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.     

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.     

Reproductive interference between animal species

Although sexual interactions between species (reproductive interference) have been reported from a wide range of animal taxa, their potential for determining species coexistence is often disregarded. Here, we review evidence from laboratory and field studies illustrating that heterospecific sexual interactions are frequently associated with fitness loss and can have severe ecological and evolutionary consequences. We define reproductive interference as any kind of interspecific interaction during the process of mate acquisition that adversely affects the fitness of at least one of the species involved and that is caused by incomplete species recognition. We distinguish seven types of reproductive interference: signal jamming, heterospecific rivalry, misdirected courtship, heterospecific mating attempts, erroneous female choice, heterospecific mating, and hybridization. We then discuss the sex-specific costs of these types and highlight two typical features of reproductive interference: density-dependence and asymmetry. Similar to competition, reproductive interference can lead to displacement of one species (sexual exclusion), spatial, temporal, or habitat segregation, changes in life history parameters, and reproductive character displacement. In many cases, patterns of coexistence might be shaped by reproductive interference rather than by resource competition, as the presence of a few heterospecifics might substantially decrease reproductive success. Therefore, interspecific sexual interactions should receive more attention in ecological research. Reproductive interference has mainly been discussed in the context of invasive species or hybrid zones, whereas its influence on naturally-occurring sympatric species pairs has rarely been addressed. To improve our knowledge of the ecological significance of reproductive interference, findings from laboratory experiments should be validated in the field. Future studies should also focus on ecological mechanisms, such as temporal spatial, or habitat partitioning, that might enable sexually interacting species to coexist. Reproductive interference also has implications for the management of endangered species, which can be threatened by sexual interactions with invasive or common species. Studies of reproductive interference might even provide new insights for biological pest control.     

SEX DIFFERENCES IN MATE RECOGNITION AND CONSPECIFIC PREFERENCE IN SPECIES WITH MUTUAL MATE CHOICE

Sexual isolation is often assumed to arise because choosy females recognize and reject heterospecific males as mates. Yet in taxa in which both males and females are choosy, males might also recognize and reject heterospecific females. Here, we asked about the relative contribution of the sexes to the strong sexual isolation found in limnetic–benthic species pairs of threespine sticklebacks, which show mutual mate choice. We asked whether males and females of the two species recognize conspecifics and also prefer to mate with them. We found evidence for mate recognition by both sexes but only females prefer conspecifics. The nature of male courtship depended on which species of female they were courting, indicating that males recognized conspecific females and differentiated them from heterospecifics. However, males courted both species of females with equal vigor and changed courtship in a manner that would increase the chance of mating with heterospecifics. Females both recognized conspecifics and strongly preferred them. They responded very little to heterospecific male courtship and almost never mated with them. Therefore, males are likely to undermine sexual isolation, but females uphold it. Despite mutual mate choice and mate recognition in both sexes, females are primarily responsible for sexual isolation in these taxa.     

The complexity of mating decisions in stalk‐eyed flies

All too often, studies of sexual selection focus exclusively on the responses in one sex, on single traits, typically those that are exaggerated and strongly sexually dimorphic. They ignore a range of less obvious traits and behavior, in both sexes, involved in the interactions leading to mate choice. To remedy this imbalance, we analyze a textbook example of sexual selection in the stalk‐eyed fly (Diasemopsis meigenii). We studied several traits in a novel, insightful, and efficient experimental design, examining 2,400 male–female pairs in a “round‐robin” array, where each female was tested against multiple males and vice versa. In D. meigenii, females exhibit strong mate preference for males with highly exaggerated eyespan, and so we deliberately constrained variation in male eyespan to reveal the importance of other traits. Males performing more precopulatory behavior were more likely to attempt to mate with females and be accepted by them. However, behavior was not a necessary part of courtship, as it was absent from over almost half the interactions. Males with larger reproductive organs (testes and accessory glands) did not make more mating attempts, but there was a strong tendency for females to accept mating attempts from such males. How females detect differences in male reproductive organ size remains unclear. In addition, females with larger eyespan, an indicator of size and fecundity, attracted more mating attempts from males, but this trait did not alter female acceptance. Genetic variation among males had a strong influence on male mating attempts and female acceptance, both via the traits we studied and other unmeasured attributes. These findings demonstrate the importance of assaying multiple traits in males and females, rather than focusing solely on prominent and exaggerated sexually dimorphic traits. The approach allows a more complete understanding of the complex mating decisions made by both males and females.     

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

Does heterospecific seminal fluid reduce fecundity in interspecific copulation between seed beetles?

