Adaptive speciation when assortative mating is based on female preference for male marker traits

Adaptive speciation occurs when frequency-dependent ecological interactions generate conditions of disruptive selection to which lineage splitting is an adaptive response. Under such selective conditions, evolution of assortative mating mechanisms enables the break-up of the ancestral lineage into diverging and reproductively isolated descendent species. Extending previous studies, I investigate models of adaptive speciation due to the evolution of indirect assortative mating that is based on three different mating traits: the degree of assortativity, a female preference trait and a male marker trait. For speciation to occur, linkage disequilibria between different mating traits, e.g. between female preference and male marker traits, as well as between mating traits and the ecological trait, must evolve. This can lead to novel speciation scenarios, e.g. when reproductive isolation is generated by a splitting in the degree of assortativeness, with one of the emerging lineages mating assortatively, and the other one disassortatively. I investigate the effects of variation in various model parameters on the likelihood of speciation, as well as robustness of speciation to introducing costs of assortative mating. Even though in the models presented speciation requires the genetic potential for strong assortment as well as rather restrictive ecological conditions, the results show that adaptive speciation due to the evolution of assortative mating when mate choice is based on separate female preference and male marker traits is a theoretically plausible evolutionary scenario.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

An analytically tractable model for competitive speciation

Several recent models have shown that frequency-dependent disruptive selection created by intraspecific competition can lead to the evolution of assortative mating and, thus, to competitive sympatric speciation. However, since most of these results rely on limited numerical analyses, their generality has been debated. Here, we consider one of the standard models (the so-called Roughgarden model) with a simplified genetics where the selected trait is determined by a single diallelic locus. This model is sufficiently complex to maintain key properties of the general multilocus case but simple enough to allow for comprehensive analytical treatment by means of invasion fitness arguments. Depending on (1) the strength and (2) the shape of stabilizing selection, (3) the strength and (4) the shape of pairwise competition, (5) the shape of the mating function, and (6) whether assortative mating leads to sexual selection, we find five different evolutionary regimes. In one of these regimes, complete reproductive isolation can evolve through arbitrarily small steps in the strength of assortative mating. Our approach provides a mechanistic understanding of several phenomena that have been found in previous models. The results demonstrate how even in a simple model, the evolutionary outcome depends in a complex way on ecological and genetic parameters.     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

The evolution of genetic architecture under frequency-dependent disruptive selection

We propose a model to analyze a quantitative trait under frequency-dependent disruptive selection. Selection on the trait is a combination of stabilizing selection and intraspecific competition, where competition is maximal between individuals with equal phenotypes. In addition, there is a density-dependent component induced by population regulation. The trait is determined additively by a number of biallelic loci, which can have different effects on the trait value. In contrast to most previous models, we assume that the allelic effects at the loci can evolve due to epistatic interactions with the genetic background. Using a modifier approach, we derive analytical results under the assumption of weak selection and constant population size, and we investigate the full model by numerical simulations. We find that frequency-dependent disruptive selection favors the evolution of a highly asymmetric genetic architecture, where most of the genetic variation is concentrated on a small number of loci. We show that the evolution of genetic architecture can be understood in terms of the ecological niches created by competition. The phenotypic distribution of a population with an adapted genetic architecture closely matches this niche structure. Thus, evolution of the genetic architecture seems to be a plausible way for populations to adapt to regimes of frequency-dependent disruptive selection. As such, it should be seen as a potential evolutionary pathway to discrete polymorphisms and as a potential alternative to other evolutionary responses, such as the evolution of sexual dimorphism or assortative mating.     

Revisiting santa rosalia to unfold a degeneracy of classic models of speciation

Abstract Many classic models of speciation incorporate assortative mating based on mating groups, such as plants with different flowering times, and they investigate whether an ecological trait under disruptive natural selection becomes genetically associated with the selectively neutral mating trait. It is well known that this genetic association is potently destroyed by recombination. In this note, we point out a more fundamental difficulty: if a "knife-edge" symmetry assumption of previous models is violated, then the mating trait is no longer neutral and sexual selection eliminates the polymorphism in the mating locus. This result strengthens the growing consensus that magic traits are the more likely route to nonallopatric speciation. We expand the model assuming also ecological selection on the mating trait and investigate the conditions for natural selection to overcome sexual selection and maintain mating polymorphism; we find that the combination of natural and sexual selection can cause also bistability of allele frequencies.     

