Conflicting intersexual mate choices maintain interspecific sexual interactions

Reproductive interference, interspecific sexual interactions that affect reproductive success, is found in various taxa and has been considered as a fundamental source of reproductive character displacement (RCD). Once RCD has occurred, persistent interspecific sexual interactions between species pairs are expected to diminish. However, reproductive interference has been reported from some species pairs that sympatrically coexist. Thus, the question arises, can reproductive interference persist even after RCD? We modeled the evolutionary dynamics of signal traits and mate recognition that determine whether interspecific sexual interactions occur. Our models incorporate male decision making based on the recognition of signal traits, whereas most previous models incorporate only female decision making in mate selection. Our models predict the following: (1) even when male decision making is incorporated, males remain promiscuous; (2) nevertheless, the frequency of interspecific mating is maintained at a low level after trait divergence; (3) the rarity of interspecific mating is due to strict female mate recognition and the consequent refusal of interspecific courtship by females; and (4) the frequency of interspecific mating becomes higher as the cost to females of refusing interspecific courtship increases. These predictions are consistent with empirical observations that males of some species engage in infrequent heterospecific mating. Thus, our models predict that reproductive interference can persist even after RCD occurred.     

The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement

Sympatric divergence in traits affecting species recognition can result from selection against cross‐species mating (reproductive character displacement, RCD) or interspecific aggression (agonistic character displacement, ACD). When the same traits are used for species recognition in both contexts, empirically disentangling the relative contributions of RCD and ACD to observed character shifts may be impossible. Here, we develop a theoretical framework for partitioning the effects of these processes. We show that when both mate and competitor recognition depend on the same trait, RCD sets the pace of character shifts. Moreover, RCD can cause divergence in competitor recognition, but ACD cannot cause divergence in mate recognition. This asymmetry arises because males with divergent recognition traits may avoid needless interspecific conflicts, but suffer reduced attractiveness to conspecific females. Therefore, the key empirical issue is whether the same or different traits are used for mate recognition and competitor recognition.     

Does character displacement demonstrate density-dependent expression in females? A test on the wing shape of two species of European damselflies

Character displacement (CD) is the evolutionary process which leads to the divergence in trait expression of closely related species in regions where species co-occur, compared to allopatric populations. In Europe CD has been investigated in males of Calopteryx splendens and C. virgo and has been related to species recognition. If species recognition is relevant for males, also females should benefit from CD. The most obvious differences between females of these two species are wing profile and colour. We sampled females from allopatric and from sympatric populations with different relative abundances of these species. Wing shape and pigmentation were evaluated for each damselfly. CD was found in wing profile but not in wing transparency. The relative abundance of species significantly affected CD, but with a different pattern in each species. The prediction that wing shape become more different from the allopatric state when the species was relatively rare, but more similar to the allopatric state when the species was common was evident only for C. splendens. Wing shape changes might increase differences in flying patterns making males more effective to discriminate between heterospecific females. So, CD we observed may be the result of a selection directed to reduce interspecific reproductive interference.     

Interspecific aggression causes negative selection on sexual characters

Interspecific aggression originating from mistaken species recognition may cause selection on secondary sexual characters, but this hypothesis has remained untested. Here we report a field experiment designed to test directly whether interspecific aggression causes selection on secondary sexual characters, wing spots, in wild damselfly populations. Males of Calopteryx virgo are more aggressive toward males of C. splendens with large than with small wing spots. This differential interspecific aggression may cause negative selection on wing spot size. Indeed, our results show that directional survival selection on wing spot size of C. splendens males was changed by experimental removal of C. virgo males. Without removal, directional selection went from positive to negative with increasing relative abundance of C. virgo males. In populations where C. virgo males were removed, this relationship disappeared. These results verify that interspecific aggression can cause negative selection on sexual characters. Thus, interspecific aggression has the potential to cause divergence on these characters between two species offering an alternative explanation for reinforcement for generating character displacement in secondary sexual characters.     

