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.

Growth-enhanced salmon modify stream ecosystem functioning.

Use of fast-growing domesticated and/or genetically modified strains of fish is becoming increasingly common in aquaculture, increasing the likelihood of deliberate or accidental introductions into the wild. To date, their ecological impacts on ecosystems remain to be quantified. Here, using a controlled phenotype manipulation by implanting growth hormone in juvenile Atlantic salmon (Salmo salar), we found that growth-enhanced fish display changes in several phenotypic traits known to be important for ecosystem functioning, such as habitat use, morphology and excretion rate. Furthermore, these phenotypic changes were associated with significant impacts on the invertebrate community and key stream ecosystem functions such as primary production and leaf-litter decomposition. These findings provide novel evidence that introductions of growth-enhanced fish into the wild can affect the functioning of natural ecosystems and represent a form of intraspecific invasion. Consequently, environmental impact assessments of growth-enhanced organisms need to explicitly consider ecosystem-level effects.

Individual and group characteristics affecting nest building in sea lamprey (Petromyzon marinus L. 1758).

Nest building relates to reproductive effort, sexual selection, intersexual conflict and cooperation and may be linked to individual phenotype and interindividual interactions. In particular, larger individuals having more energy reserves are expected to build more, larger nests, without having to trade intrasexual competition for cooperative nest building. Capture-mark-recapture and nest survey of sea lamprey (Petromyzon marinus L. 1758) were combined to assess the relationship between individuals and nesting activity on a spawning ground, throughout a breeding season, during which 202 nests were observed and 114 individuals were captured. On average, males and females stayed 8.33 ± 1.02 and 3.57 ± 1.04 days on the spawning ground, visited 2.26 ± 1.72 and 1.67 ± 1.17 nests and encountered 2.33 ± 2.13 mates for males and 2.29 ± 1.32 mates for females, respectively, and the number of mates encountered increased with the number of nests visited. Body size had no effect on the duration of presence on spawning ground, number of nests visited, number of individuals per nest and sex ratio on nest or nest volume. Bigger nests were found at the end of the season and were not necessarily built by more individuals. This work brings insights on the mating system and cooperative nest building in sea lamprey and may inform managers who want to estimate sea lamprey populations via nest surveys.

The negative ecological impacts of a globally introduced species decrease with time since introduction.

While there is a long-history of biological invasions and their ecological impacts have been widely demonstrated across taxa and ecosystems, our knowledge on the temporal dynamic of these impacts remains extremely limited. Using a meta-analytic approach, we investigated how the ecological impacts of non-native brown trout (Salmo trutta), a model species with a 170-year-long and well-documented history of intentional introductions across the globe, vary with time since introduction. We first observed significant negative ecological impacts immediately after the species introduction. Second, we found that the negative ecological impacts decrease with time since introduction and that the average ecological impacts become nonsignificant more than one century after introduction. This pattern was consistent across other ecological contexts (i.e., geographical location, levels of biological organization, and methodological approach). However, overall negative ecological impacts were more pronounced at the individual and population levels and in experimental studies. While the mechanisms leading to this decrease remain to be determined, our results indicate that rapid response of native organisms (e.g. adaptation, but also local extinction) may play an important role in this dynamic. Changes in native species traits and local extinction can have important conservation implications. Therefore, we argue that the decline of the negative ecological impacts over time should not be used as an argument to neglect the negative impacts of biological invasions.

Response to Comment on "Precipitation drives global variation in natural selection".

The comment by Myers-Smith and Myers focuses on three main points: (i) the lack of a mechanistic explanation for climate-selection relationships, (ii) the appropriateness of the climate data used in our analysis, and (iii) our focus on estimating climate-selection relationships across (rather than within) taxonomic groups. We address these critiques in our response.

The functional syndrome: linking individual trait variability to ecosystem functioning.

