Asymmetric dominance and asymmetric mate choice oppose premating isolation after allopatric divergence

Assortative mating promotes reproductive isolation and allows allopatric speciation processes to continue in secondary contact. As mating patterns are determined by mate preferences and intrasexual competition, we investigated male–male competition and behavioral isolation in simulated secondary contact among allopatric populations. Three allopatric color morphs of the cichlid fish Tropheus were tested against each other. Dyadic male–male contests revealed dominance of red males over bluish and yellow‐blotch males. Reproductive isolation in the presence of male–male competition was assessed from genetic parentage in experimental ponds and was highly asymmetric among pairs of color morphs. Red females mated only with red males, whereas the other females performed variable degrees of heteromorphic mating. Discrepancies between mating patterns in ponds and female preferences in a competition‐free, two‐way choice paradigm suggested that the dominance of red males interfered with positive assortative mating of females of the subordinate morphs and provoked asymmetric hybridization. Between the nonred morphs, a significant excess of negative assortative mating by yellow‐blotch females with bluish males did not coincide with asymmetric dominance among males. Hence, both negative assortative mating preferences and interference of male–male competition with positive assortative preferences forestall premating isolation, the latter especially in environments unsupportive of competition‐driven spatial segregation.     

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.     

Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish

Mechanisms of speciation in cichlid fish were investigated by analyzing population genetic models of sexual selection on sex-determining genes associated with color polymorphisms. The models are based on a combination of laboratory experiments and field observations on the ecology, male and female mating behavior, and inheritance of sex-determination and color polymorphisms. The models explain why sex-reversal genes that change males into females tend to be X-linked and associated with novel colors, using the hypothesis of restricted recombination on the sex chromosomes, as suggested by previous theory on the evolution of recombination. The models reveal multiple pathways for rapid sympatric speciation through the origin of novel color morphs with strong assortative mating that incorporate both sex-reversal and suppressor genes. Despite the lack of geographic isolation or ecological differentiation, the new species coexists with the ancestral species either temporarily or indefinitely. These results may help to explain different patterns and rates of speciation among groups of cichlids, in particular the explosive diversification of rock-dwelling haplochromine cichlids.     

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.     

Disassortative mating prevails in style‐dimorphic Narcissus papyraceus despite low reciprocity and compatibility of morphs

Evolution to reduce inbreeding can favor disassortative (intermorph) over assortative (intramorph) mating in hermaphroditic sexually polymorphic plant species. Heterostyly enhances disassortative pollination through reciprocal placement of stigmas and anthers of morphs and appropriate pollinators. Stylar dimorphism in which there is not reciprocal anther placement may compromise disassortative mating, particularly when there is not intramorph incompatibility. Variable rates of disassortative mating along with differential female fecundity or siring success among floral morphs could lead to variation in morph ratio. We investigated mating patterns, female fecundity, and siring success of style‐length morphs in Narcissus papyraceus, a self‐incompatible but morph‐compatible species with dimorphic (long‐ and short‐styled) and monomorphic (long‐styled) populations in central and north regions of its range, respectively. We established experimental populations in both regions and exposed them to ambient pollinators. Using paternity analysis, we found similar siring success of morphs and high disassortative mating in most populations. Female fecundity of morphs was similar in all populations. Although these results could not completely explain the loss of dimorphism in the species’ northern range, they provided evidence for the evolutionary stability of stylar dimorphism in N. papyraceus in at least some populations. Our findings support the hypothesis that prevailing intermorph mating is key for the maintenance of stylar dimorphism.     

Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish

Hybrid speciation is constrained by the homogenizing effects of gene flow from the parental species. In the absence of post‐mating isolation due to structural changes in the genome, or temporal or spatial premating isolation, another form of reproductive isolation would be needed for homoploid hybrid speciation to occur. Here, we investigate the potential of behavioural mate choice to generate assortative mating among hybrids and parental species. We made three‐first‐generation hybrid crosses between different species of African cichlid fish. In three‐way mate‐choice experiments, we allowed hybrid and nonhybrid females to mate with either hybrid or nonhybrid males. We found that hybrids generally mated nonrandomly and that hybridization can lead to the expression of new combinations of traits and preferences that behaviourally isolate hybrids from both parental species. Specifically, we find that the phenotypic distinctiveness of hybrids predicts the symmetry and extent of their reproductive isolation. Our data suggest that behavioural mate choice among hybrids may facilitate the establishment of isolated hybrid populations, even in proximity to one or both parental species.     