The presence of heterospecific males causes an Allee effect

The Allee effect is a positive causal relationship between any component of fitness and population density or size. Allee effects strongly affect the persistence of small or sparse populations. Predicting Allee effects remains a challenge, possibly because not all causal mechanisms are known. We hypothesized that reproductive interference (an interspecific reproductive interaction that reduces the fitness of the species involved) can generate an Allee effect. If the density of the interfering species is constant, an increase in the population of the species receiving interference may dilute the per capita effect of reproductive interference and may generate an Allee effect. To test this hypothesis, we examined the effect of heterospecific males on the relationship between per capita fecundity and conspecific density in Callosobruchus chinensis and C. maculatus. Of the two species, only C. maculatus females suffer reproductive interference from heterospecific males. Only C. maculatus, the species susceptible to reproductive interference, demonstrated an Allee effect, and only when heterospecific males were present. In contrast, C. chinensis, the species not susceptible to reproductive interference, demonstrated no Allee effect regardless of the presence of heterospecific males. Our results show that reproductive interference in fact generated an Allee effect, suggesting the potential importance of interspecific sexual interactions especially in small or sparse populations, even in the absence of a shared resource. It may be possible to predict Allee effects produced by this mechanism a priori by testing reproductive interference between closely related species.     

Interactions of the Males and Females of Three Sympatric Drosophila virilis-Group Species, D. montana, D. littoralis, and D. lummei, (Diptera: Drosophilidae) in Intra- and Interspecific Courtships in the Wild and in the Laboratory

Four species of the Drosophila virilis group, D. montana, D. littoralis, D. lummei, and D. ezoana, occur sympatrically in several locations in northern Europe. Courtship interactions between the flies of the three first-mentioned species were observed at malt baits in Kemi, northern Finland, to find out how the flies of different species recognize conspecific individuals and how interspecific courtships differ from intraspecific ones in the wild. Intraspecific courtships (including females of different reproductive stages) and interspecific courtships were also videotaped and analyzed in laboratory. In the wild the males courted both conspecific and allospecific females, even though the species varied in how much the males were attracted to females of different species. Interspecific courtships usually broke off when the male touched the female or when the male and/or the female vibrated his/her wings, producing acoustic cues. In the laboratory males courted conspecific females irrespective of the reproductive stage of the female, even though the courtships directed toward immature and fertilized females usually included only orienting and touching (no licking and singing). D. littoralis, and very rarely D. montana and D. lummei, males courted also allospecific females. In the few interspecific courtships between these three species, where the male proceeded to singing, females responded to male singing by vibrating their wings. This ended the courtship. It is suggested that both the chemical cues affecting female attractivity and the acoustic signals of males and females, which are produced by wing vibration, function in maintaining sexual isolation between these three species.     

Satyrization without evidence of successful insemination from interspecific mating between invasive mosquitoes

Previous research has documented low frequencies of interspecific mating in nature between the invasive vectors Aedes aegypti and Aedes albopictus. It is also known that heterospecific male accessory gland substances transferred during mating sterilize A. aegypti but not A. albopictus females, leading to satyrization, a form of reproductive interference. This paper demonstrates that satyrization of A. aegypti by A. albopictus may occur without evidence of successful insemination. Our results show that A. aegypti females, previously exposed to A. albopictus males, are rendered refractory to subsequent conspecific mating even though their spermathecae contain no heterospecific sperm. Additional experiments demonstrating transfer of labelled semen from A. albopictus males to A. aegypti females and low production of viable eggs of females housed with conspecific males, following exposure to A. albopictus males, confirm higher incidences of satyrization than expected, based on heterospecific insemination rates. We conclude that frequencies of satyrization based on detection of interspecific sperm in spermathecae may underestimate the impact of this form of reproductive interference.     

