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.     

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.     

Limits to the evolution of assortative mating by female choice under restricted gene flow

The evolution of assortative mating is a key component of the process of speciation with gene flow. Several recent theoretical studies have pointed out, however, that sexual selection which can result from assortative mating may cause it to plateau at an intermediate level; this is primarily owing to search costs of individuals with extreme phenotypes and to assortative preferences developed by individuals with intermediate phenotypes. I explore the limitations of assortative mating further by analysing a simple model in which these factors have been removed. Specifically, I use a haploid two-population model to ask whether the existence of assortative mating is sufficient to drive the further evolution of assortative mating. I find that a weakening in the effective strength of sexual selection with strong assortment leads to the existence of both a peak level of trait differentiation and the evolution of an intermediate level of assortative mating that will cause that peak. This result is robust to the inclusion of local adaptation and different genetic architecture of the trait. The results imply the existence of fundamental limits to the evolution of assortment via sexual selection in this situation, with which other factors, such as search costs, may interact.     

HOST-PLANT-INDUCED ASSORTATIVE MATING IN ENCHENOPA TREEHOPPERS

The hypothesis tested here is whether extrinsic host-plant-induced life-history timing and mating biology promote assortative mating along host-plant lines. In the arboreal, univoltine Enchenopa treehopper system, host plants mediate the timing and synchronization of egg hatch. The result is a uniform age structure with a restricted mating window during which females mate once. Enchenopa on host plants that differ in phenology have asynchronous life histories and mating windows, suggesting that temporal differences may promote assortative mating. To test this hypothesis, egg hatch of Enchenopa from the same host-plant species was manipulated to produce continuous adult age-classes. Under experimental conditions with no spatial barriers, mating occurred between individuals similar in age. The mechanism promoting this assortative mating is differential mortality in males and females, such that few males are still alive when females in successive age-classes mate. Such host-plant-induced assortative mating is viewed as an effective mechanism to protect the integrity of gene pools from migrants, permitting selection for host-plant-adapted genotypes and speciation.     

Genetic variation in flowering time induces phenological assortative mating: quantitative genetic methods applied to Brassica rapa

It has been argued from first principles that plants mate assortatively by flowering time. However, there have been very few studies of phenological assortative mating, perhaps because current methods to infer paternal phenotype are difficult to apply to natural populations. Two methods are presented to estimate the phenotypic correlation between mates-the quantitative genetic metric for assortative mating-for phenological traits. The first method uses individual flowering schedules to estimate mating probabilities for every potential pairing in a sample. These probabilities are then incorporated into a weighted phenotypic correlation between all potential mates and thus yield a prospective estimate based on mating opportunities. The correlation between mates can also be estimated retrospectively by comparing the regression of offspring phenotype over one parent, which is inflated by assortative mating, to the regression over mid-parent, which is not. In a demonstration experiment with Brassica rapa, the prospective correlation between flowering times (days from germination to anthesis) of pollen recipients and their potential donors was 0.58. The retrospective estimate of this correlation strongly agreed with the prospective estimate. The prospective method is easily employed in field studies that explore the effect of phenological assortative mating on selection response and population differentiation.     

Sexual selection and assortative mating by size and their roles in the maintenance of a polymorphism in Swedish Littorina saxatilis populations

Two independent components of mating behaviour, sexual selection and assortative mating, were studied in two allopatric morphs, one sheltered boulder shore form (S-morph) and one exposed cliff shore form (E-morph), of Littorina saxatilis from the west coast of Sweden. Sexual selection was studied by comparing the sizes of copulating and non-copulating snails in the field. Size assortative mating was studied by collecting copulating pairs in the field, while assortative mating between morphs was investigated by bringing the pure morphs together in intermediary habitats and then noting the matings. The S-morph mated randomly in relation to size in two of the studied populations and exhibited a trend towards size assortative mating in a third, while the E-morph showed size assortative mating in both studied populations. The microdistribution of sizes of snails on the shores could not explain all the size assortative mating found, and instead it is argued that a size-based mate rejection behaviour also contributes to the assortative mating in at least some of these populations. There was sexual selection on size in both males and females in the S-morph, with large individuals being favoured as mates. In contrast, copulating snails of the E-morph were smaller than non-copulating ones. The significantly different sexual selection intensities between the two morphs may help to explain the size differences between them. There was random mating between the E- and the S-morphs of L. saxatilis, which suggests no incipient reproductive isolation between morphs on Swedish rocky shores. This is in agreement with earlier studies of Swedish populations, but is in contrast to the situation found in other geographical areas.     

