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.     

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.     

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.     

PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS?

Theoretical studies of speciation have been dominated by numerical simulations aiming to demonstrate that speciation in a certain scenario may occur. What is needed now is a shift in focus to identifying more general rules and patterns in the dynamics of speciation. The crucial step in achieving this goal is the development of simple and general dynamical models that can be studied not only numerically but analytically as well. I review some of the existing analytical results on speciation. I first show why the classical theories of speciation by peak shifts across adaptive valleys driven by random genetic drift run into trouble (and into what kind of trouble). Then I describe the Bateson-Dobzhansky-Muller (BDM) model of speciation that does not require overcoming selection. I describe exactly how the probability of speciation, the average waiting time to speciation, and the average duration of speciation depend on the mutation and migration rates, population size, and selection for local adaptation. The BDM model postulates a rather specific genetic architecture of reproductive isolation. I then show exactly why the genetic architecture required by the BDM model should be common in general. Next I consider the multilocus generalizations of the BDM model again concentrating on the qualitative characteristics of speciation such as the average waiting time to speciation and the average duration of speciation. Finally, I consider two models of sympatric speciation in which the conditions for sympatric speciation were found analytically. A number of important conclusions have emerged from analytical studies. Unless the population size is small and the adaptive valley is shallow, the waiting time to a stochastic transition between the adaptive peaks is extremely long. However, if transition does happen, it is very quick. Speciation can occur by mutation and random drift alone with no contribution from selection as different populations accumulate incompatible genes. The importance of mutations and drift in speciation is augmented by the general structure of adaptive landscapes. Speciation can be understood as the divergence along nearly neutral networks and holey adaptive landscapes (driven by mutation, drift, and selection for adaptation to a local biotic and/or abiotic environment) accompanied by the accumulation of reproductive isolation as a by-product. The waiting time to speciation driven by mutation and drift is typically very long. Selection for local adaptation (either acting directly on the loci underlying reproductive isolation via their pleiotropic effects or acting indirectly via establishing a genetic barrier to gene flow) can significantly decrease the waiting time to speciation. In the parapatric case the average actual duration of speciation is much shorter than the average waiting time to speciation. Speciation is expected to be triggered by changes in the environment. Once genetic changes underlying speciation start, they go to completion very rapidly. Sympatric speciation is possible if disruptive selection and/or assortativeness in mating are strong enough. Sympatric speciation is promoted if costs of being choosy are small (or absent) and if linkage between the loci experiencing disruptive selection and those controlling assortative mating is strong.     

Ecological speciation in Gambusia fishes

Although theory indicates that natural selection can facilitate speciation as a by-product, demonstrating ongoing speciation via this by-product mechanism in nature has proven difficult. We examined morphological, molecular, and behavioral data to investigate ecology's role in incipient speciation for a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes. We show that adaptation to divergent predator regimes is driving ecological speciation as a by-product. Divergence in body shape, coupled with assortative mating for body shape, produces reproductive isolation that is twice as strong between populations inhabiting different predator regimes than between populations that evolved in similar ecological environments. Gathering analogous data on reproductive isolation at the interspecific level in the genus, we find that this mechanism of speciation may have been historically prevalent in Gambusia. These results suggest that speciation in nature can result as a by-product of divergence in ecologically important traits, producing interspecific patterns that persist long after speciation events have completed.     

ASSORTATIVE MATING PREFERENCES AMONG HYBRIDS OFFERS A ROUTE TO HYBRID SPECIATION

Homoploid speciation generates species without a change in chromosome number via introgressive hybridization and has been considered rare in animals. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has a color pattern that can be recreated by introgression of the H. melpomene red band into an H. cydno genetic background. Wild H. heurippa males show assortative mating based on color pattern and we here investigate the origin of this preference by studying first-generation backcross hybrids between H. melpomene and H. cydno that resemble H. heurippa . These hybrids show assortative mating preferences, showing a strong preference for their own color pattern over that of either parental species. This is consistent with a genetic basis to wing pattern preference and implies, first, that assortative mating preferences would facilitate the initial establishment of a homozygous hybrid color pattern by increasing the likelihood that early generation hybrids mate among themselves. Second, once established such a lineage would inherit assortative mating preferences that would lead to partial reproductive isolation from parental lineages.     

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.     

