Assortative mating in mixed swarms of the mosquito Anopheles gambiae s.s. M and S molecular forms,in Burkina Faso,West Africa

The molecular form composition of Anopheles gambiae Giles s.s. (Diptera: Culicidae) mating swarms and the associated mating pairs (copulae) were investigated during two rainy seasons (July to October, 2005 and July to November, 2006) in the villages of Soumousso and Vallée du Kou (VK7). Although the habitats of these villages differ markedly, sympatric populations of M and S molecular forms of An. gambiae s.s. occur in both places periodically. The main aim was to assess the degree to which these molecular forms mate assortatively. In Soumousso, a wooded savannah habitat, the majority of swarm samples consisted of only S‐form males (21/28), although a few M‐form males were found in mixed M‐ and S‐form swarms. In VK7, a rice growing area, the majority of swarm samples consisted of only M‐form males (38/62), until October and November 2006, when there were nearly as many mixed‐form as single‐form swarms. Overall, ～60% of M‐ and S‐form swarms were temporally or spatially segregated; the two forms were effectively prevented from encountering each other. Of the remaining 40% of swarms, however, only about half were single‐form and the rest were mixed‐form. Of the 33 copulae collected from mixed‐form swarms, only four were mixed‐form pairs, significantly fewer than expected by random pairing between forms (χ² = 10.34, d.f. = 2, P < 0.01). Finally, all specimens of inseminated females were of the same form as the sperm contained within their spermatheca (n = 91), even for the four mixed‐form copulae. These findings indicate that assortative mating occurs within mixed‐form swarms, mediated most probably by close‐range mate recognition cues.     

Morphological differentiation may mediate mate-choice between incipient species of Anopheles gambiae s.s

The M and S molecular forms of Anopheles gambiae s.s. have been considered incipient species for more than ten years, yet the mechanism underlying assortative mating of these incipient species has remained elusive. The discovery of the importance of harmonic convergence of wing beat frequency in mosquito mating and its relation to wing size have laid the foundation for exploring phenotypic divergence in wing size of wild populations of the two forms. In this study, wings from field collected mosquitoes were measured for wing length and wing width from two parts of the sympatric distribution, which differ with respect to the strength of assortative mating. In Mali, where assortative mating is strong, as evidenced by low rates of hybridization, mean wing lengths and wing widths were significantly larger than those from Guinea-Bissau. In addition, mean wing widths in Mali were significantly different between molecular forms. In Guinea-Bissau, assortative mating appears comparatively reduced and wing lengths and widths did not differ significantly between molecular forms. The data presented in this study support the hypothesis that wing beat frequency may mediate assortative mating in the incipient species of A. gambiae and represent the first documentation of a morphological difference between the M and S molecular forms.     

Assortative mating between two distinct micro-allopatric populations of Littorina saxatilis (Olivi) on the northeast coast of England

Size assortative mating is a common invertebrate mating pattern and is usually accompanied by male and female sexual selection, and these three behaviours can contribute to reproductive isolation. Two distinct populations of the marine prosobranch Littorina saxatilis, H and M, occur within 15 m of each other on the same shore. Previous studies have demonstrated that these two forms have different reproductive strategies and that the rare hybrids between the two forms show evidence of reproductive dysfunction and hence are less fit than the assumed parental forms. In both populations, female shell height was shown to be a predictor of the number of embryos contained within the brood pouch. The mean shell height of the M population was significantly larger than that of the H population, and the M population matures at a larger shell size than the H population. The two populations show complete assortative mating to type in the field, and occupy different microhabitats on the same shore. Therefore, laboratory-based experiments were performed to determine if assortative mating was maintained in sympatry and also to determine the effect of population density on mate choice. The males of both populations showed sexual selection for female size, choosing to mate with females approximately 10% larger than themselves from an assortment of female sizes. The M population showed complete assortative mating to type, irrespective of the density of H and M females, whereas at low densities the H males did occasionally mate with M females. The role of assortative mating and reinforcement (due to natural selection acting against the less fit hybrids), in maintaining the partial reproductive barrier between the two populations is discussed.     