Reproductive interference hampers species coexistence despite conspecific sperm precedence

Negative interspecific mating interactions, known as reproductive interference, can hamper species coexistence in a local patch and promote niche partitioning or geographical segregation of closely related species. Conspecific sperm precedence (CSP), which occurs when females that have mated with both conspecific and heterospecific males preferentially use conspecific sperm for fertilization, might contribute to species coexistence by mitigating the costs of interspecific mating and hybridization. We discussed whether two species exhibiting CSP can coexist in a local environment in the presence of reproductive interference. First, using a behaviorally explicit mathematical model, we demonstrated that two species characterized by negative mating interactions are unlikely to coexist because the costs of reproductive interference, such as loss of mating opportunity with conspecific partners, are inevitably incurred when individuals of both species are present. Second, we experimentally examined differences in mating activity and preference in two Harmonia ladybird species known to exhibit CSP. These behavioral differences may lead to local extinction of H. yedoensis because of reproductive interference by H. axyridis. This prediction is consistent with field observations that H. axyridis uses various food sources and habitats whereas H. yedoensis is confined to a less preferred prey item and a pine tree habitat. Finally, by a comparative approach, we observed that niche partitioning or parapatric distribution, but not sympatric coexistence in the same habitat, is maintained between species with CSP belonging to a wide range of taxa, including vertebrates and invertebrates living in aquatic or terrestrial environments. Taken together, it is possible that reproductive interference may destabilize local coexistence even in closely related species that exhibit CSP.     

Maintenance of genetic and morphological identity in two sibling Syrrhopodon species (Calymperaceae,Bryopsida) despite extensive introgression

Bryophytes are a group of land plants in which the role of hybridization has long been challenged. Using genotyping by sequencing to circumvent the lack of molecular variation at selected loci previously used for phylogeny and morphology, we determine the level of genetic and morphological divergence and reproductive isolation between the sibling Syrrhopodon annotinus and S. simmondsii (Calymperaceae, Bryopsida) that occur in sympatry but in different habitats in lowland Amazonian rainforests. A clear morphological differentiation and a low (0.06), but significant Fst derived from the analysis of 183 single nucleotide polymorphisms were observed between the two species. Conspecific pairs of individuals consistently exhibited higher average kinship coefficients along a gradient of geographic isolation than interspecific pairs. The weak, but significant genetic divergence observed is consistent with growing evidence that ecological specialization can lead to genetic differentiation among bryophyte species. Nevertheless, the spatial genetic structures of the two species were significantly correlated, as evidenced by the significant slope of the Mantel test based on kinship coefficients between pairs of interspecific individuals and the geographic distance separating them. Interspecific pairs of individuals are thus more closely related when they are geographically closer, suggesting that isolation‐by‐distance is stronger than the interspecific reproductive barrier and pointing to interspecific gene flow. We conclude that interspecific introgression, whose role has long been questioned in bryophytes, may take place even in species wherein sporophyte production is scarce due to dioicy, raising the question as to what mechanisms maintain differentiation despite weak reproductive isolation.     

Reproductive interference by male Drosophila subobscura on female D. persimilis: A laboratory experiment

While females often reject courtship attempts by heterospecific males, reproductive interference by harassment from such males can nonetheless occur, potentially reducing female fitness. Such effects may be profound following a range expansion, when males from a new species may suddenly encounter (and perhaps even become abundant relative to) females of related native species. Drosophila subobscura recently invaded North America and may impact native species through reproductive interference and other processes. We test for the potential for reproductive interference by D. subobscura males on D. persimilis females in the laboratory. D. subobscura males aggressively copulated with D. persimilis females, including many females that exhibit rejection behaviors. Despite females attempting to dismount the males, the heterospecific copulations are on average longer than conspecific copulations, and females exhibit some reluctance to remate with conspecific males following this harassment. Females confined with both conspecific and heterospecific males produce fewer adult progeny than those with either conspecific males only or with conspecific males and distantly related D. simulans males that do not engage in female harassment. Overall, our results illustrate how reproductive interference by an invasive species can have negative effects on resident natural populations.     