MALE MATING PREFERENCES AND ASSORTATIVE MATING IN THE SOLDIER BEETLE

Mating preferences for a color characteristic were examined in three northern Georgia populations of the soldier beetle, Chauliognathus pennsylvanicus De Geer, by comparing observed and expected frequencies of matings to the same phenotype. The three populations are apparently in a zone of secondary contact between disparate color morphs. In the most northern population sampled, preferences were strong and were associated with positive assortative mating with respect to the color characteristic. In the southern population, neither assortative mating nor mating preference was strong, while in the middle population, preferences were expressed in the absence of assortative mating. Mating preferences cannot be attributed to host-plant choice, microhabitat choice, or simple conditioning on the phenotype of the last mate. However, they may represent part of a specific mate-recognition system which has been maintained in part of the zone of overlap but which has eroded in other areas.     

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.     

HYBRIDIZATION STUDIES ON THE HOST RACES OF EUROSTA SOLIDAGINIS: IMPLICATIONS FOR SYMPATRIC SPECIATION

We studied the inheritance of survival ability in host-associated populations of the tephritid fly, Eurosta solidaginis, to test predictions of sympatric speciation models. Eurosta solidaginis induces galls on two species of goldenrod, Solidago altissima and S. gigantea. The host-associated populations have been hypothesized to be host races that originated in sympatry (Craig et al. 1993). We found evidence for disruptive selection for host use, which is a critical assumption of sympatric speciation models. Each host race had higher survival rates on their host plant than on the alternative host. F₁ and backcross hybrids also had lower survival rates than the pure host-race flies on their host plant. Since assortative mating occurs due to host-plant preference (Craig et al. 1993) this would select for divergence in host preference. Low hybrid survival could have been due to strong genetic incompatibilities of the populations or due to host adaptation by each population. Strong genetic incompatibilities would result in poor survival on all host plants, while host adaptation could result in low overall survival with high hybrid survival on some host plants with particularly “benign” environments. High survival of F₁, F₂, and backcross hybrids on some plant genotypes in some years supported the host adaptation hypothesis. F₁ flies mated and oviposited normally and produced viable F₂ and backcross hybrids indicating gene flow is possible between the host races. A few flies developed and emerged on the alternative host plant. This demonstrates that genes necessary to utilize the alternative host exist in both host races. This could have facilitated the origin of one of the populations via a host shift from the ancestral host. The inheritance of survival ability appears to be an autosomal trait. We did not find evidence that survival ability was maternally influenced or sex linked.     

Conditions for sympatric speciation: A diploid model incorporating habitat fidelity and non-habitat assortative mating

Summary Three types of genes have been proposed to promote sympatric speciation: habitat preference genes, assortative mating genes and habitat-based fitness genes. Previous computer models have analysed these genes separately or in pairs. In this paper we describe a multilocus model in which genes of all three types are considered simultaneously. Our computer simulations show that speciation occurs in complete sympatry under a broad range of conditions. The process includes an initial diversification phase during which a slight amount of divergence occurs, a quasi-equilibrium phase of stasis during which little or no detectable divergence occurs and a completion phase during which divergence is dramatic and gene flow between diverging habitat morphs is rapidly eliminated. Habitat preference genes and habitat-specific fitness genes become associated when assortative mating occurs due to habitat preference, but interbreeding between individuals adapted to different habitats occurs unless habitat preference is almost error free. However, nonhabitat assortative mating, when coupled with habitat preference can eliminate this interbreeding. Even when several loci contribute to the probability of expression of non-habitat assortative mating and the contributions of individual loci are small, gene flow between diverging portions of the population can terminate within less than 1000 generations.     

ALLOPATRIC DIVERGENCE AND SPECIATION IN CORAL REEF FISH: THE THREE‐SPOT DASCYLLUS,DASCYLLUS TRIMACULATUS,SPECIES COMPLEX

Long pelagic larval phases and the absence of physical barriers impede rapid speciation and contrast the high diversity observed in marine ecosystems such as coral reefs. In this study, we used the three‐spot dascyllus (Dascyllus trimaculatus) species complex to evaluate speciation modes at the spatial scale of the Indo‐Pacific. The complex includes four recognized species and four main color morphs that differ in distribution. Previous studies of the group using mitochondrial DNA revealed a noncongruence between color morphs and genetic groupings; with two of the color morphs grouped together and one color morph separated into three clades. Using extensive geographic sampling of 563 individuals and a combination of mitochondrial DNA sequences and 13 nuclear microsatellites, we defined population/species boundaries and inferred different speciation modes. The complex is composed of seven genetically distinct entities, some of which are distinct morphologically. Despite extensive dispersal abilities and an apparent lack of barriers, observed genetic partitions are consistent with allopatric speciation. However, ecological pressure, assortative mating, and sexual selection, were likely important during periods of geographical isolation. This study therefore suggests that primarily historical factors later followed by ecological factors caused divergence and speciation in this group of coral reef fish.     

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.     

Color polymorphism in siblingAmphiprion: is the reef-fish lottery rigged?

