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Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as “magic trait” loci. We use a population genetics model to examine whether “pseudomagic trait” complexes, composed of physically linked loci fulfilling these two functions, are as efficient in promoting premating isolation as magic traits. We specifically measure the evolution of choosiness, which controls the strength of assortative mating. We show that, surprisingly, pseudomagic trait complexes, and to a lesser extent also physically unlinked loci, can lead to the evolution of considerably stronger assortative mating preferences than do magic traits, provided polymorphism at the involved loci is maintained. This is because assortative mating preferences are generally favored when there is a risk of producing maladapted recombinants, as occurs with nonmagic trait complexes but not with magic traits (since pleiotropy precludes recombination). Contrary to current belief, magic traits may not be the most effective genetic architecture for promoting strong premating isolation. Distinguishing between magic traits and pseudomagic trait complexes is therefore important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.

Supergenes are genetic architectures allowing the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of sets of alleles at linked loci is determined by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, color or behavioral polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the genetic origin of supergenes remains poorly understood. Here, using a population genetic two-island model, we explore how the evolution of overdominant chromosomal inversions may lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations connected by gene flow leads to an increase in frequency of poorly adapted, immigrant haplotypes. When inversions are associated with recessive fitness cost hampering their fixation (such as a mutational load), this results in the formation of supergenes. These results provide a realistic scenario for the evolution of supergenes and inversion polymorphisms in general, and bring new light into the importance of admixture in the formation of new genetic architectures.

Cooperation does not occur in a vacuum: interactions develop over time in social groups that undergo demographic changes. Intuition suggests that stable social environments favour developing few but strong reciprocal relationships (a ‘focused' strategy), while volatile social environments favour the opposite: more but weaker social relationships (a ‘diversifying' strategy). We model reciprocal investments under a quality–quantity trade-off for social relationships. We find that volatility, counterintuitively, can favour a focused strategy. This result becomes explicable through applying the theory of antagonistic pleiotropy, originally developed for senescence, to social life. Diversifying strategies show superior performance later in life, but with costs paid at young ages, while the social network is slowly being built. Under volatile environments, many individuals die before reaching sufficiently old ages to reap the benefits. Social strategies that do well early in life are then favoured: a focused strategy leads individuals to form their first few social bonds quickly and to make strong use of existing bonds. Our model highlights the importance of pleiotropy and population age structure for the evolution of cooperative strategies and other social traits, and shows that it is not sufficient to reflect on the fate of survivors only, when evaluating the benefits of social strategies.

The mimicry of one species by another provides one of the most celebrated examples of evolution by natural selection. Edible Batesian mimics deceive predators into believing they may be defended, whereas defended Müllerian mimics have evolved a shared warning signal, more rapidly educating predators to avoid them. However, it may benefit hungry predators to attack defended prey, while the benefits of learning about unfamiliar prey depends on the future value of this information. Previous energetic state-dependent models of predator foraging behavior have assumed complete knowledge, while informational state-dependent models have assumed fixed levels of hunger. Here, we identify the optimal decision rules of predators accounting for both energetic and informational states. We show that the nature of mimicry is qualitatively and quantitatively affected by both sources of state dependence. Associative learning weakens the extent of parasitic mimicry by edible prey because naive predators often attack defended models. More importantly, mimicry among equally highly defended prey may be parasitic or mutualistic depending on the ecological context (e.g., the source of mimics and the abundance of alternative prey). Finally, mimicry by prey with intermediate defenses corresponds to Batesian or Müllerian mimicry depending on whether the mimic is profitable to attack by hungry predators, but it is not a special case of mimicry.

Cooperation does not occur in a vacuum: interactions develop over time in social groups that undergo demographic changes. Intuition suggests that stable social environments favour developing few but strong reciprocal relationships (a ‘focused’ strategy), while volatile social environments favour the opposite: more but weaker social relationships (a ‘diversifying’ strategy). We model reciprocal investments under a quality-quantity tradeoff for social relationships. We find that volatility, counterintuitively, can favour a focused strategy. This result becomes explicable through applying the theory of antagonistic pleiotropy, originally developed for senescence, to social life. Diversifying strategies show superior performance later in life, but with costs paid at young ages while the social network is slowly being built. Under volatile environments, many individuals die before reaching sufficiently old ages to reap the benefits. Social strategies that do well early in life are then favoured: a focused strategy leads individuals to form their first few social bonds quickly and to make strong use of existing bonds. Our model highlights the importance of pleiotropy and population age structure for the evolution of cooperative strategies and other social traits, and shows that it is not sufficient to reflect on the fate of survivors only, when evaluating the benefits of social strategies.

