Allopatric Males Research Articles

Fine-scale geographic patterns of gene flow and reproductive character displacement in Drosophila subquinaria and Drosophila recens.

When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species Drosophila subquinaria and Drosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine-scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. Within D.subquinaria, reinforcement is extremely effective: we find variation in mate discrimination both against D.recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression from D.recens. In D.recens, we do not find evidence for increased mate discrimination in sympatry, even where D.recens is rare, consistent with substantial gene flow throughout the species' range. Finally, we find that introgression between species is asymmetric, with more from D.recens into D.subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement within D.subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations.

Does competitive interaction drive species recognition in a house mouse secondary contact zone?

Miscommunication may induce a high risk of unnecessary escalated fights between competitors (populations to species), resulting in selection favoring signal divergence through agonistic character displacement (ACD). When signals allowing discrimination between competitors are also involved in mate recognition, ACD could explain reproductive character displacement (RCD). We tested interference competition between males as a potential driver of RCD (here, subspecies recognition) in a secondary contact zone between two mouse subspecies (Mus musculus musculus and Mus musculus domesticus) displaying asymmetric dominance. Since such asymmetry could create a conflict between subspecies (compatibility) and quality (dominance) recognition in the contact zone, we tested for geographic variation in female preference for dominant males in the subordinate subspecies, musculus. We assessed competition between males and tested ACD during dyadic encounters comparing behavior displayed during trials between heterosubspecifics originating from populations close to the secondary contact (“contact”) and further away (“allopatric”). We also compared behavior of contact versus allopatric males during homosubspecific versus heterosubspecific trials to test whether subspecies discrimination evolved under competitive interference. Although domesticus dominated most heterosubspecific trials regardless of geographic origin, agonistic behavior was more marked (i.e., lower attack latencies) during contact than allopatric encounters, suggesting that ACD occurred. Comparing behavior during homosubspecific and heterosubspecific encounters, only allopatric musculus displayed differences, that is, higher attack latencies toward heterosubspecifics, indicating that discrimination between competitors did not evolve with ACD. Finally, although allopatric musculus females seemed to prefer dominant males, their contact counterparts did not, suggesting that “compatibility” may have outweighed “quality” under a risk of hybridization.

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba.

Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations.

Female preference for sympatric vs. allopatric male throat color morphs in the mesquite lizard (Sceloporus grammicus) species complex.

Color polymorphic sexual signals are often associated with alternative reproductive behaviors within populations, and the number, frequency, or type of morphs present often vary among populations. When these differences lead to assortative mating by population, the study of such polymorphic taxa may shed light on speciation mechanisms. We studied two populations of a lizard with polymorphic throat color, an important sexual signal. Males in one population exhibit orange, yellow, or blue throats; whereas males in the other exhibit orange, yellow, or white throats. We assessed female behavior when choosing between allopatric and sympatric males. We asked whether females discriminated more when the allopatric male was of an unfamiliar morph than when the allopatric male was similar in coloration to the sympatric male. We found that female rejection of allopatric males relative to sympatric males was more pronounced when males in a pair were more different in throat color. Our findings may help illuminate how behavioral responses to color morph differences between populations with polymorphic sexual signals contribute to reproductive isolation.

Reinforcement of male mate preferences in sympatric killifish species Lucania goodei and Lucania parva

Reinforcement occurs when reduced hybrid fitness leads to the evolution of a stronger prezygotic isolation. Populations sympatric with closely related species, where hybridization occurs, are predicted to have stronger mate preferences than allopatric populations. The reinforcement of male mate preference is thought to be rarer than the reinforcement of female preference, but this inference may be biased by the lack of studies on male preference. We tested male mate preferences from sympatric and allopatric populations of two closely related species of killifish: Lucania goodei and Lucania parva. We found that sympatric males had greater preferences for conspecific females than allopatric males. Furthermore, conspecific preferences in allopatric populations were weakest when these populations were geographically distant (>50 km) from those of heterospecifics. Our data suggest that reinforcement has contributed to male conspecific preference and speciation in Lucania.

Asymmetric reproductive character displacement in male aggregation behaviour

Reproductive character displacement--the evolution of traits that minimize reproductive interactions between species--can promote striking divergence in male signals or female mate preferences between populations that do and do not occur with heterospecifics. However, reproductive character displacement can affect other aspects of mating behaviour. Indeed, avoidance of heterospecific interactions might contribute to spatial (or temporal) aggregation of conspecifics. We examined this possibility in two species of hybridizing spadefoot toad (genus Spea). We found that in Spea bombifrons sympatric males were more likely than allopatric males to associate with calling males. Moreover, contrary to allopatric males, sympatric S. bombifrons males preferentially associated with conspecific male calls. By contrast, Spea multiplicata showed no differences between sympatry and allopatry in likelihood to associate with calling males. Further, sympatric and allopatric males did not differ in preference for conspecifics. However, allopatric S. multiplicata were more variable than sympatric males in their responses. Thus, in S. multiplicata, character displacement may have refined pre-existing aggregation behaviour. Our results suggest that heterospecific interactions can foster aggregative behaviour that might ultimately contribute to clustering of conspecifics. Such clustering can generate spatial or temporal segregation of reproductive activities among species and ultimately promote reproductive isolation.