Phenotypic variability is increasingly assessed through functional response and effect traits, which provide a mechanistic framework for investigating how an organism responds to varying ecological factors and how these responses affect ecosystem functioning. Covariation between response and effect traits has been poorly examined at the intraspecific level, thus hampering progress in understanding how phenotypic variability alters the role of organisms in ecosystems. Using a multi-trait approach and a nine-month longitudinal monitoring of individual red-swamp crayfish (Procambarus clarkii), we demonstrated that most of the measured response and effect traits were partially stable during the ontogeny of individuals. Suites of response and effect traits were associated with a response syndrome and an effect syndrome, respectively, which were correlated to form a functional syndrome. Using a bioenergetic model, we predicted that differences in the response syndrome composition of hypothetical populations had important ecological effects on a key ecosystem process (i.e. whole-lake litter decomposition) to a level similar to those induced by doubling population size. Demonstrating the existence of a functional syndrome is likely to improve our understanding of the ecological impacts of phenotypic variation among individuals in wild populations across levels of biological organization, and the linkage between ecosystem and evolutionary ecology.

Precipitation drives global variation in natural selection.

Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation-natural selection-are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Genetic architecture of threshold reaction norms for male alternative reproductive tactics in Atlantic salmon (Salmo salar L.).

Alternative mating tactics have important ecological and evolutionary implications and are determined by complex interactions between environmental and genetic factors. Here, we study the genetic effect and architecture of the variability in reproductive tactics among Atlantic salmon males which can either mature sexually early in life in freshwater or more commonly only after completing a migration at sea. We applied the latent environmental threshold model (LETM), which provides a conceptual framework linking individual status to a threshold controlling the decision to develop alternative traits, in an innovative experimental design using a semi-natural river which allowed for ecologically relevant phenotypic expression. Early male parr maturation rates varied greatly across families (10 to 93%) which translated into 90% [64-100%] of the phenotypic variation explained by genetic variation. Three significant QTLs were found for the maturation status, however only one collocated with a highly significant QTL explaining 20.6% of the variability of the maturation threshold located on chromosome 25 and encompassing a locus previously shown to be linked to sea age at maturity in anadromous Atlantic salmon. These results provide new empirical illustration of the relevance of the LETM for a better understanding of alternative mating tactics evolution in natural populations.

Global Salmonidae introductions reveal stronger ecological effects of changing intraspecific compared to interspecific diversity.

The introduction of organisms within the native range of wild conspecifics is a widespread phenomenon and locally modifies patterns in intraspecific diversity. However, our knowledge of the resulting ecological effects, as opposed to those caused by invasion-induced changes in interspecific diversity, is still limited. Here, we investigated the ecological effects of native and non-native invaders across levels of biological organisations and recipient organisms using the global and long history introductions of salmonids. Our meta-analysis demonstrated that the global effects of native species introductions exceeded those induced by non-native invaders. The impacts of native invaders were primarily manifested at the individual level on wild conspecifics, but remained largely unexplored on other native organisms and at the community and ecosystem levels. Overlooked and poorly appreciated, quantifying the impacts of native invaders has important implications because human-assisted introductions of domesticated organisms are ubiquitous and likely to proliferate in the future.

Phenological response of a key ecosystem function to biological invasion.

Although climate warming has been widely demonstrated to induce shifts in the timing of many biological events, the phenological consequences of other prominent global change drivers remain largely unknown. Here, we investigated the effects of biological invasions on the seasonality of leaf litter decomposition, a crucial freshwater ecosystem function. Decomposition rates were quantified in 18 temperate shallow lakes distributed along a gradient of crayfish invasion and a temperature-based model was constructed to predict yearly patterns of decomposition. We found that, through direct detritus consumption, omnivorous invasive crayfish accelerated decomposition rates up to fivefold in spring, enhancing temperature dependence of the process and shortening the period of major detritus availability in the ecosystem by up to 39 days (95% CI: 15-61). The fact that our estimates are an order of magnitude higher than any previously reported climate-driven phenological shifts indicates that some powerful drivers of phenological change have been largely overlooked.

Shifting Thresholds: Rapid Evolution of Migratory Life Histories in Steelhead/Rainbow Trout, Oncorhynchus mykiss.