Species often replace each other spatially along contact zones, giving scope for parapatric speciation. In models of parapatric speciation driven by assortative mating, costs of female choosiness have so far be ignored. Yet, if females encounter only a limited number of males, those that are too choosy may remain unmated, and this should create direct sexual selection against choosiness. In our individual-based model of parapatric ecological speciation, disruptive viability selection leads to divergence of an ecological trait. Additionally, female choosiness (following a ‘matching mating rule’ based on the same ecological trait) can evolve at the risk of remaining unmated, and can limit gene flow between diverging populations. In line with previous litterature, out of the contact zone, the evolution of cost-free choosiness stops at intermediate values due to indirect selection against strong choosiness. Here we show that a weak cost of choosiness, by modifying genotypic frequencies on which viability selection acts, reduces this selection pressure, thus permitting the evolution of stronger choosiness than in the absence of costs. In strong contrast to sympatric models, costs of choosiness can therefore promote reproductive isolation in parapatry.

The predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the ‘Red Queen hypothesis’ emphasises the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. Whereas empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions. Recently, it has been suggested that early multicellular organisms with basic anticancer defences were presumably plagued by antagonistic interactions with transmissible cancers and that this could have played a pivotal role in the evolution of sex. Here, we dissect this argument using a population genetic model. One fundamental aspect distinguishing transmissible cancers from other parasites is the continual production of cancerous cell lines from hosts’ own tissues. We show that this influx dampens fluctuating selection and therefore makes the evolution of sex more difficult than in standard Red Queen models. Although coevolutionary cycling can remain sufficient to select for sex under some parameter regions of our model, we show that the size of those regions shrinks once we account for epidemiological constraints. Altogether, our results suggest that horizontal transmission of cancerous cells is unlikely to cause fluctuating selection favouring sexual reproduction. Nonetheless, we confirm that vertical transmission of cancerous cells can promote the evolution of sex through a separate mechanism, known as similarity selection, that does not depend on coevolutionary fluctuations., Recently, it has been suggested that early multicellular organisms with basic anticancer defenses were plagued by antagonistic interactions with transmissible cancers, and that this could have played a pivotal role in the evolution of sex. Here, mathematical models show that coevolution between multicellular organisms and transmissible cancers does not easily favour sexual reproduction.

International audience; Negative and positive ecological interactions have opposite effects on the structure of ecological communities, in particular in terms of ecological similarity among interacting species. In nature, species belonging to the same guild often interact in both negative and positive ways, yet the interplay between interactions of different kinds in intraguild community dynamics remains poorly understood. Müllerian mimetic communities are particularly suited for investigating this interplay because positive (mutualistic mimicry) and negative (competition for trophic resource and micro‐habitat) interactions are relatively easy to identify. Empirical research has shown that the combination of mutualistic mimicry and competition does not necessarily drive convergence along all dimensions of the ecological niche, but the determinants of such mixed result are unknown. Here, we analyze the structure of Müllerian mimetic communities simulated with an agent‐based model. We show that mutualistic mimicry favours ecological similarity on dimensions along which similarity favours fine‐scale co‐occurrence. Co‐mimetic species use similar micro‐habitats, but do not necessarily use similar resources. Heterogeneity of resources among micro‐habitats is necessary for ecological similarity on resource use among co‐mimetic species to occur. We therefore highlight the importance of fine‐scale co‐occurrence if we are to understand how positive and negative interactions structure ecological communities.

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large-scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population-based model. We focus on mutualistic Mullerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Mullerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Mullerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Mullerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Mullerian mimicry on ecological, spatial, and phylogenetic diversification.