THE EVOLUTION OF REPRODUCTIVE CHARACTER DISPLACEMENT CONFLICTS WITH HOW SEXUAL SELECTION OPERATES WITHIN A SPECIES

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.

Mate Choice by Non‐Virgin Females Contributes to Reproductive Isolation between Populations of the Harlequin Beetle‐Riding Pseudoscorpion

AbstractDetermining whether reproductive isolation evolves through mate choice and/or gametic factors that prevent fertilization or through the post‐zygotic mechanisms of hybrid sterility or inviability is fundamental to understanding speciation. Investigation of the pre‐ and post‐zygotic components of reproductive isolation is facilitated in the pseudoscorpion, Cordylochernes scorpioides, by its indirect method of sperm transfer and viviparous embryonic development. Previous research on this species, in which mate discrimination was assessed in virgin females, suggested that female choice played only a minor role in reproductive isolation between populations from French Guiana and Panamá. Here, in a study of three allopatric populations of C. scorpioides from Panamá, we assessed mating‐stage isolation in both virgin and once‐mated females, and found that female discrimination depends critically on mating status. Virgin females were almost invariably receptive, showing no tendency to discriminate against males from allopatric populations. By contrast, non‐virgin females were significantly more likely to reject foreign males than males from their own population. Male sexual motivation could not account for differences in either female sexual receptivity or male success in sperm transfer. Allopatric and sympatric males did not differ in number of spermatophores deposited as either a female’s first or second mate. Nonetheless, allopatric males achieved significantly lower sperm transfer success not only with choosy, non‐virgin females but also with virgin females. Given the lack of behavioral discrimination by virgin females, female receptivity was not the only factor influencing differences in sperm transfer success. Multivariate analysis of spermatophore morphology suggests that the higher failure rate of matings between allopatric males and virgin females resulted from population differences in sperm packet architecture. Overall, our findings indicate that assessment of discrimination against allopatric males that is limited to virgin females may seriously underestimate the contribution of female mate choice to reproductive isolation between populations.

Character displacement of male nuptial colour in threespine sticklebacks (Gasterosteus aculeatus)

Character displacement in signalling traits occurs when differences between species are greater in sympatry than where either species occurs alone. Finding character displacement in a signalling trait suggests that the trait has diverged as a result of interspecific interactions such as competition, aggression, predation, or reproductive interference. We tested for character displacement of male nuptial coloration between sympatric species of threespine sticklebacks (Gasterosteus aculeatus spp.). The sympatric pairs consist of a large ‘benthic’ species, which feeds on benthic invertebrates, and a smaller planktivorous ‘limnetic’ species. Breeding males of both species develop red throats and blue bodies, although limnetic males appear brighter. To test for character displacement, we compared the nuptial colour of benthics and limnetics from two species-pair lakes (sympatric) with that of males from three similar allopatric lakes (only one species present). We measured the intensity of blue and red coloration using reflectance spectra taken from live fish. We found that allopatric males were intermediate between limnetic and benthic males in the intensity of red colour, indicating character displacement in that trait in sympatry. By contrast, we found no evidence for character displacement in blue intensity, although it differed sharply between the species pairs in one lake (Priest). © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 37–48.

Female Choice by Scent Recognition in the Spotted Cucumber Beetle

AbstractIn species that demonstrate female choice, geographically distinct populations can vary in their signal‐response behaviors as a result of environmental differences or genetic drift. Observing whether or not females discriminate against males from allopatric populations can establish such signal deviations. Here we compare mating success within and between populations of the spotted cucumber beetle (Diabrotica undecimpunctata howardi) collected from Delaware, Tennessee, Missouri, and New Mexico, USA. A no‐choice cross‐mating experiment was employed to measure female preference for sympatric and allopatric males. While only two of the populations (Tennessee and Missouri) demonstrated statistically significant female preference for sympatric males, this trend was observed in all populations tested. Further, we show that (i) males from Tennessee, Missouri, and New Mexico differ in their scent, (ii) females may use population‐specific scents to discriminate among males, and (iii) females whose antennae have been surgically removed are unable to recognize acceptable mates. New Mexico males, which were never accepted by either Tennessee or Missouri females, became acceptable mates when crowded with Tennessee or Missouri males prior to copulation. We infer that male odor may be an important factor in determining cucumber beetle mating success.

REPRODUCTIVE CHARACTER DISPLACEMENT OF MALE STICKLEBACK MATE PREFERENCE: REINFORCEMENT OR DIRECT SELECTION?

