Competitive speciation and costs of choosiness

We investigate how costs of choosiness affect the evolution of assortative mating in a simple model of competitive speciation. The model allows for a comprehensive analysis by analytical and numerical techniques. We obtain results for two types of costs: mating costs, which restrict the number of males a choosy female can evaluate, and viability costs, which decrease a choosy female's survival. Mating costs significantly reduce the range of parameters for which speciation is possible, but only if the number of males a female can evaluate is small (less than 10). This type of costs can be eliminated if females are allowed to mate randomly at the end of the mating period. Although, in this case, it is not possible to achieve complete reproductive isolation, our results show partial isolation with strong phenotypic clustering. Viability costs counteract selection for assortative mating. As this selection is typically weak, speciation is possible only if viability costs, too, are weak. The above restrictions are less severe if extreme phenotypes have an intrinsically higher carrying capacity.     

Conditions for the Maintenance of Prezygotic and Zygotic Isolation in a Continent-Island Model

A continent-island model is studied in which differences are initially present at a gene locus with assortative mating (which causes prezygotic reproductive isolation) and at one or two unlinked selected loci, (which cause zygotic reproductive isolation). This model simulates secondary contact between two populations which have diverged allopatrically at loci which control isolating mechanisms. Two different models of prezygotic isolation and three different models of zygotic isolation are studied. The analysis is focused on those conditions under which differentiation is not lost through the swamping effect of gene now. In each case the critical migration rate (m_c) below which differences can be maintained is found. Results depend on the degree of assortative mating, on the level of selection on the genes involved, and on the particular models of reproductive isolation considered. However, in all the models, for high values of such parameters the two isolating mechanisms interact strongly, and consequently the stability of the difference at each locus (as measured by m_c) is noticeably influenced by the presence of the difference at the other locus (or loci). The nature and strength of the effects of this interaction differ according to whether or not there is selection on the assortative mating locus and whether selection against hybrids or directional selection is hypothesized.     

HABITAT AVOIDANCE: OVERLOOKING AN IMPORTANT ASPECT OF HOST‐SPECIFIC MATING AND SYMPATRIC SPECIATION?

Understanding speciation requires discerning how reproductive barriers to gene flow evolve between previously interbreeding populations. Models of sympatric speciation for phytophagous insects posit that reproductive isolation can evolve in the absence of geographic isolation as a consequence of an insect shifting and ecologically adapting to a new host plant. One important adaptation contributing to sympatric differentiation is host-specific mating. When organisms mate in preferred habitats, a system of positive assortative mating is established that facilitates sympatric divergence. Models of host fidelity generally assume that host choice is determined by the aggregate effect of alleles imparting positive preferences for different plant species. But negative effect genes for avoiding nonnatal plants may also influence host use. Previous studies have shown that apple and hawthorn-infesting races of Rhagoletis pomonella flies use volatile compounds emitted from the surface of fruit as key chemosensory cues to recognize and distinguish between their host plants. Here, we report results from field trials indicating that in addition to preferring the odor of their natal fruit, apple and hawthorn flies, and their undescribed sister species infesting flowering dogwood (Cornus florida), also avoid the odors of nonnatal fruit. We discuss the implications of nonnatal fruit avoidance for the evolutionary dynamics and genetics of sympatric speciation. Our findings reveal an underappreciated role for habitat avoidance as a potential postmating, as well as prezygotic, barrier to gene flow.     

Levels of genetic polymorphism: marker loci versus quantitative traits.

Species are the units used to measure ecological diversity and alleles are the units of genetic diversity. Genetic variation within and among species has been documented most extensively using allozyme electrophoresis. This reveals wide differences in genetic variability within, and genetic distances among, species, demonstrating that species are not equivalent units of diversity. The extent to which the pattern observed for allozymes can be used to infer patterns of genetic variation in quantitative traits depends on the forces generating and maintaining variability. Allozyme variation is probably not strictly neutral but, nevertheless, heterozygosity is expected to be influenced by population size and genetic distance will be affected by time since divergence. The same is true for quantitative traits influenced by many genes and under weak stabilizing selection. However, the limited data available suggest that allozyme variability is a poor predictor of genetic variation in quantitative traits within populations. It is a better predictor of general phenotypic divergence and of postzygotic isolation between populations or species, but is only weakly correlated with prezygotic isolation. Studies of grasshopper and planthopper mating signal variation and assortative mating illustrate how these characters evolve independently of general genetic and morphological variation. The role of such traits in prezygotic isolation, and hence speciation, means that they will contribute significantly to the diversity of levels of genetic variation within and among species.     