Comparisons of positive assortative mating and sexual selection models

A series of theoretical models of positive assortative mating and sexual selection are contrasted. It is established that for a dominant trait partial positive assortative mating generally implies some fixation, whereas sexual selection exhibits a unique globally stable polymorphism exhibiting Hardy-Weinberg proportions. The effects of monogamy against polygamy do not qualitatively alter the equilibrium outcomes, although the rate of evolutionary change is generally slowed with monogamy vis-à-vis polygamy. For sexual selection the influence of timing of random mating as against preferential mating causes no change in the equilibrium states, although the rates of convergence can be slowed if sexual selection occurs late in the breeding season. Under assortative mating the timing can alter the equilibrium outcomes. The amount of heterozygosity is always deficient in cases of assortative mating, but always exhibits Hardy-Weinberg ratios under a sexual selection mechanism. This suggests that observations consistent with Hardy-Weinberg equilibrium states cannot preclude ipso facto certain forms of selection forces, including mating patterns and some natural selection structures.     

Evolutionary responses of tree phenology to the combined effects of assortative mating,gene flow and divergent selection

The timing of bud burst (TBB) in temperate trees is a key adaptive trait, the expression of which is triggered by temperature gradients across the landscape. TBB is strongly correlated with flowering time and is therefore probably mediated by assortative mating. We derived theoretical predictions and realized numerical simulations of evolutionary changes in TBB in response to divergent selection and gene flow in a metapopulation. We showed that the combination of the environmental gradient of TBB and assortative mating creates contrasting genetic clines, depending on the direction of divergent selection. If divergent selection acts in the same direction as the environmental gradient (cogradient settings), genetic clines are established and inflated by assortative mating. Conversely, under divergent selection of the same strength but acting in the opposite direction (countergradient selection), genetic clines are slightly constrained. We explored the consequences of these dynamics for population maladaptation, by monitoring pollen swamping. Depending on the direction of divergent selection with respect to the environmental gradient, pollen filtering owing to assortative mating either facilitates or impedes adaptation in peripheral populations.     

Assortative mating for fitness and the evolution of recombination

To understand selection on recombination, we need to consider how linkage disequilibria develop and how recombination alters these disequilibria. Any factor that affects the development of disequilibria, including nonrandom mating, can potentially change selection on recombination. Assortative mating is known to affect linkage disequilibria but its effects on the evolution of recombination have not been previously studied. Given that assortative mating for fitness can arise indirectly via a number of biologically realistic scenarios, it is plausible that weak assortative mating occurs across a diverse set of taxa. Using a modifier model, we examine how assortative mating for fitness affects the evolution of recombination under two evolutionary scenarios: selective sweeps and mutation-selection balance. We find there is no net effect of assortative mating during a selective sweep. In contrast, assortative mating could have a large effect on recombination when deleterious alleles are maintained at mutation-selection balance but only if assortative mating is sufficiently strong. Upon considering reasonable values for the number of loci affecting fitness components, the strength of selection, and the mutation rate, we conclude that the correlation in fitness between mates is unlikely to be sufficiently high for assortative mating to affect the evolution of recombination in most species.     

Is size‐assortative mating important for rapid pigment differentiation in a freshwater isopod?

Identifying mechanisms behind assortative mating is central to the understanding of ecological divergence and speciation. Recent studies show that populations of the freshwater isopod Asellus aquaticus can rapidly become locally differentiated when submerged Chara vegetation expands in lakes. In the novel Chara habitat, isopods have become lighter pigmented and smaller than in ancestral reed stands. In this study, we used a laboratory multiple-choice experiment to investigate assortative mating as a possible prezygotic reproductive barrier between Chara and reed isopods. Mating was assortative when Chara isopods were experimentally mixed with isopods from an adjacent reed site with large-size individuals, suggesting a partial prezygotic reproductive barrier. No deviation from random mating could, however, be detected when Chara isopods were mixed with smaller sized isopods from another reed site. In both experiments, assortative mating was apparently based on size, as Chara isopods were larger and reed isopods smaller in mixed pairs than in assortative pairs. Pigmentation did not have any clear influence on mating. We suggest that divergence in pigmentation evolved through natural selection in conjunction with size-assortative mating indirectly causing assortative mating between Chara and reed isopods. Size-assortative mating is likely a by-product of natural selection, but its importance may hypothetically be transient, if selection erodes the correlation between pigmentation and size over time.     

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.     

Effects of female preference intensity on the permissiveness of sexual trait polymorphisms

Recent developments in sexual selection theory suggest that on their own, mate preferences can promote the maintenance of sexual trait diversity. However, how mate preferences constrain the permissiveness of sexual trait diversity in different environmental regimes remains an open question. Here, we examine how a range of mate choice parameters affect the permissiveness of sexual trait polymorphism under several selection regimes. We use the null model of sexual selection and show that environments with strong assortative mating significantly increase the permissiveness of sexual trait polymorphism. We show that for a given change in mate choice parameters, the permissiveness of polymorphism changes more in environments with strong natural selection on sexual traits than in environments with weak selection. Sets of nearly stable polymorphic populations with weak assortative mating are more likely to show accidental divergence in sexual traits than sets of populations with strong assortative mating. The permissiveness of sexual trait polymorphism critically depends upon particular combinations of natural selection and mate choice parameters.     