A theoretical investigation of sympatric evolution of temporal reproductive isolation as illustrated by marine broadcast spawners

Recent theory suggests that frequency-dependent disruptive selection in combination with assortative mating can lead to the establishment of reproductive isolation in sympatry. Here we explore how temporal variation in reproduction might simultaneously generate both disruptive selection and assortative mating, and result in sympatric speciation. The conceptual framework of the model may be applicable to biological systems with negative frequency-dependent selection, such as marine broadcast spawners or systems with pollinator limitation. We present a model that is motivated by recent findings in marine broadcast spawners and is parameterized with data from the Montastraea annularis species complex. Broadcast spawners reproduce via external fertilization and synchronous spawning is required to increase the probability of successful fertilization, but empirical evidence shows that as density increases, so does the risk of polyspermy. Polyspermy is the fusion of multiple sperm with an egg at fertilization, a process that makes the embryo unviable. Synchrony can therefore also act as a source of negative density-dependent disruptive selection. Model analysis shows that the interaction between polyspermy and spawning synchrony can lead to temporal reproductive isolation in sympatry and that, more generally, increased density promotes maintenance of genetic variation.     

Speciation and the evolution of dispersal along environmental gradients

We analyze the joint evolution of an ecological character and of dispersal distance in asexual and sexual populations inhabiting an environmental gradient. Several interesting phenomena resulting from the evolutionary interplay of these characters are revealed. First, asexual and sexual populations exhibit two analogous evolutionary regimes, in which either speciation in the ecological character occurs in conjunction with evolution of short-range dispersal, or dispersal distance remains high and speciation does not occur. Second, transitions between these two regimes qualitatively differ between asexual and sexual populations, with the former showing speciation with long-range dispersal and the latter showing no speciation with short-range dispersal. Third, a phenotypic gradient following the environmental gradient occurs only in the last case, i.e., for non-speciating sexual populations evolving towards short-range dispersal. Fourth, the transition between the evolutionary regimes of long-range dispersal with no speciation and short-range dispersal with speciation is typically abrupt, mediated by a positive feedback between incipient speciation and the evolution of short-range dispersal. Fifth, even though the model of sexual evolution analyzed here does not permit assortative mating preferences, speciation occurs for a surprisingly wide range of conditions. This illustrates that dispersal evolution is a powerful alternative to preference evolution in enabling spatially distributed sexual populations to respond to frequency-dependent disruptive selection.     

A quantitative genetic competition model for sympatric speciation

I use multilocus genetics to describe assortative mating in a competition model. The intensity of competition between individuals is influenced by a quantitative character whose value is determined additively by alleles from many loci. With assortative mating based on this character, frequency- and density-dependent competition can subdivide a population with an initially unimodal character distribution. The character distribution becomes bimodal, and the subpopulations corresponding to the two modes are reproductively separated because mating is assortative. This happens if the resource distribution is unimodal, i.e. even if selection due to phenotypic carrying capacities is not disruptive. The results suggest that sympatric speciation due to frequency-dependent selection can occur in quite general ecological scenarios if mating is assortative. I also discuss the evolution of assortative mating. Since it induces bimodal phenotype distributions, assortative mating leads to a better match of the resources if their distribution is also bimodal. Moreover, in a population with a bimodal phenotype distribution, the average strength of frequency-dependent competition is lower than in a unimodal population. Therefore, assortative mating permits higher equilibrium densities than random mating even if the resource distribution is unimodal. Thus, even though it may lead to a less efficient resource use, assortative mating is favoured over random mating because it reduces frequency-dependent effects of competition.     

Disruptive ecological selection on a mating cue

Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such ‘magic’ or ‘multiple-effect’ traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.     

When is sympatric speciation truly adaptive? An analysis of the joint evolution of resource utilization and assortative mating

The plausibility of sympatric speciation has long been debated among evolutionary ecologists. The process necessarily involves two key elements: the stable coexistence of at least two ecologically distinct types and the emergence of reproductive isolation. Recent theoretical studies within the theoretical framework of adaptive dynamics have shown how both these processes can be driven by natural selection. In the standard scenario, a population first evolves to an evolutionary branching point, next, disruptive selection promotes ecological diversification within the population, and, finally, the fitness disadvantage of intermediate types induces a selection pressure for assortative mating behaviour, which leads to reproductive isolation and full speciation. However, the full speciation process has been mostly studied through computer simulations and only analysed in part. Here I present a complete analysis of the whole speciation process by allowing for the simultaneous evolution of the branching ecological trait as well as a continuous trait controlling mating behaviour. I show how the joint evolution can be understood in terms of a gradient landscape, where the plausibility of different evolutionary paths can be evaluated graphically. I find sympatric speciation unlikely for scenarios with a continuous, unimodal, distribution of resources. Rather, ecological settings where the fitness inferiority of intermediate types is preserved during the ecological branching are more likely to provide opportunity for adaptive, sympatric speciation. Such scenarios include speciation due to predator avoidance or specialization on discrete resources. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Artificial neural networks in models of specialization, guild evolution and sympatric speciation