Evidence for divergent selection between the molecular forms of <Emphasis Type="Italic">Anopheles gambiae</Emphasis>: role of predation

Background  

The molecular forms of Anopheles gambiae are undergoing speciation. They are characterized by a strong assortative mating and they display partial habitat segregation. The M form is mostly found in flooded/irrigated areas whereas the S form dominates in the surrounding areas, but the ecological factors that shape this habitat segregation are not known. Resource competition has been demonstrated between species undergoing divergent selection, but resource competition is not the only factor that can lead to divergence.     

PARTITIONING THE EFFECTS OF SPATIAL ISOLATION,NEST HABITAT,AND INDIVIDUAL DIET IN CAUSING ASSORTATIVE MATING WITHIN A POPULATION OF THREESPINE STICKLEBACK

Assortative mating is measured as a phenotypic or genotypic correlation between mates. Although biologists typically view assortative mating in terms of mate preference for similar partners, correlations between mates can also arise from phenotypic spatial structure arising from spatial isolation or habitat preferences. Here, we test whether diet‐assortative mating within an ecologically variable population of threespine stickleback results from small‐scale geographic isolation or microhabitat preference. We find evidence for assortative mating in the form of a positive correlation between mated pairs’ diets (measured using stable isotopes). Stable isotopes reveal diet differences between different nesting areas and among individuals using different nest habitat within a nesting area. This spatial segregation of diet types should generate some assortative mating, but is insufficient to explain the observed assortment strength. Significant male–female isotope correlations remain after controlling for spatial variables. We therefore conclude that sticklebacks’ diet‐assortative mating arises from additional behavioral preference. More generally, our results illustrate the point that spatial segregation can only drive appreciable levels of phenotypic assortative mating when environment‐phenotype correlations are parallel and strong in both sexes. Consequently, intraspecific assortative mating may typically entail mating preferences rather than just spatial cosegregation of phenotypes.     

Pairing dynamics and the origin of species

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

Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host

Sex-role-reversed mating systems in which females compete for males and males may be choosy are usually associated with males investing more than females in offspring. We report that sex-role reversal may also be caused by selfish genetic elements which distort the sex ratio towards females. Some populations of the butterflies Acraea encedon and Acraea encedana are extremely female biased because over 90% of females are infected with a Wolbachia bacterium that is maternally inherited and kills male embryos. Many females in these populations are virgins suggesting that their reproductive success may be limited by access to males. These females form lekking swarms at landmarks in which females exhibit behaviours which we interpret as functioning to solicit matings from males. The hypothesis that female A. encedon swarm in order to mate is supported by the finding that, in release recapture experiments, mated females tend to leave the swarm while unmated females remained. This behaviour is a sex-role-reversed form of a common mating system in insects in which males form lekking swarms at landmarks and compete for females. Female lekking swarms are absent from less female-biased populations and here the butterflies are instead associated with resources in the form of the larval food plant.     

Non-random Mating in the Dance Fly Empis borealis: The Importance of Male Choice

In the dance-fly Empis borealis (Diptera, Empididae), females form swarms to which males, carrying a nuptial gift, come for mating. We examined whether males or females were choosy and/or competed for mates. First, measurements of the size relationships between copulating males and females, nuptial gifts and the swarming females from different swarms were assessed. Second, male visiting time in differently sized female swarms was recorded. Larger (wing-length) females participated disproportionately in copulations in each swarm, but not for the population at large. Female mating status (virgin/non-virgin) or proximity to oviposition (egg size) did not influence the likelihood of copulation. No assortative mating pattern was found: male size and size of nuptial gift did not correlate with size of the mating female. The time spent by males in swarms increased with the number of females present and it took longer when males left a swarm without copulation than when doing so. Male visiting time per female was negatively correlated with number of females in swarms. Males more often left smaller than larger swarms without mating. We conclude that E. borealis males discriminate among females but find no evidence for male competition or for female choice. It is still a question to what degree females compete for males.     