Interspecific aggression,not interspecific mating,drives character displacement in the wing coloration of male rubyspot damselflies (Hetaerina)

Traits that mediate intraspecific social interactions may overlap in closely related sympatric species, resulting in costly between-species interactions. Such interactions have principally interested investigators studying the evolution of reproductive isolation via reproductive character displacement (RCD) or reinforcement, yet in addition to reproductive interference, interspecific trait overlap can lead to costly between-species aggression. Previous research on rubyspot damselflies (Hetaerina spp.) demonstrated that sympatric shifts in male wing colour patterns and competitor recognition reduce interspecific aggression, supporting the hypothesis that agonistic character displacement (ACD) drove trait shifts. However, a recent theoretical model shows that RCD overshadows ACD if the same male trait is used for both female mate recognition and male competitor recognition. To determine whether female mate recognition is based on male wing coloration in Hetaerina, we conducted a phenotype manipulation experiment. Compared to control males, male H. americana with wings manipulated to resemble a sympatric congener (H. titia) suffered no reduction in mating success. Thus, female mate recognition is not based on species differences in male wing coloration. Experimental males did, however, experience higher interspecific fighting rates and reduced survival compared to controls. These results greatly strengthen the case for ACD and highlight the mechanistic distinction between ACD and RCD.     

Asymmetric reproductive isolation between two sympatric annual killifish with extremely short lifespans

Background

Interspecific reproductive isolation is typically achieved by a combination of intrinsic and extrinsic barriers. Behavioural isolating barriers between sympatric, closely related species are often of primary importance and frequently aided by extrinsic factors causing spatial and temporal interspecific separation. Study systems with a severely limited role of extrinsic factors on reproductive isolation may provide valuable insights into how reproductive isolation between sympatric species is maintained. We used no-choice experimental set-up to study reproductive barriers between two closely related sympatric African killifish species, Nothobranchius furzeri and Nothobranchius orthonotus. These fish live in small temporary savannah pools and have complete spatial and temporal overlap in reproductive activities and share a similar ecology.

Principal Findings

We found that the two species display largely incomplete and asymmetric reproductive isolation. Mating between N. furzeri males and N. orthonotus females was absent under standard experimental conditions and eggs were not viable when fish were forced to mate in a modified experimental setup. In contrast, male N. orthonotus indiscriminately mated with N. furzeri females, the eggs were viable, and offspring successfully hatched. Most spawnings, however, were achieved by male coercion and egg production and embryo survival were low. Behavioural asymmetry was likely facilitated by mating coercion from larger males of N. orthonotus and at relatively low cost to females. Interestingly, the direction of asymmetry was positively associated with asymmetry in post-mating reproductive barriers.

Significance

We showed that, in fish species with a promiscuous mating system and multiple matings each day, selection for strong mate preferences was relaxed. This effect was likely due to the small proportion of resources allocated to each single mating and the high potential cost to females from mating refusal. We highlight and discuss the fact that males of rarer species may often coercively mate with females of a related, more abundant species.     

Interspecific Competition and Speciation in Endoparasitoids

Ecological speciation occurs when inherent reproductive barriers to gene flow evolve between populations as a result of divergent natural selection. Frequency dependent effects associated with intraspecific resource competition are thought to be one important source of divergent selection facilitating ecological speciation. Interspecific competition may also play an important role in promoting population divergence. Although evidence for interspecific competition in nature is ubiquitous, there is currently little empirical data supporting its role in the speciation process. Here, we discuss two general models in which interspecific competition among species can promote ecological speciation among populations within a species. In both models, interspecific competition is the source of divergent selection driving adaption to different portions of the resource distribution, generating ecological reproductive isolation from other conspecific populations. We propose that the biology of endoparasitoids that attack phytophagous insects make model systems for studying the role of interspecific competition in ecological speciation. We describe details for one such system, the community of endoparasitic braconid wasps attacking Rhagoletis fruit flies, as a potential model for investigating competitive speciation. We conclude by hypothesizing that a model in which interspecific competition forces an inferior competitor to alternative fly hosts may be a common theme contributing to parasitoid diversification in the Rhagoletis-parasitoid system.     

Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards

Interspecific competition can occur when species are unable to distinguish between conspecific and heterospecific mates or competitors when they occur in sympatry. Selection in response to interspecific competition can lead to shifts in signalling traits—a process called agonistic character displacement. In two fan-throated lizard species—Sitana laticeps and Sarada darwini—females are morphologically indistinguishable and male agonistic signalling behaviour is similar. Consequently, in areas where these species overlap, males engage in interspecific aggressive interactions. To test whether interspecific male aggression between Si. laticeps and Sa. darwini results in agonistic character displacement, we quantified species recognition and signalling behaviour using staged encounter assays with both conspecifics and heterospecifics across sympatric and allopatric populations of both species. We found an asymmetric pattern, wherein males of Si. laticeps but not Sa. darwini showed differences in competitor recognition and agonistic signalling traits (morphology and behaviour) in sympatry compared with allopatry. This asymmetric shift in traits is probably due to differences in competitive abilities between species and can minimize competitive interactions in zones of sympatry. Overall, our results support agonistic character displacement, and highlight the role of asymmetric interspecific competition in driving shifts in social signals.     

The number of subordinates moderates intrasexual competition among males in cooperatively breeding meerkats

For dominant individuals in cooperatively breeding species, the presence of subordinates is associated with both benefits (i.e. increased reproductive output and other group-living benefits) and costs (i.e. intrasexual competition on reproduction). The biological market theory predicts that dominant individuals are tolerant to same-sex group members when there are only a few subordinates, so as to maximize their own reproductive success. We investigated factors affecting aggression by dominant males and submission by subordinate males for a cooperatively breeding mammal, meerkats, Suricata suricatta. In this species, reproductive conflict occurs between the dominant male and the non-offspring males. As predicted, the number of subordinates in a group was positively associated with the aggression frequency by the dominant male and with the submission frequency by the subordinate males. Relative to the aggression frequency against male offspring, the frequency of aggression against non-offspring males was comparable in small groups, but was higher in large groups. These results indicate that reproductive conflict is present between the dominant male and the non-offspring males but is moderated in groups with small numbers of subordinates. This study provides an empirical data agreeing with the biological market theory in the context of intrasexual competition in cooperatively breeding species.     

Interspecific aggression and character displacement in the damselfly Calopteryx splendens

Problems in species recognition are thought to affect the evolution of secondary sexual characters mainly through avoidance of maladaptive hybridization. Another, but much less studied avenue for the evolution of sexual characters due to species recognition problems is through interspecific aggression. In the damselfly, Calopteryx splendens, males have pigmented wing spots as a sexual character. Large-spotted males resemble males of another species, Calopteryx virgo, causing potential problems in species recognition. In this study, we investigate whether there is character displacement in wing spot size and whether interspecific aggression could cause this pattern. We found first that wing spot size of C. splendens in populations decreased with increasing relative abundance of C. virgo. Secondly, C. virgo males were more aggressive towards large- than small-spotted C. splendens males. Thirdly, in interspecific contests C. virgo males had better territory holding ability than C. splendens males. These results suggest that interspecific aggression may have caused character displacement in wing spot size of C. splendens, because the intensity of aggression towards large-spotted males is likely to increase with relative abundance of C. virgo males. Thus, interspecific aggression may be an evolutionarily significant force that is able to cause divergence in secondary sexual characters.     

The mechanism of the fecundity reduction in Callosobruchus maculatus caused by Callosobruchus chinensis males