The context dependence of assortative mating: a demonstration with conspecific salmonid populations

Assortative mating is thought to play a key role in reproductive isolation. However, most experimental studies of assortative mating do not take place in multiple natural environments, and hence, they ignore its potential context dependence. We implemented an experiment in which two populations of brown trout (Salmo trutta) with different natural flow regimes were placed into semi‐natural stream channels under two different artificial flow regimes. Natural reproduction was allowed, and reproductive isolation was measured by means of parentage assignment to compare within‐population vs. between‐population male–female mating and relative offspring production. For both metrics, reproductive isolation was highly context dependent: no isolation was evident under one flow regime, but strong isolation was evident under the other flow regime. These patterns were fully driven by variance in the mating success of males from one of the two populations. Our results highlight how reproductive isolation through assortative mating can be strongly context dependent, which could have dramatic consequences for patterns of gene flow and speciation under environmental change.     

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.     

Positive assortative mating between recently described sympatric morphs of Icelandic sticklebacks

Recently, models of sympatric speciation have suggested that assortative mating can develop between sympatric morphs due to divergence in an ecologically important character. For example, in sympatric pairs of threespine stickleback (Gasterosteus aculeatus L.) size-assortative mating seems to be instrumental in reproductive isolation. Here, we examine courtship behaviour and assortative mating of newly described sympatric stickleback morphs in Lake Thingvallavatn, Iceland. We find that the two morphs show strong positive assortative mating. However, the mechanism involved in mate choice does not seem to be as straightforward as in other similar systems of sympatric stickleback morphs and may involve variation in nest type.     

Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments

Speciation involves the evolution of reproductive isolation between populations. One potentially important mechanism is the evolution of pre- or postzygotic isolation between populations as a by-product of adaptation to different environments. In this paper, we tested for assortative mating between allopatric stickleback populations adapted to different ecological niches. Our experimental design controlled for interpopulation interactions and non-adaptive explanations for assortative mating. We found that prezygotic isolation was surprisingly strong: when given a choice, the majority of matings occurred between individuals from similar environments. Our results indicate that the by-product mechanism is a potent source of reproductive isolation, and likely contributed to the origin of sympatric species of sticklebacks.     

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.     

Delayed prezygotic isolating mechanisms: evolution with a twist

Assortative mating characterizes the situation wherein reproducing individuals pair according to similarity. Usually, the impetus for this bias is attributed to some type of mate choice conferring benefits (e.g., increased fitness or genetic compatibility) and, thereby, promoting speciation and phenotypic evolution. We investigate, by computer simulation of an evolving deme-structured snail population, the ramifications ensuing from passive assortative mating wherein couples exhibiting opposite shell coil direction phenotypes experience a physical constraint on mating success: putative mating partners inhabiting stout dextral and sinistral shells are unable to exchange sperm. Because shell coil chirality genotype is encoded at a single locus by shell coil alleles that are inherited maternally, snails containing sinistral alleles can present the typical dextral phenotype. Consequently, the incidence of a sinistral allele in as few as one snail can be manifested as prezygotic reproductive isolation within a deme in a subsequent generation. However, because the efficacy of achieving this type of prezygotic reproductive isolation is affected by shell form, the likelihood and product of single-gene speciation should be determined by deme interaction (migration) and composition (morphological distribution). We test this hypothesis and show how stochastic migration interacts with passive assortative mating yielding morphologically induced prezygotic reproductive isolation to produce new species phenotypes. The results show that demes can achieve rapid macroscopic phenotypic transformation and indicate that sympatric speciation might be more plausible than naturalists recognize conventionally.     

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.     

Origin and evolution of assortative mating in actively speciating mole rats

The origin and evolution of positive assortative mating in the actively speciating subterranean mole rats of the Spalax ehrenbergi superspecies in Israel, may be deciphered by comparing female mate preference in the laboratory between ancestral and derivative species. Estrous females of the recent derivative of speciation (chromosomal species 2n = 60) showed trimodal mate preference distribution significantly differing from a normal curve. Females consisted of three phenotypes, comprising negative, low positive, and high positive preference for homospecific males. By contrast, mate preference in encounters of ancestral species (2n = 52, 54, and 58) showed a prevalence of a positive homospecific mate preference. It is suggested that the three modal distribution is explicable even on the basis of one major gene with three genotypes. The evolution of ethological reproductive isolation proceeded presumably from a high polymorphism in the most recent derivative of speciation towards increasing monomorphism of positive assortative mating among ancestral species. If an assortative mating locus combines with sexual selection of the frequent male adapted optimally to the local environment, then speciation and adaptation will be tightly linked in the evolution of mole rats.     

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.     