Breeding season and nesting assemblages in two forms oflethenteron reissneri, with reference to reproductive isolating mechanisms

The level of reproductive isolation and reproductive characteristics were examined in sympatric populations of the northern and southern forms ofLethenteron reissneri, in the Ushiwatari Stream, a tributary of the Gakko River, Yamagata Prefecture, Japan, to elucidate the reproductive isolating mechanisms existing between them. Extensive allozyme data showed no gene exchange between the two forms in the study area, evidence of their strict reproductive isolation from each other. The spawning seasons overlapped between the northern and southern forms, the spawning period of the latter being slightly later than that of the former. The size at maturity also overlapped between the two forms, although the southern form indicated significantly larger in average size than the northern one. These results suggested that neither seasonal reproductive isolation nor size assortative mating occurred. On the other hand, the nesting assemblages were observed to comprise only males and females of each respective form, suggesting that a recognition system restricted to each form may operate as a premating isolating mechanism.     

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.     

DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae

Anopheles gambiae populations in west Africa are complex, being composed of multiple, sympatric subpopulations. Recent studies have failed to reveal significant genetic differences among subpopulations, stimulating a debate regarding the levels of gene flow among them. The observed homogeneity may be the consequence of substantial contemporary gene flow or it may be that reproductive isolation is complete, but too recent for the accumulation of significant levels of genic divergence. Here, we report the results of a study estimating contemporary levels of gene flow between An. gambiae subpopulations by analysing females and transferred sperm removed from their reproductive systems. A total of 251 female and associated sperm extracts was analysed from a single site in Mali. Two molecular forms of An. gambiae, the M- and S-forms, occurred in sympatry at this site. Overall, we found very strong positive assortative mating within forms, however, we did observe significant hybridization between forms. In the M subpopulation 2/195 females (1.03%) contained sperm from S-form males and in 55 S-form females we found one female containing M-form sperm (1.82%). We also identified a mated M xS hybrid adult female. From mating frequencies, we estimate the Nem between the M- and S-form at 16.8, and from the adult hybrid frequency at 5.6. These values are consistent with our earlier estimate, based on FST for 21 microsatellite loci in which Nem = 5.8. We conclude that the general lack of genetic divergence between the M and S subpopulations of An. gambiae can be explained entirely by contemporary gene flow.     

The origins of premating reproductive isolation: testing hypotheses in the grasshopper Chorthippus parallelus

There are many proposed routes for the origin of premating reproductive isolation, but few systematic studies aimed at testing their relative importance. Accumulated information about the biogeographical history of the European meadow grasshopper, Chorthippus parallelus, has allowed us to make a planned series of comparisons among populations aimed at distinguishing the contributions of some of these hypotheses. We have compared the effects on assortative mating of long-term isolation in glacial refugia, founder events during postglacial colonization, and sympatry with a closely related species. A likelihood-based analysis allowed us to separate effects of variation in male and female mating propensity among populations from variation in mate choice leading to assortative mating. All three effects contributed significantly to the overall variation in mating pattern in a set of 21 pairwise comparisons among seven populations. Male cuticular composition, but not other candidate signals, was significantly associated with the level of assortative mating. Of the hypotheses for the origin of reproductive isolation, only the predictions of the founder hypothesis explained a significant amount of the variation in assortative mating. This does not rule out the possiblity that there may be some other explanation. Having established the pattern of divergence, it is possible to generate hypotheses that explain our results at least as well as the founder hypothesis. However, because many such post hoc hypotheses are possible, they cannot be tested with this dataset. On this basis, our results favor the hypothesis that some aspect of the colonization process tends to accelerate divergence in mating signals leading to premating reproductive isolation. This could be accomplished through any one of several mechanisms. Colonization involves many bottlenecks as new populations are established at the edge of the range by long-distance migrants. Genetic effects may be important, but these bottlenecks may also alter the conditions under which mates are found and chosen, as suggested by Kaneshiro. At the same time, the colonizing populations may encounter novel environmental challenges.     