Reproductive isolation can evolve between species as a byproduct of adaptation to different niches, through reinforcement, and by direct selection on mating preferences. We investigated the potential role of direct selection in the reproductive isolation between sympatric species of threespine sticklebacks. Each sympatric pair consists of a small-bodied limnetic species and large-bodied benthic species. We compared the mate preferences and courtship behavior of males from one sympatric limnetic population and two allopatric populations. We used limnetic-like allopatric populations to control for the effects of ecological character displacement and adaptation to different niches on mate preferences. The sympatric limnetic males preferred the small limnetic females, whereas the allopatric limnetic-like males preferred the large benthic females, suggesting that adaptation to the limnetic niche does not automatically confer a preference for small limnetic females. This reproductive character displacement of male preference is consistent with the predictions of both reinforcement and direct selection on mate preferences. To test for direct selection, we assessed a prediction of one proposed mechanism: predation by benthic females on eggs guarded by limnetic males. The allopatric males come from populations in which there is no egg predation. Sympatric limnetic males were more aggressive toward benthic females than toward limnetic females, whereas the allopatric limnetic-like males did not treat the two types of females differently. The contrast in male behavior suggests that egg predation has shaped male preferences. Direct selection is potentially more effective than indirect selection via reinforcement, and it is likely that it has been important in building up reproductive isolation between limnetic and benthic sticklebacks.

Functional incompatibility between the fertilization systems of two allopatric populations of Callosobruchus maculatus (Coleoptera: Bruchidae).

Recent studies indicate that postcopulatory sexual selection may represent an important component of the speciation process by initiating reproductive isolation via the evolutionary divergence of fertilization systems. Using two geographically isolated populations of the polyandrous beetle Callosobruchus maculatus, we investigated divergence in fertilization systems by determining the extent of postcopulatory functional incompatibility. Through reciprocal, cross-population matings we were able to separately estimate the effects of male and female population origin and their interaction on the extent of last-male sperm precedence, female receptivity to further copulation and female oviposition. Our results indicate partial incompatibility between the fertilization systems of the two populations at all three functional levels. Males derived from the same population as females outcompete rival, allopatric males with respect to sperm preemption, sperm protection, and ability to stimulate female oviposition. This pattern is reciprocated in both populations indicating that postcopulatory, prezygotic events represent important mechanisms by which between-population gene flow is reduced. We suggest the partial gametic isolation observed is a by-product of the coevolution of male and female fertilization systems by a process of cryptic female choice. Our results are consistent with a mechanism akin to conventional mate choice models although they do not allow us to reject antagonistic sexual coevolution as the mechanism of cryptic female choice.

Current reproductive isolation between ancestors of natural hybrids in Bacillus stick insects (Insecta: Phasmatodea)

Interspecific hybrids raise a variety of developmental, reproductive, and evolutionary issues. In Sicily, geographically and chronologically distinct hybridizations between the highly differentiated Bacillus rossius and B. grandii have produced hybridogenetic strains and clonal parthenogenetic species. In northern Sicily, all-female populations of facultatively Parthenogenetic B. rossius and bisexual B. grandii benazzii co-occur and we could test their current hybridization through electrophoretic marker analyses; control crosses with allopatric males were also carried out. Hybrid female progeny percentages ranged from 0 to 74 being fewer in egg batches laid by parthenogenetic mothers than in those of amphimictic females; no difference was noticed between sympatric and allopatric pairs. F1 hybrids of both sexes proved sterile; although some eggs started cleaving, no hemiclonal or clonal progeny hatched, only rare androgenetics being obtained. In currently produced hybrids a complete disruption of gametogenesis occurs, so that genetic constraints between parental taxa appear stronger now than in the past, most likely the result of ancestor evolution.

Incipient speciation in the flour beetle, Tribolium confusum: premating isolation between natural populations.

We report the existence of partial reproductive isolation between two natural populations of the flour beetle, Tribolium confusum, collected in Kaduna, Nigeria and Zagreb, Croatia. When a female from either population is paired with a single sympatric or allopatric male, she produces near normal numbers of semifertile offspring. However, when females are multiply mated with allopatric and sympatric males, the sympatric males sire the large majority of offspring. When measured in offspring numbers, the mean relative fitness of allopatric males is 0.425 with Nigerian females and 0.085 with Croatian females. Thus, the reproductive isolation is reciprocal but asymmetric. Behavioural observations indicate that only a fraction of mating attempts by allopatric males are successful because females do not become quiescent as often when mounted by allopatric males. The premating isolation is also reciprocal but asymmetric: Nigerian females are more accepting of allopatric males as mates than are Croatian females. The prezygotic behavioural isolation between these two populations is different from the postmating, prezygotic isolation observed between two other species in the genus, T. castaneum and T. freemani. Furthermore, the T. confusum interpopulation hybrids are fertile although they exhibit a weak female bias.

Species recognition in Darwin's finches ( Geospiza, Gould). II. Geographic variation in mate preference

The mate preferences of male Darwin's finches ( Geospiza) were compared in areas of sympatry and allopatry, using female models in choice tests. Males from sympatric populations showed significantly stronger sexual preferences for conspecific females than did allopatric males. At one sympatric site (Isla Pinta), we found enhanced preferences for conspecific females despite the absence of character displacement in cues important for visual recognition. Lack of preferential male courtship is correlated with hybridization with immigrants in one allopatric population, Daphne Major G. fortis. Tests at other allopatric sites showed that the ability to distinguish unfamiliar species from conspecifics by visual cues varies among populations, and generally is better-developed on islands having more congeners.