) and make use of this model to infer the effect of transcripts dynamics on an integrated phenotype - here weight loss. Our analysis shows long-term non-random fluctuating atg expression dynamics and reveals for the first time a significant contribution of atg transcripts production over time to weight loss. The proposed approach thus offers a new perspective on the long-term transcriptional control of autophagy and its physiological role.

Experimental evidence of population differences in reproductive investment conditional on environmental stochasticity.

Environmental stochasticity is expected to shape life histories of species, wherein organisms subjected to strong environmental variation should display adaptive response by being able to tune their reproductive investment. For riverine ecosystems, climate models forecast an increase in the frequency and intensity of extreme events such as floods and droughts. The speed and the mechanisms by which organisms may adapt their reproductive investment are therefore of primary importance to understand how species will cope with such radical environmental changes. In the present study, we sampled spawners from two different populations of wild brown trout, originating from two environments with contrasting levels of flow stochasticity. We placed them in sympatry within an experimental channel during reproductive season. In one modality, water flow was maintained constant, whereas in another modality, water flow was highly variable. Reproductive investment of all individuals was monitored using weight and energetic plasma metabolite variation throughout the reproductive season. Only the populations originating from the most variable environment showed a plastic response to experimental manipulation of water flow, the females being able to reduce their weight variation (from 19.2% to 13.1%) and metabolites variations (from 84.2% to 18.6% for triglycerides for instance) under variable flow conditions. These results imply that mechanisms to cope with environmental stochasticity can differ between populations of the same species, where some populations can be plastic whereas other cannot.

The concentration of plasma metabolites varies throughout reproduction and affects offspring number in wild brown trout (Salmo trutta).

In wild populations, measuring energy invested in the reproduction and disentangling investment in gametes versus investment in reproductive behavior (such as intrasexual competition or intersexual preference) remain challenging. In this study, we investigated the energy expenditure in brown trout reproductive behavior by using two proxies: variation in weight and variation of plasma metabolites involved in energy production, over the course of reproductive season in a semi natural experimental river. We estimated overall reproductive success using genetic assignment at the end of the reproductive season. Results show that triglycerides and free fatty acid concentrations vary negatively during reproduction, while amino-acids and glucose concentrations remain stable. Decrease in triglyceride and free fatty acid concentrations during reproduction is not related to initial concentration levels or to weight variation. Both metabolite concentration variations and weight variations are correlated to the number of offspring produced, which could indicate that gametic and behavioral reproductive investments substantially contribute to reproductive success in wild brown trout. This study opens a path to further investigate variations in reproductive investment in wild populations.

No early gender effects on energetic status and life history in a salmonid.

Throughout an organism's early development, variations in physiology and behaviours may have long lasting consequences on individual life histories. While a large part of variation in critical life-history transitions remains unexplained, a significant proportion may be caused by early gender effects as part of gender-specific life histories shaped by sexual selection. In this study, we investigated the presence of early gender effects on the timing of emergence from gravel and the energetic status of brown trout (Salmo trutta) early stages. To investigate this question, individual measures of emergence timing, metabolic rate and energetic content were coupled for the first time with the use of a recent genetic marker for sdY (sexually dimorphic on the Y-chromosome), a master sex-determining gene. Our results show that gender does not influence the energetic content of emerging juveniles or their emergence timing. These findings suggest that gender differences may appear later throughout salmonid life history and that selective pressures associated with the critical period of emergence from gravel may shape early life-history traits similarly in both males and females.

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 1950's 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.

Female effects on offspring energetic status and consequences on early development in yolk feeding brown trout (Salmo trutta).

Energetic status can be defined as the interaction between energy stores and metabolic rate. In salmonids, it is variable and influences the timing of emergence, and therefore may have strong effects on both juvenile and maternal fitness. The aim of this study is to (i) describe the ontogeny of energy use for different brown trout clutches to understand how such a variability of energetic status is developed at the end of incubation and (ii) to estimate maternal influences over offspring physiological processes. Using individual measures of total mass and metabolism throughout ontogeny combined with a hierarchical Bayesian modeling approach, we successfully described clutch-specific (i) metabolic trajectories, (ii) use of yolk resources and the building of new tissues throughout ontogeny. Our results show that females laying large eggs have offspring with lower metabolic costs and higher yolk conversion efficiencies. Females also influence within clutch variance of metabolic and yolk consumption rates leading to potential developmental variations. These results are discussed with regard to their consequences on early life history through the critical period of emergence.