昆虫同域物种形成机制及检验

从生物学、生态和遗传的角度阐述昆虫同域物种形成过程中涉及到的可能性机制。昆虫同域种的分化与作用于同域初始种群的歧化选择密切相关,歧化选择间接导致种群生态特征和遗传特征的分化,促进同域近缘种群间的生殖隔离。同域物种形成的过程中涉及到性状替换、性选择、同型交配等机制。寄主专化型多见于昆虫同域种的分化过程中,一般以植食性昆虫为主。有关昆虫同域物种形成的检验机制有多种,归纳起来主要包括同型交配的检验、遗传漂流的量化、遗传分化程度和连锁不平衡(LD)的检测、杂交后代适合度的估算等。目前发现在许多昆虫种类中存在同域物种形成的可能性,但是有关其隔离机制并没有得到充分的解释。     

GENETIC DIFFERENTIATION AND SELECTION AGAINST MIGRANTS IN EVOLUTIONARILY REPLICATED EXTREME ENVIRONMENTS

We investigated mechanisms of reproductive isolation in livebearing fishes (genus Poecilia) inhabiting sulfidic and nonsulfidic habitats in three replicate river drainages. Although sulfide spring fish convergently evolved divergent phenotypes, it was unclear if mechanisms of reproductive isolation also evolved convergently. Using microsatellites, we found strongly reduced gene flow between adjacent populations from different habitat types, suggesting that local adaptation to sulfidic habitats repeatedly caused the emergence of reproductive isolation. Reciprocal translocation experiments indicate strong selection against immigrants into sulfidic waters, but also variation among drainages in the strength of selection against immigrants into nonsulfidic waters. Mate choice experiments revealed the evolution of assortative mating preferences in females from nonsulfidic but not from sulfidic habitats. The inferred strength of sexual selection against immigrants (RI_s) was negatively correlated with the strength of natural selection (RI_m), a pattern that could be attributed to reinforcement, whereby natural selection strengthens behavioral isolation due to reduced hybrid fitness. Overall, reproductive isolation and genetic differentiation appear to be replicated and direct consequences of local adaptation to sulfide spring environments, but the relative contributions of different mechanisms of reproductive isolation vary across these evolutionarily independent replicates, highlighting both convergent and nonconvergent evolutionary trajectories of populations in each drainage.     

Premating, not postmating, barriers drive genetic dynamics in experimental hybrid populations of the endangered Sonoran topminnow

The timing and pattern of reproductive barrier formation in allopatric populations has received much less attention than the accumulation of reproductive barriers in sympatry. The theory of allopatric speciation suggests that reproductive barriers evolve simply as by-products of overall genetic divergence. However, observations of enhanced premating barriers in allopatric populations suggest that sexual selection driven by intraspecific competition for mates may enhance species-specific signals and accelerate the speciation process. In a previous series of laboratory trials, we examined the strength of premating and postmating barriers in an allopatric species pair of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis. Behavioral observations provided evidence of asymmetrical assortative mating, while reduced brood sizes and male-biased F(1) sex ratios suggest postmating incompatibilities. Here we examine the combined effects of premating and postmating barriers on the genetic makeup of mixed populations, using cytonuclear genotype frequencies of first- and second-generation offspring. Observed genotype frequencies strongly reflect the directional assortative mating observed in behavioral trials, illustrating how isolating barriers that act earlier in the reproductive cycle will have a greater effect on total reproductive isolation and may be more important to speciation than subsequent postmating reproductive barriers.     

Evolution of host specificity drives reproductive isolation among RNA viruses

Ecological speciation hypotheses claim that assortative mating evolves as a consequence of divergent natural selection for ecologically important traits. Reproductive isolation is expected to be particularly likely to evolve by this mechanism in species such as phytophagous insects that mate in the habitats in which they eat. We tested this expectation by monitoring the evolution of reproductive isolation in laboratory populations of an RNA virus that undergoes genetic exchange only when multiple virus genotypes coinfect the same host. We subjected four populations of the RNA bacteriophage phi6 to 150 generations of natural selection on a novel host. Although there was no direct selection acting on host range in our experiment, three of the four populations lost the ability to infect one or more alternative hosts. In the most extreme case, one of the populations evolved a host range that does not contain any of the hosts infectible by the wild-type phi6. Whole genome sequencing confirmed that the resulting reproductive isolation was due to a single nucleotide change, highlighting the ease with which an emerging RNA virus can decouple its evolutionary fate from that of its ancestor. Our results uniquely demonstrate the evolution of reproductive isolation in allopatric experimental populations. Furthermore, our data confirm the biological credibility of simple "no-gene" mechanisms of assortative mating, in which this trait arises as a pleiotropic effect of genes responsible for ecological adaptation.