Sympatric speciation can arise as a result of disruptive selection with assortative mating as a pleiotropic by-product. Studies on host choice, employing artificial neural networks as models for the host recognition system in exploiters, illustrate how disruptive selection on host choice coupled with assortative mating can arise as a consequence of selection for specialization. Our studies demonstrate that a generalist exploiter population can evolve into a guild of specialists with an 'ideal free' frequency distribution across hosts. The ideal free distribution arises from variability in host suitability and density-dependent exploiter fitness on different host species. Specialists are less subject to inter-phenotypic competition than generalists and to harmful mutations that are common in generalists exploiting multiple hosts.When host signals used as cues by exploiters coevolve with exploiter recognition systems, our studies show that evolutionary changes may be continuous and cyclic. Selection changes back and forth between specialization and generalization in the exploiters, and weak and strong mimicry in the hosts, where non-defended hosts use the host investing in defence as a model. Thus, host signals and exploiter responses are engaged in a red-queen mimicry process that is ultimately cyclic rather then directional. In one phase, evolving signals of exploitable hosts mimic those of hosts less suitable for exploitation (i.e. the model). Signals in the model hosts also evolve through selection to escape the mimic and its exploiters. Response saturation constraints in the model hosts lead to the mimic hosts finally perfecting its mimicry, after which specialization in the exploiter guild is lost. This loss of exploiter specialization provides an opportunity for the model hosts to escape their mimics. Therefore, this cycle then repeats.We suggest that a species can readily evolve sympatrically when disruptive selection for specialization on hosts is the first step. In a sexual reproduction setting, partial reproductive isolation may first evolve by mate choice being confined to individuals on the same host. Secondly, this disruptive selection will favour assortative mate choice on genotype, thereby leading to increased reproductive isolation.     

Evolution of mate choice and the so‐called magic traits in ecological speciation

Non‐random mating provides multiple evolutionary benefits and can result in speciation. Biological organisms are characterised by a myriad of different traits, many of which can serve as mating cues. We consider multiple mechanisms of non‐random mating simultaneously within a unified modelling framework in an attempt to understand better which are more likely to evolve in natural populations going through the process of local adaptation and ecological speciation. We show that certain traits that are under direct natural selection are more likely to be co‐opted as mating cues, leading to the appearance of magic traits (i.e. phenotypic traits involved in both local adaptation and mating decisions). Multiple mechanisms of non‐random mating can interact so that trait co‐evolution enables the evolution of non‐random mating mechanisms that would not evolve alone. The presence of magic traits may suggest that ecological selection was acting during the origin of new species.     

Independent evolution of the sexes promotes amphibian diversification

Classic ecological theory predicts that the evolution of sexual dimorphism constrains diversification by limiting morphospace available for speciation. Alternatively, sexual selection may lead to the evolution of reproductive isolation and increased diversification. We test contrasting predictions of these hypotheses by examining the relationship between sexual dimorphism and diversification in amphibians. Our analysis shows that the evolution of sexual size dimorphism (SSD) is associated with increased diversification and speciation, contrary to the ecological theory. Further, this result is unlikely to be explained by traditional sexual selection models because variation in amphibian SSD is unlikely to be driven entirely by sexual selection. We suggest that relaxing a central assumption of classic ecological models—that the sexes share a common adaptive landscape—leads to the alternative hypothesis that independent evolution of the sexes may promote diversification. Once the constraints of sexual conflict are relaxed, the sexes can explore morphospace that would otherwise be inaccessible. Consistent with this novel hypothesis, the evolution of SSD in amphibians is associated with reduced current extinction threat status, and an historical reduction in extinction rate. Our work reconciles conflicting predictions from ecological and evolutionary theory and illustrates that the ability of the sexes to evolve independently is associated with a spectacular vertebrate radiation.     

Mechanisms of species divergence through visual adaptation and sexual selection: Perspectives from a cichlid model sys-tem

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences are directly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process, because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. When divergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence. Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selection against intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual envi-ronment constitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investi-gate the direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours (red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extract general principles, and discuss future perspectives.     

On the origin of species by means of assortative mating.