Influence of energetic status on ontogenetic niche shifts: emergence from the redd is linked to metabolic rate in brown trout.

Ontogenetic niche shift should occur when the ratio of growth opportunities to mortality risk becomes higher in the subsequent habitat. While most studies have focused on size to understand the timing of these shifts, an endogenous factor like energetic status (interaction between energy available and energy requirements) appears as a natural candidate to integrate and analyze the growth trade-off between habitats. In this study, we measure energetic content and metabolic rate of individual brown trout (Salmo trutta) fry at emergence from gravel to investigate the influence of energetic status on the timing of this critical ontogenetic niche shift. In addition, as offspring energetic status is subject to parental effects, we examine how females could maximize their own fitness by influencing offspring emergence timing. Our results demonstrate that emergence from gravel is influenced by energetic status. Individuals that emerge first have a higher energetic content but deplete it faster because of a higher metabolic rate. We also find that female fecundity is positively related to emergence period duration. Moreover, our results suggest that females may decrease kin competition during the critical period of emergence by influencing the energetic status of offspring, thus, maximizing their own fitness. Our results help elucidate the mechanisms underlying early ontogenetic niche shifts in juvenile fish and suggest reasons why maternal investment can be so variable within populations.

Natural and sexual selection giveth and taketh away reproductive barriers: models of population divergence in guppies.

The standard predictions of ecological speciation might be nuanced by the interaction between natural and sexual selection. We investigated this hypothesis with an individual-based model tailored to the biology of guppies (Poecilia reticulata). We specifically modeled the situation where a high-predation population below a waterfall colonizes a low-predation population above a waterfall. Focusing on the evolution of male color, we confirm that divergent selection causes the appreciable evolution of male color within 20 generations. The rate and magnitude of this divergence were reduced when dispersal rates were high and when female choice did not differ between environments. Adaptive divergence was always coupled to the evolution of two reproductive barriers: viability selection against immigrants and hybrids. Different types of sexual selection, however, led to contrasting results for another potential reproductive barrier: mating success of immigrants. In some cases, the effects of natural and sexual selection offset each other, leading to no overall reproductive isolation despite strong adaptive divergence. Sexual selection acting through female choice can thus strongly modify the effects of divergent natural selection and thereby alter the standard predictions of ecological speciation. We also found that under no circumstances did divergent selection cause appreciable divergence in neutral genetic markers.

Occurrence and variation of egg cannibalism in brown trout Salmo trutta.

Egg cannibalism is a common behavior among fish taxa and is largely studied in species with parental care. Heterocannibalism and filial cannibalism have both been reported in salmonids, a group with no extended parental care, but the topic remained somewhat under-documented, especially in brown trout (Salmo trutta). In the present study, 83 spawning events were recorded finely with high-resolution video in three natural populations. Redd covering dynamics by females and the timing of cannibalism showed that eggs were vulnerable mainly during the first 120 s after spawning. Cannibalism occurred in 25% of spawnings and was principally perpetrated by peripherals but the sires also cannibalized their brood, especially after multiple mating. The probability of cannibalism increased with operational sex ratio but did not correlate with the date in spawning season. Occurrence of cannibalism also differed between populations. Our results suggest that such behavior is frequent and may reduce the fitness of parents. Its evolutionary implications for population ecology should be considered, since it appeared to be controlled by environmental and spatial factors.

Assessing maternal effects on metabolic rate dynamics along early development in brown trout (Salmo trutta): an individual-based approach.

Routine metabolic rate (oxygen consumption) of individual eggs and larvae of brown trout (Salmo trutta) originating from different families were monitored from fertilisation to the onset of emergence by means of flow through micro-respirometry. This measuring system revealed an accurate tool to measure oxygen consumption on small organisms at the individual level, and daily consumption proved to be very stable. The mass-specific metabolic rate remained low from fertilisation to hatching, and then increased quickly until the age of emergence. A Bayesian modelling approach was used to adequately infer maternal effects on metabolic rate dynamics all along the development period. Substantial differences were found between families, affecting average metabolic rate as well as intra-family variance. That is, offspring originating from different females may have different energetic needs at emergence from gravel. Moreover, between siblings, variability in metabolic rate is also under the influence of maternal effects. Implications of this metabolic rate variability are discussed with regard to life history strategies and early behaviours.