EVOLUTION OF DOMINANCE UNDER FREQUENCY-DEPENDENT INTRASPECIFIC COMPETITION IN AN ASSORTATIVELY MATING POPULATION

We study the evolution of higher levels of dominance as a response to negative frequency-dependent selection. In contrast to previous studies, we focus on the effect of assortative mating on the evolution of dominance under frequency-dependent intraspecific competition. We analyze a two-locus two-allele model, in which the primary locus has a major effect on a quantitative trait that is under a mixture of frequency-independent stabilizing selection, density-dependent selection, and frequency-dependent selection caused by intraspecific competition for a continuum of resources. The second (modifier) locus determines the degree of dominance at the trait level. Additionally, the population mates assortatively with respect to similarities in the ecological trait. Our analysis shows that the parameter region in which dominance can be established decreases if small levels of assortment are introduced. In addition, the degree of dominance that can be established also decreases. In contrast, if assortment is intermediate, sexual selection for extreme types can be established, which leads to evolution of higher levels of dominance than under random mating. For modifiers with large effects, intermediate levels of assortative mating are most favorable for the evolution of dominance. For large modifiers, the speed of fixation can even be higher for intermediate levels of assortative mating than for random mating.     

Sexual size dimorphism and assortative mating for morphological traits in Passer domesticus

In this study, assortative mating for different morphological traits was studied in a captive population of house sparrows (Passer domesticus). Males were larger than females. Assortative mating was found for tail length, wing length and general body size. Males with larger badge size mated with females with longer tails. The strongest assortative mating occurred for tail length (r=0.77), and this assortative mating remained significant after controlling for wing length, mass and tarsus length, suggesting that it was not an artefact of assortative mating for body size. The possibility of sexual selection for tail length in the house sparrow is discussed.     

Can Preference for Oviposition Sites Initiate Reproductive Isolation in Callosobruchus maculatus?

Theory has identified a variety of evolutionary processes that may lead to speciation. Our study includes selection experiments using different host plants and test key predictions concerning models of speciation based on host plant choice, such as the evolution of host use (preference and performance) and assortative mating. This study shows that after only ten generations of selection on different resources/hosts in allopatry, strains of the seed beetle Callosobruchus maculatus develop new resource preferences and show resource-dependent assortative mating when given the possibility to choose mates and resources during secondary contact. The resulting reduced gene flow between the different strains remained for two generations after contact before being overrun by disassortative mating. We show that reduced gene flow can evolve in a population due to a link between host preference and assortative mating, although this result was not found in all lines. However, consistent with models of speciation, assortative mating alone is not sufficient to maintain reproductive isolation when individuals disperse freely between hosts. We conclude that the evolution of reproductive isolation in this system cannot proceed without selection against hybrids. Other possible factors facilitating the evolution of isolation would be longer periods of allopatry, the build up of local adaptation or reduced migration upon secondary contact.     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Frequency-dependent selection and the evolution of assortative mating

A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.     

Pairing dynamics and the origin of species

Whether sexual selection alone can drive the evolution of assortative mating in the presence of gene flow is a long-standing question in evolutionary biology. Here, we report a role for pairing dynamics of individuals when mate choice is mutual, which is sufficient for the evolution of assortative mating by sexual selection alone in the presence of gene flow. Through behavioural observation, individual-based simulation and population genetic analysis, we evaluate the pairing dynamics of coral reef fish in the genus Hypoplectrus (Serranidae), and the role these dynamics can play for the evolution of assortative mating. When mate choice is mutual and the stability of mating pairs is critical for reproductive success, the evolution of assortative mating in the presence of gene flow is not only possible, but is also a robust evolutionary outcome.     

Introgressive hybridization as a mechanism for species rescue

Rapid evolution on ecological time scales can play a key role in species responses to environmental change. One dynamic that has the potential to generate the diversity necessary for evolution rapid enough to allow response to sudden environmental shifts is introgressive hybridization. However, if distinct sub-species exist before an environmental shift, mechanisms that impede hybridization, such as assortative mating and hybrid inferiority, are likely to be present. Here we explore the theoretical potential for introgressive hybridization to play a role in response to environmental change. In particular, we incorporate assortative mating, hybrid inferiority, and demographic stochasticity into a two-locus, two-allele population genetic model of two interacting species where one locus identifies the species and the other determines how fitness depends on the changing environment. Simulation results indicate that moderately high values for the strength of assortative mating will allow enough hybridization events to outweigh demographic stochasticity but not so many that continued hybridization outweighs backcrossing and introgression. Successful introgressive hybridization also requires intermediate relative fitness at the allele negatively affected by environmental change such that hybrid survivorship outweighs demographic stochasticity but selection remains strong enough to affect the genetic dynamics. The potential for successful introgression instead of extinction with greater environmental change is larger with monogamous rather than promiscuous mating due to lower stochasticity in mating events. These results suggest species characteristics (e.g., intermediate assortative mating and mating systems with low variation in mating likelihood) which indicate a potential for rapid evolution in response to environmental change via introgressive hybridization.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.