Negative Coupling: The Coincidence of Premating Isolating Barriers Can Reduce Reproductive Isolation.

Speciation can be mediated by a variety of reproductive barriers, and the interaction among different barriers has often been shown to enhance overall reproductive isolation, a process referred to as "coupling." Here, we analyze a population genetics model to study the establishment of linkage disequilibrium (LD) among loci involved in multiple premating barriers, an aspect that has received little theoretical attention to date. We consider a simple genetic framework underlying two distinct premating barriers, each encoded by a preference locus and its associated mating trait locus. We show that their interaction can lead to a decrease in overall reproductive isolation relative to a situation with a single barrier, a process we call "negative coupling." More specifically, in our model, negative coupling results either from sexual selection that reduces divergence at all loci, or from reduced LD that occurs because the presence of many females with "mismatched" preferences causes the mating success of recombinant males to become high. Interestingly, the latter effect may even cause LD among preference loci to become negative when recombination rates among loci are low. We conclude that coincident reproductive barriers may not necessarily reinforce each other, and that the underlying loci may not necessarily develop a positive association.

Senescence evolution under the catastrophic accumulation of deleterious mutations.

For aging to evolve, selection against mortality must decrease with age. This prevailing view in the evolutionary theory of senescence posits that mutations with deleterious effects happening late in life-when purging selection is weak-may become fixed via genetic drift in the germline, and produce a senescent phenotype. Theory, however, has focused primarily on growing populations and the fate of single deleterious mutations. In a mathematical model, we demonstrate that relaxing both of these simplifying assumptions leads to unrealistic outcomes. In density-regulated populations, previously fixed deleterious mutations should promote the fixation of other deleterious mutations that lead to senescence at ever younger ages, until death necessarily occurs at sexual maturity. This sequential fixation of deleterious mutations is not promoted by a decrease in population size, but is due to a change in the strength of selection. In an individual-based model, we also show that such evolutionary dynamics should lead to the extinction of most populations. Our models therefore make rather unrealistic predictions, underlining the need for a reappraisal of current theories. In this respect, we have further assumed in our models that the deleterious effects of mutations can only occur at certain ages, marked, for instance, by somatic or physiological changes. Under this condition, we show that the catastrophic accumulation of deleterious mutations in the germline can stop. This new finding emphasizes the importance of investigating somatic factors, as well as other mechanisms underlying the deleterious effects of mutations, to understand senescence evolution. More generally, our model therefore establishes that patterns of senescence in nature depend not only on the decrease in selection strength with age but also on any mechanism that stops the catastrophic accumulation of mutations.

The interplay of local adaptation and gene flow may lead to the formation of supergenes.

Supergenes are genetic architectures resulting in the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of alleles at linked loci is often facilitated by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, colour or behavioural polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the formation of supergenes remains poorly understood. Here, using a two-island population genetic model, we explore how gene flow and the evolution of overdominant chromosomal inversions may jointly lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations, both under disruptive selection, leads to an increase in frequency of poorly adapted, immigrant haplotypes. Indeed, rare allelic combinations, such as immigrant haplotypes, are more frequently reshuffled by recombination than common allelic combinations, and therefore benefit from the recombination suppression generated by inversions. When an inversion capturing a locally adapted haplotype spreads but is associated with a fitness cost hampering its fixation (e.g. a recessive mutation load), the maintenance of a non-inverted haplotype in the population is enhanced; under certain conditions, the immigrant haplotype persists alongside the inverted local haplotype, while the standard local haplotype disappears. This establishes a stable, local polymorphism with two non-recombining haplotypes encoding alternative adaptive strategies, that is, a supergene. These results bring new light to the importance of local adaptation, overdominance, and gene flow in the formation of supergenes and inversion polymorphisms in general.

Structural Variants and Speciation: Multiple Processes at Play.