Expression of phenotypic plasticity depends on reaction norms adapted to historic selective regimes; anthropogenic changes in these selection regimes necessitate contemporary evolution or declines in productivity and possibly extinction. Adaptation of conditional strategies following a change in the selection regime requires evolution of either the environmentally influenced cue (e.g., size-at-age) or the state (e.g., size threshold) at which an individual switches between alternative tactics. Using a population of steelhead (Oncorhynchus mykiss) introduced above a barrier waterfall in 1910, we evaluate how the conditional strategy to migrate evolves in response to selection against migration. We created 9 families and 917 offspring from 14 parents collected from the above- and below-barrier populations. After 1 year of common garden-rearing above-barrier offspring were 11% smaller and 32% lighter than below-barrier offspring. Using a novel analytical approach, we estimate that the mean size at which above-barrier fish switch between the resident and migrant tactic is 43% larger than below-barrier fish. As a result, above-barrier fish were 26% less likely to express the migratory tactic. Our results demonstrate how rapid and opposing changes in size-at-age and threshold size contribute to the contemporary evolution of a conditional strategy and indicate that migratory barriers may elicit rapid evolution toward the resident life history on timescales relevant for conservation and management of conditionally migratory species.

Investigating the genetic architecture of conditional strategies using the environmental threshold model.

The threshold expression of dichotomous phenotypes that are environmentally cued or induced comprise the vast majority of phenotypic dimorphisms in colour, morphology, behaviour and life history. Modelled as conditional strategies under the framework of evolutionary game theory, the quantitative genetic basis of these traits is a challenge to estimate. The challenge exists firstly because the phenotypic expression of the trait is dichotomous and secondly because the apparent environmental cue is separate from the biological signal pathway that induces the switch between phenotypes. It is the cryptic variation underlying the translation of cue to phenotype that we address here. With a 'half-sib common environment' and a 'family-level split environment' experiment, we examine the environmental and genetic influences that underlie male dimorphism in the earwig Forficula auricularia. From the conceptual framework of the latent environmental threshold (LET) model, we use pedigree information to dissect the genetic architecture of the threshold expression of forceps length. We investigate for the first time the strength of the correlation between observable and cryptic 'proximate' cues. Furthermore, in support of the environmental threshold model, we found no evidence for a genetic correlation between cue and the threshold between phenotypes. Our results show strong correlations between observable and proximate cues and less genetic variation for thresholds than previous studies have suggested. We discuss the importance of generating better estimates of the genetic variation for thresholds when investigating the genetic architecture and heritability of threshold traits. By investigating genetic architecture by means of the LET model, our study supports several key evolutionary ideas related to conditional strategies and improves our understanding of environmentally cued decisions.

Life-history syndromes: integrating dispersal through space and time.

Recent research has highlighted interdependencies between dispersal and other life-history traits, i.e. dispersal syndromes, thereby revealing constraints on the evolution of dispersal and opportunities for improved ability to predict dispersal by considering suites of dispersal-related traits. This review adds to the growing list of life-history traits linked to spatial dispersal by emphasising the interdependence between dispersal through space and time, i.e. life-history diversity that distributes individuals into separate reproductive events. We reviewed the literature that has simultaneously investigated spatial and temporal dispersal to examine the prediction that traits of these two dispersal strategies are negatively correlated. Our results suggest that negative covariation is widely anticipated from theory. Empirical studies often reported evidence of weak negative covariation, although more complicated patterns were also evident, including across levels of biological organisation. Existing literature has largely focused on plants with dormancy capability, one or two phases of the dispersal process (emigration and/or transfer) and a single level of biological organisation (theory: individual; empirical: species). We highlight patterns of covariation across levels of organisation and conclude with a discussion of the consequences of dispersal through space and time and future research areas that should improve our understanding of dispersal-related life-history syndromes.

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.

Assessing whether mortality is additive using marked animals: a Bayesian state-space modeling approach.

Whether different sources of mortality are additive, compensatory, or depensatory is a key question in population biology. A way to test for additivity is to calculate the correlation between cause-specific mortality rates obtained from marked animals. However, existing methods to estimate this correlation raise several methodological issues. One difficulty is the existence of an intrinsic bias in the correlation parameter. Although this bias can be formally expressed, it requires knowledge about natural survival without any competing mortality source, which is difficult to assess in most cases. Another difficulty lies in estimating the true process correlation while properly accounting for sampling variation. Using a Bayesian approach, we developed a state-space model to assess the correlation between two competing sources of mortality. By distinguishing the mortality process from its observation through dead recoveries and live recaptures, we estimated the process correlation. To correct for the intrinsic bias, we incorporated experts' opinions on natural survival. We illustrated our approach using data on a hunted population of wild boars. Mortalities were not additive and natural mortality increased with hunting mortality likely as a consequence of non-controlled mortality by crippling loss. Our method opens perspectives for wildlife management and for the conservation of endangered species.

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.