Reproductive interference through mating between related species can cause fitness reduction and affect population dynamics of the interacting species. In experimental matings between two seed beetles, Callosobruchus chinensis and Callosobruchus maculatus, C. maculatus females, but not C. chinensis females, suffer from significant loss of fecundity when conspecific mating is followed by heterospecific mating. We hypothesized that male traits associated with sexual conflict, which are often harmful to females, pleiotropically affect fitness of heterospecific females through interspecific mating. We examined the effect of ejaculate of C. chinensis males on C. maculatus females as the cause of the fecundity loss in C. maculatus females due to interspecific copulation. We found that frequent interspecific copulation occurred between C. maculatus females and C. chinensis males, but not between C. chinensis females and C. maculatus males, resulting in frequent interspecific ejaculate transfer from C. chinensis males to C. maculatus females. However, injection of the extract from C. chinensis male reproductive organs into C. maculatus females did not significantly affect C. maculatus fecundity compared with saline injection, indicating that the effect of the heterospecific ejaculate transfer on fecundity is negligible. We suggest that other harmful male traits such as genital spines of C. chinensis males are mainly responsible for the fecundity reduction in C. maculatus females that have experienced interspecific mating.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

Male and Female Soldier Beetles Relax Choice for Mate Quality Across Daily Courtship Periods

Mutual mate choice occurs when members of each sex will reject some potential mates in efforts to encounter better prospects later. The decision to reject may represent the interaction between mate preferences, mate availability, and temporal constraints. Theory predicts that mutual mate choice will favor relaxed choosiness as mate availability and time for courtship decline. We explored mutual mate choice in the soldier beetle, Chauliognathus pennsylvanicus (Cantharidae), where courtship consisted of males attempting to secure evasive females. We employed field observations, laboratory experiments, and stochastic simulations to investigate the decline in choosiness over the daily courtship period, during which individuals can mate at most once. We found that reproductive success of males and females increases with mate size and mating frequency. Females biased copulations toward larger mates by attempting to evade suitors, while males biased copulations by releasing the smaller females they capture. However, late in the day males and females may increase reproductive success by accepting rather than rejecting lower quality mates to maintain high mating rates. Stochastic simulations indicated that reproductive success, the product of mating frequency and mean mate size, was maximized in males and females by incrementally reducing mate standards across daily courtship periods. In the field, large males who rejected small females early in the daily courtship period rarely did so later. Large females used less effective evasive maneuvers later in the courtship period, resulting in copulations with progressively smaller males. These results support models of mutual mate choice that predict that individuals of high quality will maximize reproductive success by relaxing choosiness as the courtship period wanes.     

Beyond magic traits: Multimodal mating cues in Heliconius butterflies

Species coexistence involves the evolution of reproductive barriers opposing gene flow. Heliconius butterflies display colorful patterns affecting mate choice and survival through warning signaling and mimicry. These patterns are called “magic traits” for speciation because divergent natural selection may promote mimicry shifts in pattern whose role as mating cue facilitates reproductive isolation. By contrast, between comimetic species, natural selection promotes pattern convergence. We addressed whether visual convergence interferes with reproductive isolation by testing for sexual isolation between two closely related species with similar patterns, H. timareta thelxinoe and H. melpomene amaryllis. Experiments with models confirmed visual attraction based on wing phenotype, leading to indiscriminate approach. Nevertheless, mate choice experiments showed assortative mating. Monitoring male behavior toward live females revealed asymmetry in male preference, H. melpomene males courting both species equally while H. timareta males strongly preferred conspecifics. Experiments with hybrid males suggested an important genetic component for such asymmetry. Behavioral observations support a key role for short‐distance cues in determining male choice in H. timareta. Scents extracts from wings and genitalia revealed interspecific divergence in chemical signatures, and hybrid female scent composition was significantly associated with courtship intensity by H. timareta males, providing candidate chemical mating cues involved in sexual isolation.     