Reinforcement of mate preference among hybridizing Heliconius butterflies

Recent models of mate preference evolution suggest that direct selection on alleles at preference loci and correlated evolution of preference with locally adapted mating cues are more likely to drive the evolution of assortative mate preference than reinforcement. Mate preference evolution in mimetic Heliconius butterflies has been attributed to all three forms of selection, but here we show that reinforcement has been critical. By examining geographical variation in assortative mating and male mate preference among seven populations of three hybridizing Heliconius species from Costa Rica, we found pronounced character displacement of preference such that sexual isolation was enhanced in areas of interspecific contact. Of the different explanations for the evolution of assortative mate preference, only reinforcement is dependent on interspecific contact in this system. Thus, the observed pattern of reproductive character displacement of mate preference is best explained as a product of indirect selection generated by natural selection against nonmimetic hybrids.     

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.     

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.     

Divergent host-plant use promotes reproductive isolation among cynipid gall wasp populations

Ecological speciation occurs when reproductive isolation evolves as a consequence of divergent natural selection among environments. A direct prediction of this process is that ecologically divergent pairs of populations will exhibit greater reproductive isolation than ecologically similar pairs of populations. By comparing allopatric populations of the cynipid gall wasp Belonocnema treatae infesting Quercus virginiana and Quercus geminata, we tested the role that divergent host use plays in generating ecological divergence and sexual isolation. We found differences in body size and gall structure associated with divergent host use, but no difference in neutral genetic divergence between populations on the same or different host plant. We observed significant assortative mating between populations from alternative host plants but not between allopatric populations on the same host plant. Thus, we provide evidence that divergent host use promotes speciation among gall wasp populations.     

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.     

Digest: The evolution of sexual imprinting as an assortative mating mechanism*

In this issue, Yeh et al. (2018) investigated whether sexual imprinting could act as an assortative mating mechanism, reducing hybridization and increasing premating isolation. While they indeed find that imprinting leads to assortative mating and reduced hybridization, the strength at which imprinting evolves is usually intermediate, because it is counterbalanced by the costs of imprinting and the benefits of adaptive hybridization. Thus, while sexual imprinting can act as an assortative mating mechanism, it is often not the sole element of female mate choice.     

No mate preference associated with the supergene controlling social organization in Alpine silver ants

Disassortative mating is a powerful mechanism stabilizing polymorphisms at sex chromosomes and other supergenes. The Alpine silver ant, Formica selysi, has two forms of social organization—single‐queen and multiple‐queen colonies—determined by alternate haplotypes at a large supergene. Here, we explore whether mate preference contributes to the maintenance of the genetic polymorphism at the social supergene. With mate choice experiments, we found that females and males mated randomly with respect to social form. Moreover, queens were able to produce offspring irrespective of whether they had mated with a male from the same or the alternative social form. Yet, females originating from single‐queen colonies were more fertile, suggesting that they may be more successful at independent colony founding. We conclude that the pattern of asymmetric assortative mating documented from mature F. selysi colonies in the field is not caused by mate preferences or major genetic incompatibilities between social forms. More generally, we found no evidence that disassortative mate preference contributes to the maintenance of polymorphism at this supergene controlling ant social organization.     

Reinforcement and the genetics of nonrandom mating

Abstract.— The occurrence of reinforcement is compared when premating isolation is caused by the spread of a gene causing females to prefer to mate with males carrying a population-specific trait (a "preference" model) and by a gene that causes females to prefer to mate with males that share their own trait phenotype (an "assortative mating" model). Both two-island models, which have symmetric gene flow, and continent-island models, which have one-way gene flow, are explored. Reinforcement is found to occur much more easily in a two-island assortative mating model than in any of the other three models. This is due primarily to the fact that in this model the assortative mating allele will automatically become genetically associated in each population with the trait allele that is favored by natural selection on that island. In contrast, natural selection on the trait both favors and opposes the evolution of premating isolation in the two-island preference model, depending on the particular population. These results imply that species recognition in the context of mating may evolve particularly easily when it targets cues that are favored by natural selection in each population. In the continent-island models, reinforcement is found to occur more often under the preference model than the assortative mating model, thus reversing the trend from the two-island models. Patterns of population subdivision may therefore play a role in determining what types of premating isolation may evolve.