Synopsis Captive-bred offspring from a single pair ofAmphiprion frenatus displayed two independent color polymorphisms, one for juvenile stripe pattern and one for adult color. The adult polymorphism encompassed color morphs representingA. frenatus, A. rubrocinctus andA. melanopus. Positive assortative mating occurred, with viable F₂ offspring from one pairing. Hybridization has been achieved previously betweenA. melanopus, A. frenatus andA. ephippium, so these four species may be stable polymorphs of a single species, the different morphs selectively maintained in different geographic regions. The extent of polymorphism among marine fishes is poorly understood.     

Genetic differentiation between the ant Myrmica rubra and its microgynous social parasite

Hymenopteran inquiline species have been proposed to originate by sympatric speciation through intraspecific social parasitism. One such parasite, Myrmica microrubra, was recently synonymized with its Myrmica rubra host, because comparisons across Europe indicated insufficient genetic differentiation. Here, we use microsatellite markers to study genetic differentiation more precisely in a sample of Finnish M. rubra and its inquilines collected at two localities, supplemented with mitochondrial DNA sequences. The parasite had much lower genetic variation than the host at three of the four loci studied. Genetic differentiation between the host populations was moderate (F _ST = 0.089), whereas the parasite populations were more strongly subdivided (F _ST = 0.440). The host and parasite were highly genetically differentiated both across populations (F _ST = 0.346) and in strict sympatry (0.327, 0.364), a result that remained robust both in a haplotype network and in PCA ordination. Individual assignments of genotypes indicated that gene flow between sympatric host and inquiline populations is reduced by about an order of magnitude relative to the gene flow within the morphs. Our results suggest that the parasitic morph of M. rubra may be an incipient species, but it remains unclear to what extent the observed genetic differentiation between host and inquiline is due to possible assortative mating and selection against hybrids or to recurrent bottlenecking and genetic drift. We conclude that an explicitly functional species concept would be unambiguous in treating this inquiline as a full species, as it begets its own kind and maintains its integrity in spite of occasional interbreeding with the host.     

Divergent warning patterns contribute to assortative mating between incipient Heliconius species

Theoretical models suggest that traits under divergent ecological selection, which also contribute to assortative mating, will facilitate speciation with gene flow. Evidence for these so‐called “magic traits” now exists across a range of taxa. However, their importance during speciation will depend on the extent to which they contribute to reproductive isolation. Addressing this requires experiments to determine the exact cues involved as well as estimates of assortative mating in the wild. Heliconius butterflies are well known for their diversity of bright warning color patterns, and their amenability to experimental manipulation has provided an excellent opportunity to test their role in reproductive isolation. Here, we reveal that divergent color patterns contribute to mate recognition between the incipient species Heliconius himera and H. erato, a taxon pair for which assortative mating by color pattern has been demonstrated among wild individuals: First, we demonstrate that males are more likely to attempt to mate conspecific females; second, we show that males are more likely to approach pinned females that share their own warning pattern. These data are valuable as these taxa likely represent the early stages of speciation, but unusually also allow comparisons with rates of interbreeding between divergent ecologically relevant phenotypes measured in the wild.     

Case studies and mathematical models of ecological speciation. 3: Ecotype formation in a Swedish snail

Formation of partially reproductively isolated ecotypes in the rough periwinkle, Littorina saxatilis , may be a case of incipient nonallopatric ecological speciation. To better understand the dynamics of ecotype formation, its timescale, driving forces and evolutionary consequences, we developed a spatially explicit, individual-based model incorporating relevant ecological, spatial and mate selection data for Swedish L. saxatilis . We explore the impact of bounded hybrid superiority, ecological scenarios and mate selection systems on ecotype formation, gene flow and the evolution of prezygotic isolation. Our model shows that ecotypes are expected to form rapidly in parapatry under conditions applicable to Swedish L. saxatilis and may proceed to speciation. However, evolution of nonrandom mating had complex behaviour. Ecotype evolution was inhibited by pre-existing mating preferences, but facilitated by the evolution of novel preferences. While in many scenarios positive assortative mating reduced gene flow between ecotypes, in others negative assortative mating arose, preferences were lost after ecotype formation, preferences were confined to one ecotype or the ancestral ecotype became extinct through sexual selection. Bounded hybrid superiority (as observed in nature) enhanced ecotype formation but increased gene flow. Our results highlight that ecotype formation and speciation are distinct processes: factors that contribute to ecotype formation can be detrimental to speciation and vice versa. The complex interactions observed between local adaptation and nonrandom mating imply that generalization from data is unreliable without quantitative theory for speciation.     

Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria

Colour polymorphisms have fascinated evolutionary ecologists for a long time. Yet, knowledge on the mechanisms that allow their persistence is restricted to a handful of well‐studied cases. We studied two species of Lake Victoria cichlid fish, Neochromis omnicaeruleus and Neochromis greenwoodi, exhibiting very similar sex‐linked colour polymorphisms. The ecology and behaviour of one of these species is well studied, with colour‐based mating and aggression preferences. Here, we ask whether the selection potentially resulting from female and male mating preferences and aggression biases reduces gene flow between the colour morphs and permits differentiation in traits other than colour. Over the past 14 years, the frequencies of colour morphs have somewhat oscillated, but there is no evidence for directional change, suggesting the colour polymorphism is persistent on an ecological timescale. We find limited evidence of eco‐morphological differentiation between sympatric ancestral (plain) and derived (blotched) colour morphs. We also find significantly nonrandom genotypic assignment and an excess of linkage disequilibrium in the plain morph, which together with previous information on mating preferences suggests nonrandom mating between colour morphs. This, together with negative frequency‐dependent sexual selection, found in previous studies, may facilitate maintenance of these polymorphisms in sympatry.     

Flickers of speciation: Sympatric colour morphs of the arc‐eye hawkfish,Paracirrhites arcatus,reveal key elements of divergence with gene flow

One of the primary challenges of evolutionary research is to identify ecological factors that favour reproductive isolation. Therefore, studying partially isolated taxa has the potential to provide novel insight into the mechanisms of evolutionary divergence. Our study utilizes an adaptive colour polymorphism in the arc‐eye hawkfish (Paracirrhites arcatus) to explore the evolution of reproductive barriers in the absence of geographic isolation. Dark and light morphs are ecologically partitioned into basaltic and coral microhabitats a few metres apart. To test whether ecological barriers have reduced gene flow among dark and light phenotypes, we evaluated genetic variation at 30 microsatellite loci and a nuclear exon (Mc1r) associated with melanistic coloration. We report low, but significant microsatellite differentiation among colour morphs and stronger divergence in the coding region of Mc1r indicating signatures of selection. Critically, we observed greater genetic divergence between colour morphs on the same reefs than that between the same morphs in different geographic locations. We hypothesize that adaptation to the contrasting microhabitats is overriding gene flow and is responsible for the partial reproductive isolation observed between sympatric colour morphs. Combined with complementary studies of hawkfish ecology and behaviour, these genetic results indicate an ecological barrier to gene flow initiated by habitat selection and enhanced by assortative mating. Hence, the arc‐eye hawkfish fulfil theoretical expectations for the earliest phase of speciation with gene flow.     

Variable discrimination and asymmetric preferences in laboratory tests of reproductive isolation between cichlid colour morphs

Mating behaviour affects reproductive isolation and phenotypic differentiation. In Lake Tanganyika, the cichlid fish Tropheus moorii diversified into numerous, currently allopatric colour variants. Allopatric isolation is periodically interrupted by dispersal and secondary contact during lake level fluctuations, making long‐term differentiation partly dependent on assortative mating. Laboratory experiments with two moderately distinct morphs revealed assortative female preferences in one (Nakaku), but random mate choice in the other morph (Mbita). No discrimination was apparent between two subtly differentiated morphs (Chimba and Moliro). Tested against each other in a previous study, the highly distinct Moliro and Nakaku exhibited strong assortative preferences. The correlation between colour pattern similarity and mate discrimination suggests that allopatry and philopatric behaviour are less crucial for the maintenance of differentiation between highly distinct morphs than for more similar morphs. Interestingly, the asymmetric isolation in one pair of morphs is congruent with a pattern of unidirectional mitochondrial introgression between populations.     

No evidence for size‐assortative mating in the wild despite mutual mate choice in sex‐role‐reversed pipefishes

Size‐assortative mating is a nonrandom association of body size between members of mating pairs and is expected to be common in species with mutual preferences for body size. In this study, we investigated whether there is direct evidence for size‐assortative mating in two species of pipefishes, Syngnathus floridae and S. typhle, that share the characteristics of male pregnancy, sex‐role reversal, and a polygynandrous mating system. We take advantage of microsatellite‐based “genetic‐capture” techniques to match wild‐caught females with female genotypes reconstructed from broods of pregnant males and use these data to explore patterns of size‐assortative mating in these species. We also develop a simulation model to explore how positive, negative, and antagonistic preferences of each sex for body size affect size‐assortative mating. Contrary to expectations, we were unable to find any evidence of size‐assortative mating in either species at different geographic locations or at different sampling times. Furthermore, two traits that potentially confer a fitness advantage in terms of reproductive success, female mating order and number of eggs transferred per female, do not affect pairing patterns in the wild. Results from model simulations demonstrate that strong mating preferences are unlikely to explain the observed patterns of mating in the studied populations. Our study shows that individual mating preferences, as ascertained by laboratory‐based mating trials, can be decoupled from realized patterns of mating in the wild, and therefore, field studies are also necessary to determine actual patterns of mate choice in nature. We conclude that this disconnect between preferences and assortative mating is likely due to ecological constraints and multiple mating that may limit mate choice in natural populations.