Reproductive interference, priority effects and the maintenance of parapatry in Skistodiaptomus copepods

Reproductive interactions among species, such as attempts to mate with heterospecifics, can have profound impacts on patterns of geographic range and co-occurrence. For example, several theoretical models demonstrate that reproductive interference-the negative influence of heterospecifics on the abilities of conspecifics to successfully mate-can lead to parapatry, even across homogeneous landscapes, when the parapatric species are initially allopatric. However, the potential consequences of reproductive interactions on patterns of range limits and co-occurrence have been largely ignored by ecologists. Here, I use a combination of laboratory mating experiments and a genetic survey for two parapatric species of Skistodiaptomus copepods to evaluate the potential importance of interspecific reproductive interactions on the maintenance of parapatry. The genetic survey demonstrates phylogenetic exclusivity of these species, suggesting that gene flow has not occurred between them. Moreover, laboratory crosses between both species demonstrate that their parapatric boundary is not maintained as a hybrid zone because the two species cannot form viable hybrids. However, Skistodiaptomus oregonensis and S. pygmaeus males mate indiscriminately and interfere with the ability of heterospecific females to successfully reproduce. I suggest that reproductive interference results in priority effects that strongly influence the maintenance of this parapatric boundary and stress that reproductive traits are important and often-overlooked in ecological models for species range limits.     

Direct mate choice for simultaneous acoustic and visual courtship displays in the damselfish, Dascyllus albisella (Pomacentridae)

Acoustic signals are well established as key components of mate selection in terrestrial species, but not in aquatic species. It has long been known that damselfish (Pomacentridae) use a combined visual and acoustic display in their courtship.. This study examined several male qualities including individual size, courtship vigor, territory size and complexity, as well as components of the acoustic call including dominant frequency, pulse characteristics and repetition rate. The objective was to determine which male traits were correlated with mating success. Observations made over ten reproductive cycles revealed that female mate choices were not random and that male mating success was correlated with courtship rate (a simultaneous visual and acoustic cue) and the number of neighboring females, but not with male morphological traits, territory quality, or acoustic call structure. These results suggest that females choose mates based on a condition-dependent trait (courtship rate) that advertises quality of paternal care, which supports good parent models of sexual selection, thereby demonstrating the importance of the combined acoustic/visual display for sexual selection in fishes     

The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation in vertebrates.     

Female mate recognition and sexual isolation depending on courtship song in Drosophila sechellia and its siblings

In Drosophila sechellia, females accept males that sing heterospecific songs less than those that do not sing, whereas in D. melanogaster and D. simulans, females accept males that sing heterospecific song more than those that do not sing. Here we studied the sexual isolation of D. sechellia and its siblings using interspecific hybrids to reveal the mechanisms underlying female mate recognition. The females of hybrids mated more with winged males of the parent species than with wingless ones, suggesting that the discrimination against heterospecific songs by D. sechellia females is recessive. Female preference for courtship songs seems to be inherited additively or semidominantly. In addition, we examined female receptivity without the stimuli of courtship songs by comparing the mating frequencies between the crosses using wingless males and found that it is also inherited additively or semidominantly.     

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the “gatekeepers” of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close‐range signals are as important as long‐distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.     

Mating system of the Amazonian cichlid angel fish, Pterophyllum scalare.

The species, Pterophyllum scalare distinguishes itself by its breeding behavior, involving competition for territory, sexual partners, courtship and parental care. The purpose of this study was to identify the mating system adopted by this species of fish. Twenty males and twenty females were observed under semi-natural and experimental conditions to test the hypothesis of serial monogamy. Under semi-natural conditions, after the third breeding cycle, the couples changed mates. Under experimental conditions, the couples changed partners after the first breeding cycle. Under experimental conditions, mate recognition was investigated through the preference of the females, indicated by the time they spent with the males. The females were available or not for courtship from new males, depending on their aggressiveness or submission. The larger and more aggressive males obtained new mating opportunities while the submissive males were rejected by the females. The mated fish were aggressive towards intruders in the presence of the mate, protecting their pair bond. In the interval between breeding cycles, the couples did not display aggression towards intruders, confirming the hypothesis of serial monogamy. Best mate selection by the females and the opportunity of new matings for both sexes influenced the reproductive success of this species.     

Reproductive interference explains persistence of aggression between species

Interspecific territoriality occurs when individuals of different species fight over space, and may arise spontaneously when populations of closely related territorial species first come into contact. But defence of space is costly, and unless the benefits of excluding heterospecifics exceed the costs, natural selection should favour divergence in competitor recognition until the species no longer interact aggressively. Ordinarily males of different species do not compete for mates, but when males cannot distinguish females of sympatric species, females may effectively become a shared resource. We model how reproductive interference caused by undiscriminating males can prevent interspecific divergence, or even cause convergence, in traits used to recognize competitors. We then test the model in a genus of visually orienting insects and show that, as predicted by the model, differences between species pairs in the level of reproductive interference, which is causally related to species differences in female coloration, are strongly predictive of the current level of interspecific aggression. Interspecific reproductive interference is very common and we discuss how it may account for the persistence of interspecific aggression in many taxonomic groups.     

