Transgenerational effects of mild heat in Arabidopsis thaliana show strong genotype specificity that is explained by climate at origin.

Transgenerational environmental effects can trigger strong phenotypic variation. However, it is unclear how cues from different preceding generations interact. Also, little is known about the genetic variation for these life history traits. Here, we present the effects of grandparental and parental mild heat, and their combination, on four traits of the third-generation phenotype of 14 Arabidopsis thaliana genotypes. We tested for correlations of these effects with climate and constructed a conceptual model to identify the environmental conditions that favour the parental effect on flowering time. We observed strong evidence for genotype-specific transgenerational effects. On average, A. thaliana accustomed to mild heat produced more seeds after two generations. Parental effects overruled grandparental effects in all traits except reproductive biomass. Flowering was generally accelerated by all transgenerational effects. Notably, the parental effect triggered earliest flowering in genotypes adapted to dry summers. Accordingly, this parental effect was favoured in the model when early summer heat terminated the growing season and environments were correlated across generations. Our results suggest that A. thaliana can partly accustom to mild heat over two generations and genotype-specific parental effects show non-random evolutionary divergence across populations that may support climate change adaptation in the Mediterranean.

Evolving mutation rate advances the invasion speed of a sexual species.

BACKGROUND: Many species are shifting their ranges in response to global climate change. Range expansions are known to have profound effects on the genetic composition of populations. The evolution of dispersal during range expansion increases invasion speed, provided that a species can adapt sufficiently fast to novel local conditions. Genetic diversity at the expanding range border is however depleted due to iterated founder effects. The surprising ability of colonizing species to adapt to novel conditions while being subjected to genetic bottlenecks is termed 'the genetic paradox of invasive species'. Mutational processes have been argued to provide an explanation for this paradox. Mutation rates can evolve, under conditions that favor an increased rate of adaptation, by hitchhiking on beneficial mutations through induced linkage disequilibrium. Here we argue that spatial sorting, iterated founder events, and population structure benefit the build-up and maintenance of such linkage disequilibrium. We investigate if the evolution of mutation rates could play a role in explaining the 'genetic paradox of invasive species' for a sexually reproducing species colonizing a landscape of gradually changing conditions. RESULTS: We use an individual-based model to show the evolutionary increase of mutation rates in sexual populations during range expansion, in coevolution with the dispersal probability. The observed evolution of mutation rate is adaptive and clearly advances invasion speed both through its effect on the evolution of dispersal probability, and the evolution of local adaptation. This also occurs under a variable temperature gradient, and under the assumption of 90% lethal mutations. CONCLUSIONS: In this study we show novel consequences of the particular genetic properties of populations under spatial disequilibrium, i.e. the coevolution of dispersal probability and mutation rate, even in a sexual species and under realistic spatial gradients, resulting in faster invasions. The evolution of mutation rates can therefore be added to the list of possible explanations for the 'genetic paradox of invasive species'. We conclude that range expansions and the evolution of mutation rates are in a positive feedback loop, with possibly far-reaching ecological consequences concerning invasiveness and the adaptability of species to novel environmental conditions.

The Adequate Use of Limited Information in Dispersal Decisions.

Several theoretical studies predict that informed (e.g., density-dependent) dispersal should generally result in lower emigration probabilities than uninformed (random) dispersal. In a 2012 publication, Bocedi et al. surprisingly come to the opposite conclusion. For most scenarios investigated, they found that noninformed and, particularly, less precisely informed dispersers evolve lower dispersal propensity than dispersers following "fully informed" strategies. Further, they observed that fully informed individuals evolved a steplike dispersal response-a response to local density that contradicts theoretical predictions for organisms with nonoverlapping generations. Replicating the individual-based simulations of Bocedi et al. we find that these conclusions are not justified and are based on a misinterpretation of simulation results: their controversial findings result from (i) a misleading use of the term "population density," (ii) a misconception concerning the true informative value of the different decision criteria they compared, and (iii) arbitrary constraints on the evolution of the dispersal response that prevented the evolution of strategies that allow for a fitness-enhancing utilization of available information.

Optimal life-history strategy differs between philopatric and dispersing individuals in a metapopulation.