Assortative mating may split a population even in the absence of natural selection. Here, we study when this happens if mating depends on one or two quantitative traits. Not surprisingly, the modes of assortative mating that can cause sympatric speciation without selection are rather strict. However, some of them may occur in nature. Slow elimination of intermediate individuals caused by the gradual tightening of assortative mating, which evolves owing to relatively weak disruptive selection, provides the alternative scenario for sympatric speciation, in addition to fast elimination of intermediate individuals as a result of the direct action of strong disruptive selection under an invariant mode of assortative mating. Even when assortative mating alone cannot split an initially coherent population, it may be able to prevent the merging of species after their secondary contact.     

Multimodal pattern formation in phenotype distributions of sexual populations

During bouts of evolutionary diversification, such as adaptive radiations, the emerging species cluster around different locations in phenotype space. How such multimodal patterns in phenotype space can emerge from a single ancestral species is a fundamental question in biology. Frequency-dependent competition is one potential mechanism for such pattern formation, as has previously been shown in models based on the theory of adaptive dynamics. Here, we demonstrate that also in models similar to those used in quantitative genetics, phenotype distributions can split into multiple modes under the force of frequency-dependent competition. In sexual populations, this requires assortative mating, and we show that the multimodal splitting of initially unimodal distributions occurs over a range of assortment parameters. In addition, assortative mating can be favoured evolutionarily even if it incurs costs, because it provides a means of alleviating the effects of frequency dependence. Our results reveal that models at both ends of the spectrum between essentially monomorphic (adaptive dynamics) and fully polymorphic (quantitative genetics) yield similar results. This underscores that frequency-dependent selection is a strong agent of pattern formation in phenotype distributions, potentially resulting in adaptive speciation.     

Divergent outcomes of reinforcement speciation: the relative importance of assortative mating and migration modification

Most studies of reinforcement speciation focus on the evolution of assortative mating, but R. A. Fisher argued that migration modification is likely to be a common alternative mechanism. Despite previous models showing that assortative mating and migration modification may both be involved in reinforcement, no one has determined their relative evolutionary importance. This is surprising because understanding the biological conditions favoring these mechanisms may explain why certain pairs of species exhibit abutting, nonoverlapping geographical ranges with habitat fidelity while other pairs coexist in sympatry with sexual isolation. In this article, we explicitly model the evolution of both mechanisms simultaneously. First, we explore how these mechanisms differ in their evolutionary dynamics. Second, we ask how they affect each other's evolution and whether the interaction alters their relative importance in reinforcement. Our results reveal that assortative mating may evolve faster and under a broader range of biological conditions than migration modification. However, direct evolutionary interactions favor migration modification when populations experience strong divergent selection. Depending on the nature of postmating isolation, these mechanisms may either interfere with each other's evolution or coevolve in the same system. These results illustrate the importance of studying multiple mechanisms of speciation simultaneously in future speciation models.     

Sympatric Speciation: When Is It Possible in Bacteria?

According to theory, sympatric speciation in sexual eukaryotes is favored when relatively few loci in the genome are sufficient for reproductive isolation and adaptation to different niches. Here we show a similar result for clonally reproducing bacteria, but which comes about for different reasons. In simulated microbial populations, there is an evolutionary tradeoff between early and late stages of niche adaptation, which is resolved when relatively few loci are required for adaptation. At early stages, recombination accelerates adaptation to new niches (ecological speciation) by combining multiple adaptive alleles into a single genome. Later on, without assortative mating or other barriers to gene flow, recombination generates unfit intermediate genotypes and homogenizes incipient species. The solution to this tradeoff may be simply to reduce the number of loci required for speciation, or to reduce recombination between species over time. Both solutions appear to be relevant in natural microbial populations, allowing them to diverge into ecological species under similar constraints as sexual eukaryotes, despite differences in their life histories.     

Assortative mating by diet in a phenotypically unimodal but ecologically variable population of stickleback

Speciation with gene flow may be driven by a combination of positive assortative mating and disruptive selection, particularly if selection and assortative mating act on the same trait, eliminating recombination between ecotype and mating type. Phenotypically unimodal populations of threespine stickleback (Gasterosteus aculeatus) are commonly subject to disruptive selection due to competition for alternate prey. Here we present evidence that stickleback also exhibit assortative mating by diet. Among-individual diet variation leads to variation in stable isotopes, which reflect prey use. We find a significant correlation between the isotopes of males and eggs within their nests. Because egg isotopes are derived from females, this correlation reflects assortative mating between males and females by diet. In concert with disruptive selection, this assortative mating should facilitate divergence. However, the stickleback population remains phenotypically unimodal, highlighting the fact that assortative mating and disruptive selection do not guarantee evolutionary divergence and speciation.