Variation in the conspicuousness of colour patterns is observed within and among defended prey species. The evolution of conspicuous colour pattern in defended species can be strongly impaired because of increased detectability by predators. Nevertheless, such evolution of the colour pattern can be favoured if changes in conspicuousness result in Müllerian mimicry with other defended prey. Here, we develop a model describing the population dynamics of a conspicuous defended prey species, and we assess the invasion conditions of derived phenotypes that differ from the ancestral phenotype by their conspicuousness. Such change in conspicuousness may then modify their level of mimicry with the local community of defended species. Derived colour pattern displayed in this focal population can therefore be either exactly similar, partially resembling or completely dissimilar to the local mimicry ring displaying the ancestral colour pattern. We assume that predation risk depends (1) on the number of individuals sharing a given colour pattern within the population, (2) on the occurrence of co-mimetic defended species, and (3) on the availability of alternative edible prey. Using a combination of analytical derivations and numerical simulations, we show that less conspicuous colour patterns are generally favoured within mimicry rings, unless reduced conspicuousness impairs mimicry. By contrast, when a mutation affecting the colour pattern leads to a shift toward a better protected mimicry ring, crypsis is no longer necessarily beneficial and a more conspicuous colour pattern can be favoured. The selected aposematic pattern then depends on the local composition of mimetic communities, as well as on the detectability, memorability and level of mimicry of the colour patterns.

International audience; Evolutionary theory predicts that positive assortative mating the tendency of similar individuals to mate with each other-plays a key role for speciation by generating reproductive isolation between diverging populations. However, comprehensive tests for an effect of assortative mating on species richness at the macroevolution-ary scale are lacking. We used a meta-analytic approach to test the hypothesis that the strength of assortative mating within populations is positively related to species richness across a broad range of animal taxa. Specifically, we ran a phylogenetically independent meta-analysis using an extensive database of 1,447 effect sizes for the strength of assortative mating, encompassing 307 species from 130 families and 14 classes. Our results suggest that there is no relationship between the strength of assortative mating and species richness across and within major taxonomic groups and trait categories. Moreover, our analysis confirms an earlier finding that animals typically mate assor-tatively (global Pearson correlation coefficient: r p 0:36; 95% confidence interval: 0.19-0.52) when accounting for phylogenetic non-independence. We argue that future advances will rely on a better understanding of the evolutionary causes and consequences of the observed intra-and interspecific variation in the strength of assortative mating.

Differential species responses to atmospheric CO 2 concentration (Ca) could lead to quantitative changes in competition among species and community composition, with flow‐on effects for ecosystem function. However, there has been little theoretical analysis of how elevated Ca (eC a) will affect plant competition, or how composition of plant communities might change. Such theoretical analysis is needed for developing testable hypotheses to frame experimental research. Here, we investigated theoretically how plant competition might change under eC a by implementing two alternative competition theories, resource use theory and resource capture theory, in a plant carbon and nitrogen cycling model. The model makes several novel predictions for the impact of eC a on plant community composition. Using resource use theory, the model predicts that eC a is unlikely to change species dominance in competition, but is likely to increase coexistence among species. Using resource capture theory, the model predicts that eC a may increase community evenness. Collectively, both theories suggest that eC a will favor coexistence and hence that species diversity should increase with eC a. Our theoretical analysis leads to a novel hypothesis for the impact of eC a on plant community composition. This hypothesis has potential to help guide the design and interpretation of eC a experiments.

International audience; Online enhancements: supplemental PDF. Dryad data: http://dx.doi.org/10.5061/dryad.b1039. abstract: Understanding the conditions under which moderately defended prey evolve to resemble better-defended prey and whether this mimicry is parasitic (quasi-Batesian) or mutualistic (Müllerian) is central to our understanding of warning signals. Models of predator learning generally predict quasi-Batesian relationships. However, predators' attack decisions are based not only on learning alone but also on the potential future rewards. We identify the optimal sampling strategy of predators capable of classifying prey into different profitability categories and contrast the implications of these rules for mimicry evolution with a classical Pavlovian model based on conditioning. In both cases, the presence of moderately unprofitable mimics causes an increase in overall consumption. However, in the case of the optimal sampling strategy, this increase in consumption is typically outweighed by the increase in overall density of prey sharing the model appearance (a dilution effect), causing a decrease in mortality. It suggests that if predators forage efficiently to maximize their long-term payoff, genuine quasi-Batesian mimicry should be rare, which may explain the scarcity of evidence for it in nature. Nevertheless, we show that when moderately defended mimics are profitable to attack by hungry predators, then they can be parasitic on their models, just as classical Batesian mimics are.

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large-scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population-based model. We focus on mutualistic Müllerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Müllerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Müllerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Müllerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Müllerian mimicry on ecological, spatial, and phylogenetic diversification.