Abundant empirical evidence for dispersal syndromes contrasts with the rarity of theoretical predictions about the evolution of life-history divergence between dispersing and philopatric individuals. We use an evolutionary model to predict optimal differences in age-specific reproductive effort between dispersing and philopatric individuals inhabiting the same metapopulation. In our model, only young individuals disperse, and their lifelong reproductive decisions are potentially affected by this initial event. Juvenile survival declines as density of adults and other juveniles increases. We assume a trade-off between reproduction and survival, so that different patterns of age-specific reproductive effort lead to different patterns of aging. We find that young immigrant mothers should allocate more resources to reproduction than young philopatric mothers, but these life-history differences vanish as immigrant and philopatric individuals get older. However, whether the higher early reproductive effort of immigrants results in higher fecundity depends on the postimmigration cost on fecundity. Dispersing individuals have consequently a shorter life span. Ultimately, these life-history differences are due to the fact that young dispersing individuals most often live in recently founded populations, where competition is relaxed and juvenile survival higher, favoring larger investment in offspring production at the expense of survival.

Kin competition as a major driving force for invasions.

Current theory explains accelerating invasions with increased levels of dispersal as being caused by "spatial selection." Here we argue that another selective force, strong kin competition resulting from high relatedness due to subsequent founder effects at the expanding margin, is of at least comparable importance for dispersal evolution during invasions. We test this hypothesis with individual-based simulations of a spatially structured population invading empty space. To quantify the relative contribution of kin competition to dispersal evolution, we contrast two scenarios, one including kin effects and one excluding them without influencing spatial selection. We find that kin competition is a major determinant for dispersal evolution at invasion fronts, especially under environmental conditions that favor a pronounced kin structure (i.e., small patches, low environmental stochasticity, and high patch isolation). We demonstrate the importance of kin competition and thus biotic influences on dispersal evolution during invasions.

Why are metapopulations so rare?

Roughly 40 years after its introduction, the metapopulation concept is central to population ecology. The notion that local populations and their dynamics may be coupled by dispersal is without any doubt of great importance for our understanding of population-level processes. A metapopulation describes a set of subpopulations linked by (rare) dispersal events in a dynamic equilibrium of extinctions and recolonizations. In the large body of literature that has accumulated, the term "metapopulation" is often used in a very broad sense; most of the time it simply implies spatial heterogeneity. A number of reviews have recently addressed this problem and have pointed out that, despite the large and still growing popularity of the metapopulation concept, there are only very few empirical examples that conform with the strict classical metapopulation (CM) definition. In order to understand this discrepancy between theory and observation, we use an individual-based modeling approach that allows us to pinpoint the environmental conditions and the life-history attributes required for the emergence of a CM structure. We find that CM dynamics are restricted to a specific parameter range at the border between spatially structured but completely occupied and globally extinct populations. Considering general life-history attributes, our simulations suggest that CMs are more likely to occur in arthropod species than in (large) vertebrates. Since the specific type of spatial population structure determines conservation concepts, our findings have important implications for conservation biology. Our model suggests that most spatially structured populations are panmictic, patchy, or of mainland-island type, which makes efforts spent on increasing connectivity (e.g., corridors) questionable. If one does observe a true CM structure, this means that the focal metapopulation is on the brink of extinction and that drastic conservation measures are needed.

Assortative mating counteracts the evolution of dispersal polymorphisms.

Polymorphic dispersal strategies are found in many plant and animal species. An important question is how the genetic variation underlying such polymorphisms is maintained. Numerous mechanisms have been discussed, including kin competition or frequency-dependent selection. In the context of sympatric speciation events, genetic and phenotypic variation is often assumed to be preserved by assortative mating. Thus, recently, this has been advocated as a possible mechanism leading to the evolution of dispersal polymorphisms. Here, we examine the role of assortative mating for the evolution of trade-off-driven dispersal polymorphisms by modeling univoltine insect species in a metapopulation. We show that assortative mating does not favor the evolution of polymorphisms. On the contrary, assortative mating favors the evolution of an intermediate dispersal type and a uni-modal distribution of traits within populations. As an alternative, mechanism dominance may explain the occurrence of two discrete morphs.

On the elasticity of range limits during periods of expansion.

Dispersal is known to play a crucial role in the formation of species' ranges. Recent studies demonstrate that dispersiveness increases rapidly during the range expansion of species due to a fitness increase for dispersers at the expanding front. R. D. Holt concluded, however, that emigration should decline after the period of invasion and hence predicted some range contraction following the initial expansion phase. In this study, we evaluate this hypothesis using a spatially explicit individual-based model of populations distributed along environmental gradients. In our experiments we allow the species to spread along a gradient of declining conditions. Results show that range contraction did emerge in a gradient of dispersal mortality, caused by the rapid increase in emigration probability during invasion and selection disfavoring dispersal, once a stable range is formed. However, gradients in growth rate, local extinction rate, and patch capacity did not lead to a noticeable contraction of the range. We conclude, that the phenomenon of range contraction may emerge, but only under conditions that select for a reduction in dispersal at the range edge in comparison to the core region once the expansion period is over.