Male promiscuity sometimes results in interspecific reproductive interaction, also known as reproductive interference. Reproductive interference entails costs for the individuals involved and affects the community structure by reducing the population growth rate. However, our understanding of the mechanisms generating reproductive interference is still insufficient. Two congeneric bean weevils, Callosobruchus chinensis and C. maculatus, show asymmetric reproductive interference; only C. chinensis males reduce the fecundity of the other species. Here we investigated the mechanism of reproductive interference by C. chinensis males on C. maculatus females in terms of lifetime fecundity. Callosobruchus chinensis males with ablated genitals, which could harass C. maculatus females but not copulate with them, did not reduce the C. maculatus fecundity, suggesting that interspecific copulation was necessary. However, a single interspecific copulation did not affect C. maculatus fecundity as long as the females also copulated with a conspecific male. Exposure to C. chinensis males for 24 h prior to oviposition significantly reduced C. maculatus fecundity, and fecundity was negatively correlated with the number of C. chinensis males the females were exposed to. Additionally, C. maculatus females experienced more interspecific copulations when they were housed with more C. chinensis males. Together these findings suggest that multiple interspecific copulations by C. chinensis males reduce the fecundity of C. maculatus females. Thus in general, even if a single interspecific copulation is apparently harmless, repeated interspecific copulations can be costly for the individuals involved. Furthermore, only by quantifying reproductive success were we able to identify the precise mechanism of reproductive interference.     

Sex differences in hormonal responses to social conflict in the monogamous California mouse

Monogamous species are usually considered to be less likely to exhibit sex differences in behavior or brain structure. Most previous studies examining sex differences in stress hormone responses have used relatively sexually dimorphic species such as rats. We examined the stress hormone responses of monogamous California mice (Peromyscus californicus) to resident-intruder tests. We also tested males and females under different photoperiods, because photoperiod has been shown to affect both aggression and stress hormone responses. Females, but not males showed a significant increase in corticosterone levels immediately following a resident-intruder test. Males but not females showed elevated corticosterone levels under short days. Females tested in aggression tests also showed a significant increase in plasma oxytocin levels, but only when housed in long days. This was consistent with our observation that females but not males had more oxytocin positive cells in the paraventricular nucleus (PVN) when housed under long days. Our data show that sex differences in glucocorticoid responses identified in other rodents are present in a monogamous species.     

Male cleaner wrasses adjust punishment of female partners according to the stakes

Punishment is an important deterrent against cheating in cooperative interactions. In humans, the severity of cheating affects the strength of punishment which, in turn, affects the punished individual's future behaviour. Here, we show such flexible adjustments for the first time in a non-human species, the cleaner wrasse (Labroides dimidiatus), where males are known to punish female partners. We exposed pairs of cleaners to a model client offering two types of food, preferred 'prawn' items and less-preferred 'flake' items. Analogous to interactions with real clients, eating a preferred prawn item ('cheating') led to model client removal. We varied the extent to which female cheating caused pay-off reduction to the male and measured the corresponding severity of male punishment. Males punished females more severely when females cheated during interactions with high value, rather than low value, model clients; and when females were similar in size to the male. This pattern may arise because, in this protogynous hermaphrodite, cheating by similar-sized females may reduce size differences to the extent that females change sex and become reproductive competitors. In response to more severe punishment from males, females behaved more cooperatively. Our results show that punishment can be adjusted to circumstances and that such subtleties can have an important bearing on the outcome of cooperative interactions.     

Inhibition of female mating receptivity by male-derived extracts in two Callosobruchus species: Consequences for interspecific mating

We investigated the effects of injecting male-derived extracts on congeneric female receptivity in two species of Callosobruchus beetle, C. chinensis and C. maculatus. We also examined the influence of interspecific mating on female remating behaviour in these two species. Male-derived extracts reduced congeneric female receptivity in both species. As quick-acting components, extracts of C. chinensis male seminal vesicles reduced the receptivity of C. maculatus females, whereas extracts of C. maculatus male testes reduced the receptivity of C. chinensis females. As slow-acting components, extracts of male accessory glands of other species reduced the receptivity of both C. maculatus and chinensis females. After interspecific mating, the sperm of C. maculatus males were transferred to the reproductive organs of C. chinensis females, thereby reducing their receptivity. In contrast, no C. chinensis sperm were transferred to the reproductive organs of C. maculatus females; accordingly, the latter's receptivity was not reduced. Furthermore, the survival rate of C. chinensis females decreased markedly after interspecific mating. These results raise the possibility that under circumstances where populations of these two species share the same habitat, reproductive interference would occur only in the interactions between C. maculatus males and C. chinensis females.