Behavioral reproductive isolation inDrosophila silvestris,D. heteroneura,and their F1 hybrids (Diptera: Drosophilidae)

We investigated the role that courtship and aggressive interactions may have for the maintenance of reproductive isolation betweenDrosophila silvestris andD. heteroneura. We examined the behavioral bases of reproductive isolation between the parental species and we examined the courtship success of each sex of both reciprocal F₁ hybrids when paired with the parental species. We found reduced copulation success among heterotypic parental pairs compared to homotypic pairs, which was primarily due to the lack of courtship initiation betweenD. silvestris males andD. heteroneura females. When hybrid males from both reciprocal crosses were paired with parental females their copulation successes were not significantly different from that of parental males. In contrast, hybrid females from both crosses had reduced copulation success withD. silvestris males, which in turn was primarily due to a reduced success of reaching later stages of courtship. The time spent in copulation by hybrid males was intermediate between the two parental males. We studied aggression by observing the interactions of males of heterotypic pairs, both between the parental species and between the hybrids and parental males. A lack of aggressive interactions betweenD. silvestris males andD. heteroneura males in addition to the lack of courtship suggests thatD. silvestris males do not respond toD. heteroneura individuals of either sex. Hybrid males were equally successful in winning fights with bothD. silvestris andD. heteroneura males. These results indicate that the behavioral isolation betweenD. silvestris andD. heteroneura may be largely a consequence of the earliest stages of interactions. The two species may differ either in activity levels or in morphological or chemical traits that are important for species and mate recognition. The relatively high copulation and aggressive success of hybrids indicates that sexual selection against hybrids alone is unlikely to be a sufficient force to reduce gene flow and maintain species distinctions.     

Genetics of incipient speciation in Drosophila mojavensis. I. Male courtship song, mating success, and genotype x environment interactions

Few studies have examined genotype by environment (GxE) effects on premating reproductive isolation and associated behaviors, even though such effects may be common when speciation is driven by adaptation to different environments. In this study, mating success and courtship song differences among diverging populations of Drosophila mojavensis were investigated in a two-environment quantitative trait locus (QTL) analysis. Baja California and mainland Mexico populations of D. mojavensis feed and breed on different host cacti, so these host plants were used to culture F2 males to examine host-specific QTL effects and GxE interactions influencing mating success and courtship songs. Linear selection gradient analysis showed that mainland females mated with males that produced songs with significantly shorter L(long)-IPIs, burst durations, and interburst intervals. Twenty-one microsatellite loci distributed across all five major chromosomes were used to localize effects of mating success, time to copulation, and courtship song components. Male courtship success was influenced by a single detected QTL, the main effect of cactus, and four GxE interactions, whereas time to copulation was influenced by three different QTLs on the fourth chromosome. Multiple-locus restricted maximum likelihood (REML) analysis of courtship song revealed consistent effects linked with the same fourth chromosome markers that influenced time to copulation, a number of GxE interactions, and few possible cases of epistasis. GxE interactions for mate choice and song can maintain genetic variation in populations, but alter outcomes of sexual selection and isolation, so signal evolution and reproductive isolation may be slowed in diverging populations. Understanding the genetics of incipient speciation in D. mojavensis clearly depends on cactus-specific expression of traits associated with courtship behavior and sexual isolation.     

Does sexual experience affect the strength of male mate choice for high‐quality females in Drosophila melanogaster?

Although females are traditionally thought of as the choosy sex, there is increasing evidence in many species that males will preferentially court or mate with certain females over others when given a choice. In the fruit fly, Drosophila melanogaster, males discriminate between potential mating partners based on a number of female traits, including species, mating history, age, and condition. Interestingly, many of these male preferences are affected by the male''s previous sexual experiences, such that males increase courtship toward types of females that they have previously mated with and decrease courtship toward types of females that have previously rejected them. D. melanogaster males also show courtship and mating preferences for larger females over smaller females, likely because larger females have higher fecundity. It is unknown, however, whether this preference shows behavioral plasticity based on the male''s sexual history as we see for other male preferences. Here, we manipulate the sexual experience of D. melanogaster males and test whether this manipulation has any effect on the strength of male mate choice for large females. We find that sexually inexperienced males have a robust courtship preference for large females that is unaffected by previous experience mating with, or being rejected by, females of differing sizes. Given that female body size is one of the most common targets of male mate choice across insect species, our experiments with D. melanogaster may provide insight into how these preferences develop and evolve.