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.     

INCIPIENT REPRODUCTIVE ISOLATION BETWEEN TWO SYMPATRIC MORPHS OF THE INTERTIDAL SNAIL LITTORINA SAXATILIS

The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub-groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone. In Galician populations of the marine snail Littorina saxatilis, two main morphs appear on the same shores, one on the upper-shore barnacle belt and the other in the lower-shore mussel belt. The two morphs overlap in distribution in the midshore where hybrids are found together with pure forms. Allozyme variation indicates that the two parental morphs share a common gene pool, although within shores, gene flow between morphs is less than gene flow within morphs. In this study, we observed mating behavior in the field, and we found that mating was not random in midshore sites, with a deficiency of heterotypic pairs. Habitat selection, assortative mating, and possibly sexual selection among females contributed to the partial reproductive isolation between the pure morphs. Sizes of mates were often positively correlated, in particular, in the upper shore, indicating size-assortative mating too. However, this seemed to be a consequence of nonrandom microdistributions of snails of different sizes. Because we also argue that the hybrid zone is of primary rather than secondary origin, this seems to be an example of sympatric reproductive isolation, either established by means of reinforcement or as a by-product to divergent selection acting on other characters.     

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.     

Male discrimination of female mucous trails permits assortative mating in a marine snail species

Recent research has shown the potential for nonallopatric speciation, but we lack an adequate understanding of the mechanisms of prezygotic barriers and how these evolve in the presence of gene flow. The marine snail Littorina saxatilis has distinct ecotypes in different shore microhabitats. Ecotypes hybridize in contact zones, but gene flow is impeded by assortative mating. Earlier studies have shown that males and females of the same ecotype copulate for longer than mates of different ecotype. Here we report a new mechanism that further contributes to reproductive isolation between ecotypes in the presence of gene flow. This mechanism is linked to the ability of males to track potential partners by following their mucous trail. We show that cliff ecotype males follow the trails of females of the same ecotype for longer than females of the alternate (boulder) ecotype. In addition, cliff males are more likely to follow the mucous trail in the correct direction if the trail is laid by a cliff-female. The capacity to discriminate the ecotype of female mucous trails combined with differential copulation times creates a strong prezygotic reproductive barrier between ecotypes of L. saxatilis that reduces gene flow from cliff to boulder ecotypes by >/=80%.     

Speciation by natural and sexual selection: models and experiments

A large number of mathematical models have been developed that show how natural and sexual selection can cause prezygotic isolation to evolve. This article attempts to unify this literature by identifying five major elements that determine the outcome of speciation caused by selection: a form of disruptive selection, a form of isolating mechanism (assortment or a mating preference), a way to transmit the force of disruptive selection to the isolating mechanism (direct selection or indirect selection), a genetic basis for increased isolation (a one- or two-allele mechanism), and an initial condition (high or low initial divergence). We show that the geographical context of speciation (allopatry vs. sympatry) can be viewed as a form of assortative mating. These five elements appear to operate largely independently of each other and can be used to make generalizations about when speciation is most likely to happen. This provides a framework for interpreting results from laboratory experiments, which are found to agree generally with theoretical predictions about conditions that are favorable to the evolution of prezygotic isolation.     

Multiple reproductive barriers separate recently diverged sunflower ecotypes

Measuring reproductive barriers between groups of organisms is an effective way to determine the traits and mechanisms that impede gene flow. However, to understand the ecological and evolutionary factors that drive speciation, it is important to distinguish between the barriers that arise early in the speciation process and those that arise after speciation is largely complete. In this article, we comprehensively test for reproductive isolation between recently diverged (<10,000 years bp) dune and nondune ecotypes of the prairie sunflower, Helianthus petiolaris. We find reproductive barriers acting at multiple stages of hybridization, including premating, postmating–prezygotic, and postzygotic barriers, despite the recent divergence. Barriers include extrinsic selection against immigrants and hybrids, a shift in pollinator assemblage, and postpollination assortative mating. Together, these data suggest that multiple barriers can be important for reducing gene flow in the earliest stages of speciation.     