Research on the genomic architecture of speciation has increasingly revealed the importance of structural variants (SVs) that affect the presence, abundance, position, and/or direction of a nucleotide sequence. SVs include large chromosomal rearrangements such as fusion/fissions and inversions and translocations, as well as smaller variants such as duplications, insertions, and deletions (CNVs). Although we have ample evidence that SVs play a key role in speciation, the underlying mechanisms differ depending on the type and length of the SV, as well as the ecological, demographic, and historical context. We review predictions and empirical evidence for classic processes such as underdominance due to meiotic aberrations and the coupling effect of recombination suppression before exploring how recent sequencing methodologies illuminate the prevalence and diversity of SVs. We discuss specific properties of SVs and their impact throughout the genome, highlighting that multiple processes are at play, and possibly interacting, in the relationship between SVs and speciation.

The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

The effectiveness of pseudomagic traits in promoting premating isolation.

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 favoured when there is a risk of producing maladapted recombinants, as occurs with non-magic 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. Therefore, distinguishing between magic traits and pseudomagic trait complexes is important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.

Volatile social environments can favour investments in quality over quantity of social relationships.

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.

Digest: Evolutionary rescue following the introduction of a pathogen.

To what extent can adaptive evolution rescue a population from extinction following the introduction of a pathogen? Searle and Christie (2021) show how evolutionary rescues in host-pathogen systems may differ from those that occur in response to abiotic changes. In particular, they pinpoint how epidemiological feedback and pathogen evolution, inherent to host-pathogen systems, can greatly affect the likelihood of rescue.

Transmissible cancers and the evolution of sex under the Red Queen hypothesis.

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.

State-Dependent Decision-Making by Predators and Its Consequences for Mimicry.

AbstractThe 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.

Positive density dependence acting on mortality can help maintain species-rich communities.

Conspecific negative density dependence is ubiquitous and has long been recognized as an important factor favoring the coexistence of competing species at local scale. By contrast, a positive density-dependent growth rate is thought to favor species exclusion by inhibiting the growth of less competitive species. Yet, such conspecific positive density dependence often reduces extrinsic mortality (e.g. reduced predation), which favors species exclusion in the first place. Here, using a combination of analytical derivations and numerical simulations, I show that this form of positive density dependence can favor the existence of equilibrium points characterized by species coexistence. Those equilibria are not globally stable, but allow the maintenance of species-rich communities in multispecies simulations. Therefore, conspecific positive density dependence does not necessarily favor species exclusion. On the contrary, some forms of conspecific positive density dependence may even help maintain species richness in natural communities. These results should stimulate further investigations into the precise mechanisms underlying density dependence.

Coevolution of male and female mate choice can destabilize reproductive isolation.

Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic 'preference cycling' triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.

Assortative Mating in Animals and Its Role for Speciation.

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 macroevolutionary 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 assortatively (global Pearson correlation coefficient: r=0.36; 95% confidence interval: 0.19-0.52) when accounting for phylogenetic nonindependence. 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.

Mimicry among Unequally Defended Prey Should Be Mutualistic When Predators Sample Optimally.

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.

Mutualistic mimicry enhances species diversification through spatial segregation and extension of the ecological niche space.

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.

Elevated carbon dioxide is predicted to promote coexistence among competing species in a trait-based model.

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.

Diversity in Müllerian mimicry: The optimal predator sampling strategy explains both local and regional polymorphism in prey.

The convergent evolution of warning signals in unpalatable species, known as Müllerian mimicry, has been observed in a wide variety of taxonomic groups. This form of mimicry is generally thought to have arisen as a consequence of local frequency-dependent selection imposed by sampling predators. However, despite clear evidence for local selection against rare warning signals, there appears an almost embarrassing amount of polymorphism in natural warning colors, both within and among populations. Because the model of predator cognition widely invoked to explain Müllerian mimicry (Müller's "fixed n(k)" model) is highly simplified and has not been empirically supported; here, we explore the dynamical consequences of the optimal strategy for sampling unfamiliar prey. This strategy, based on a classical exploration-exploitation trade-off, not only allows for a variable number of prey sampled, but also accounts for predator neophobia under some conditions. In contrast to Müller's "fixed n(k)" sampling rule, the optimal sampling strategy is capable of generating a variety of dynamical outcomes, including mimicry but also regional and local polymorphism. Moreover, the heterogeneity of predator behavior across space and time that a more nuanced foraging strategy allows, can even further facilitate the emergence of both local and regional polymorphism in prey warning color.