Evolution of reproductive isolation within a parasitic fungal species complex

Despite important advances in the last few years, the evolution of reproductive isolation (RI) remains an unresolved and critical gap in our understanding of speciation processes. In this study, we investigated the evolution of RI among species of the parasitic fungal species complex Microbotryum violaceum, which is responsible for anther smut disease of the Caryophyllaceae. We found no evidence for significant positive assortative mating by M. violaceum even over substantial degrees of genetic divergence, suggesting a lack of prezygotic isolation. In contrast, postzygotic isolation increased with the genetic distance between mating partners when measured as hyphal growth. Total RI, measured as the ability of the pathogen to infect and produce a diploid progeny in the host plant, was significantly and positively correlated with genetic distance, remaining below complete isolation for most of the species pairs. The results of this study, the first one on the time course of speciation in a fungus, are therefore consistent with previous works showing that RI generally evolves gradually with genetic distance, and thus presumably with time. Interestingly, prezygotic RI due to gamete recognition did not increase with genetic distance, in contrast to the pattern found in plants and animals.     

Phylogenetic evidence for multiple sympatric ecological diversification in a marine snail

Parallel speciation can occur when traits determining reproductive isolation evolve independently in different populations that experience a similar range of environments. However, a common problem in studies of parallel evolution is to distinguish this hypothesis from an alternative one in which different ecotypes arose only once in allopatry and now share a sympatric scenario with substantial gene flow between them. Here we show that the combination of a phylogenetic approach with life-history data is able to disentangle both hypotheses in the case of the intertidal marine snail Littorina saxatilis on the rocky shores of Galicia in northwestern Spain. In this system, numerous phenotypic and genetic differences have evolved between two sympatric ecotypes spanning a sharp ecological gradient, and as aside effect of the former have produced partial reproductive isolation. A mitochondrial phylogeny of these populations strongly suggests that the two sympatric ecotypes have originated independently several times. Building upon earlier work demonstrating size-based assortative mating as the main contributor to reproductive isolation among ecotypes, our analysis provides strong evidence that divergent selection across a sharp ecological gradient promoted the parallel divergence of body size and shape between two sympatric ecotypes. Thus, divergent selection occurring independently in different populations has produced the marine equivalent of host races, which may represent the first step in speciation.     

A comparative study of Gaussian mating preference functions: a key element of sympatric speciation models

Simulating the evolution of reproductive isolation under sympatric speciation scenarios is a complex process that requires modelling several phases, including evolution of phenotypes, demography, migration, fitness components and mating preference. The last has been shown to be a key parameter in several simulation studies, allowing the incorporation of assortative mating (premating isolation). Mating preference can be modelled by different mathematical functions but, as far as we know, a formal comparison of those functions has not yet been undertaken. In this work, we briefly review the main functions used in the literature and suggest a new one. In doing so, we also define three basic properties (monotonicity, proportionality and symmetry) that an ideal function should satisfy when generating assortative mating. We simulated several scenarios to compare how all these functions perform based on these properties. We also draw attention to the fact that the existing functions are affected distinctly by changing the scale of the preferred trait value. Some functions remain unaffected by scaling the trait, while in others assortative mating increases proportionally to the trait value. Most of the functions tested did not fulfil all the properties studied, and we find certain flaws in some of them that should be considered before being used in future studies. We provide some general recommendations for using the preference functions in simulation studies, and suggest that an unnoticed scaling effect could have underestimated the chance to obtain speciation under certain scenarios. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 642–657.     

Extinction and introgression in a community of partially cross-fertile plant species

We develop a model to study the demography and genetics of an encounter between two partially cross-fertile plant species. We assume prezygotic reproductive isolation between the species, a common situation when the species differ by their phenology or floral traits that cause assortative mating. Three outcomes are possible: coexistence of both species with minimal introgression; domination by one species, with the other becoming extinct or surviving only through recurrent migration; or domination of the community by hybrid derivatives, with both species surviving but with a rather high level of introgression between them. The first situation is reached when interfertility is low, while the third requires high interfertility to develop. Occurrence of the second situation is observed with intermediate values of interfertility. Gene flow from nearby monospecific populations can prevent both introgression and the domination of the community by one species. Conversely, increasing the number of loci that determine the reproductive isolation between species or decreasing the degree of nonadditive interactions (epistasis and/or dominance) between alleles and loci makes introgression more likely. We found that hybridization can create positive frequency dependence and make extinction possible, even when hybrid individuals have no intrinsic fitness advantage.     

The evolution of partial reproductive isolation as an adaptive optimum

Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding—namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.     

Mechanisms of reinforcement in natural and simulated polymorphic populations

Reinforcement speciation is the process whereby selection against hybrids drives the evolution of enhanced pre‐mating reproductive isolation. Work has focused on divergent mating preferences (assortative mating) but pre‐mating isolation can also arise via various migration modification behaviours, such as divergent habitat preferences. The relative importance of these two different mechanisms of reinforcement remains unclear. A recent theoretical model (Yukilevich–True model) found that relative fixation probabilities between these mechanisms can vary. Additionally, natural populations of Timema cristinae walking‐sticks exhibit variation (polymorphism) in both mechanisms, generating questions about the patterns expected for allele frequencies prior to fixation, during the early stages of the speciation process. In the present study, we report: (1) new analyses examining the correlation between fixation probabilities for assortative mating and migration modification in the Yukilevich–True model; (2) novel simulations examining allele frequencies in polymorphic populations; and (3) empirical patterns of reinforcement in T. cristinae in the context of theoretical predictions. Simulations of both types yielded congruent results, revealing that the outcome of reinforcement was dependent on the strength of selection. Under weak selection, reinforcement by either mechanism is unlikely. Under intermediate selection, the conditions favoring the rise and fixation of one mechanism favored the rise and fixation of the other. However, assortative mating evolved somewhat more readily than migration modification. Populations of T. cristinae, which experience such intermediate selection, supported these predictions. Under strong selection, the evolution of migration modification generally interfered with the evolution of assortative mating by decreasing migration between populations, thereby reducing selection for assortative mating. Congruence of the results for allele frequencies versus fixation probabilities suggests that similar patterns of reinforcement are expected during different stages of the speciation process. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 305–319.     

Geographic contrasts between pre‐ and postzygotic barriers are consistent with reinforcement in Heliconius butterflies

Identifying the traits causing reproductive isolation and the order in which they evolve is fundamental to understanding speciation. Here, we quantify prezygotic and intrinsic postzygotic isolation among allopatric, parapatric, and sympatric populations of the butterflies Heliconius elevatus and Heliconius pardalinus. Sympatric populations from the Amazon (H. elevatus and H. p. butleri) exhibit strong prezygotic isolation and rarely mate in captivity; however, hybrids are fertile. Allopatric populations from the Amazon (H. p. butleri) and Andes (H. p. sergestus) mate freely when brought together in captivity, but the female F1 hybrids are sterile. Parapatric populations (H. elevatus and H. p. sergestus) exhibit both assortative mating and sterility of female F1s. Assortative mating in sympatric populations is consistent with reinforcement in the face of gene flow, where the driving force, selection against hybrids, is due to disruption of mimicry and other ecological traits rather than hybrid sterility. In contrast, the lack of assortative mating and hybrid sterility observed in allopatric populations suggests that geographic isolation enables the evolution of intrinsic postzygotic reproductive isolation. Our results show how the types of reproductive barriers that evolve between species may depend on geography.     

The concept of effective recombination rate and its application in speciation theory

The goal of this study is to develop a unifying theoretical framework to quantify the strength of reproductive isolation. We propose the use of the "effective recombination rate," which measures how fast associations of genes are broken by interlocus recombination. Applying the well-established theory of the effective migration rate, we derive two techniques to investigate the effective recombination rate in models of speciation: the weak migration approximation for parapatric scenarios and the weak recombination approximation for sympatric scenarios. We illustrate the use of these two methods by two examples each: (1) single-locus genetic incompatibility and (2) two-locus genetic incompatibility for the first method, and (3) assortative mating and (4) assortative mating combined with disruptive selection for the second method. An advantage of the effective recombination rate over previous approaches is that it integrates gene flow in both directions into a single index measuring the strength of isolation. This enables straightforward comparisons of speciation scenarios with the same or different geographic histories. The method also allows us to evaluate the relative contributions of F2 hybrid deficiency or linkage between multiple barriers in reproductive isolation.     

Experimental evolution of mating discrimination in budding yeast

Assortative mating, when individuals of similar phenotypes mate, likely plays a key role in preventing gene flow during speciation. Reinforcement occurs when two previously geographically separated (allopatric) groups meet after having evolved partial postzygotic isolation; they are selected to evolve or enhance assortative mating to prevent costly intergroup matings that produce only maladaptive or sterile hybrids. Studies in Drosophila have shown that the genetic architectures of mating discrimination could differ significantly with or without reinforcement, suggesting that the evolution of assortative mating may be more complicated than expected. To study the evolution of assortative mating, we evolved mating discrimination in populations of the budding yeast, Saccharomyces cerevisiae. After 36 cycles of selection, these cells are five times more likely to mate with each other than to their ancestors, despite detectable one-way gene flow between the selected and reference populations. Several individual cultures evolved mating discrimination by changing their mating kinetics, with some mating more rapidly and others more slowly than the ancestral population. Genetic analysis indicates that multiple mutations have accumulated to produce the altered mating preference. Our results show that subtle details of mating behavior can play an important role in the evolution of reproductive isolation.     

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.