Male mate preference for large size overrides species recognition in allopatric flat lizards (<Emphasis Type="Italic"> Platysaurus broadleyi</Emphasis>)

Species recognition and mate preference both influence mate choice but can be in conflict with each other. In such cases the relative importance of the two functions depends on the costs of mating with heterospecifics and the frequency of such interactions. We tested whether male flat lizards (Platysaurus broadleyi) are able to discriminate between conspecific females and females of its allopatric sister species P. capensis. Given a simultaneous choice between equally sized females of both species, males courted conspecific females in 85% of trials. We then tested whether mate preference for large female body size can override species recognition. When offered a choice between a larger heterospecific female and a smaller conspecific, males showed no preference for conspecifics and courted larger heterospecific females in 58% of trials. Comparison of the two sets of trials showed a significant effect of female body size on male mate preference, supporting the hypothesis that mate quality can override species recognition.Communicated by K. Kotrschal     

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

The presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.     

Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues

Females increase their risk of mating with heterospecifics whenthey prefer the traits of conspecifics that overlap with traitsfound in heterospecifics. Xiphophorus pygmaeus females havea strong preference for larger males, which could lead to femalespreferring to mate with heterospecific males; almost all sympatricX. cortezi males are larger than X. pygmaeus males. In thisstudy, we show that X. pygmaeus females preferred the chemicalcues from conspecifics over those of X. cortezi males. However,preference for the chemical cues of conspecifics could not reversethe preference for larger heterospecific males. Only when femaleswere presented with two species-specific cues (vertical barsand chemical cues) did more females spend more time on averagewith the smaller conspecific males. These results support the"backup signal" hypothesis for the evolution of multiple preferences;together, the two species-specific cues increased the accuracywith which females were able to avoid heterospecific males.In addition, the results suggest that in those situations inwhich the traits of conspecifics overlap with traits found inheterospecifics, females can use the assessment of multiplecues to avoid mating with heterospecifics without compromisingtheir preference for the highest-quality conspecific.     

Males,but not females,contribute to sexual isolation between two sympatric species of <Emphasis Type="Italic">Gambusia</Emphasis>

Reproductive isolation restricts genetic exchange between species. Various pre- and post-mating barriers, such as behavior, physiology and gametic incompatibility, have been shown to evolve in sympatry. In certain scenarios, isolation can be asymmetrical, where species differentially prefer conspecifics. We examined sexual isolation via conspecific mate preference between Gambusia affinis and G. geiseri in both sexes. To investigate male contribution to sexual isolation, we compared the number of mating attempts (gonopodial thrusts) directed at either a conspecific or a heterospecific female, in both species. We also examined sperm priming and expenditure in males in the presence of conspecific or heterospecific females. We then measured female preference for either a conspecific or heterospecific male, in both species. We found that males of both species preferred to mate with conspecific females, but showed no difference in sperm production or expenditure between conspecific and heterospecific females. Females of both species did not prefer conspecific over heterospecific males. Our results suggest that sexual isolation might be mediated by male mate choice in this system and not female choice, suggesting that there is asymmetrical reproductive isolation between the sexes in G. affinis and G. geiseri, but symmetrical species isolation.     

Sequential mate choice and sexual isolation in threespine stickleback species

Sequential mate choice strategies predict how females should alter their choosiness based on the availability of attractive males. There are many studies on sequential mate choice within species, but few have asked whether females apply these strategies to interactions between species and how these strategies may affect hybridization. We tested how previous interactions with conspecific and heterospecific males affect mate preference and sexual isolation in two threespine stickleback species (benthics and limnetics: Gasterosteus spp.). Consistent with previous work, we found that within species, stickleback females gauge male attractiveness relative to previously encountered males. If females extend these decision rules between species, we predicted that previous interactions with conspecifics should make heterospecifics less attractive, whereas interactions with heterospecifics should make conspecifics more attractive. However, females found heterospecifics less attractive after prior experience, largely independent of the species of male first encountered. Thus, sequential mate choice strategies are used within but not between species in sticklebacks. Further, learning from prior courtship interactions acts to enhance existing sexual isolation between species.     

Species recognition by male swordtails via chemical cues

Species recognition can often play a key role in female matingpreferences. Far less is known about conspecific mate recognitionfrom the male perspective. In many closely related taxa, femalesexhibit few obvious visual differences and males might haveto attend to chemical cues in mate recognition, a possibilitythat has rarely been explored in vertebrates. Here, we examinemale species recognition via odor cues in the swordtail fish,Xiphophorus birchmanni. In dichotomous choice experiments wefirst tested whether males respond to female odor cues. We foundthat males were attracted to conspecific female odor and thoseof a related allopatric congener, Xiphophorus malinche, overa water control. Males did not, however, respond to the femaleodor of the more distantly related sympatric platyfish, Xiphophorusvariatus. We then gave male X. birchmanni the choice betweenconspecific and heterospecific female stimuli. Males, in thisscenario, significantly preferred the conspecific odor whenthe alternative was platyfish. However, when offered odor cuesof X. malinche, male X. birchmanni actually preferred the heterospecificfemale cue. The complex array of preferences reported here,previously documented only in females, underscores the needto consider the behavior of both sexes in dictating actual matingoutcomes.     

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.     

Predator experience overrides learned aversion to heterospecifics in stickleback species pairs

Predation risk can alter female mating decisions because the costs of mate searching and selecting attractive mates increase when predators are present. In response to predators, females have been found to plastically adjust mate preference within species, but little is known about how predators alter sexual isolation and hybridization among species. We tested the effects of predator exposure on sexual isolation between benthic and limnetic threespine sticklebacks (Gasterosteus spp.). Female discrimination against heterospecific mates was measured before and after females experienced a simulated attack by a trout predator or a control exposure to a harmless object. In the absence of predators, females showed increased aversion to heterospecifics over time. We found that predator exposure made females less discriminating and precluded this learned aversion to heterospecifics. Benthic and limnetic males differ in coloration, and predator exposure also affected sexual isolation by weakening female preferences for colourful males. Predator effects on sexual selection were also tested but predators had few effects on female choosiness among conspecific mates. Our results suggest that predation risk may disrupt the cognitive processes associated with mate choice and lead to fluctuations in the strength of sexual isolation between species.     

Cross-fostering Does Not Influence the Mate Preferences and Territorial Behaviour of Males in Lake Victoria Cichlids

The ability to recognise conspecifics in contexts of mate choice and territorial defence may have large effects on an individual's fitness. Understanding the development of assortative behaviour may shed light on how species assortative behaviour evolves and how it may influence reproductive isolation. This is the case not only for female mate preferences, but also for male mate preferences and male territorial behaviour. Here we test with a cross-fostering experiment whether early learning influences male mate preferences and male–male aggression biases in two closely related, sympatrically occurring cichlid species Pundamilia pundamilia and Pundamilia nyererei from Lake Victoria. Males that had been fostered, either by a conspecific female or by a heterospecific female, were tested for their aggression bias, as well as for their mate preferences, in two-way choice tests. Males cross-fostered with conspecific and heterospecific foster mothers selectively directed their aggression towards conspecific intruders. The cross-fostering treatment also did not affect male mate preferences. These results are in striking contrast with the finding that females of these species show a sexual preference for males of the foster species.     

Degree of male ornamentation affects female preference for conspecific versus heterospecific males.

Several studies have shown female preference for conspecific males with the attached artificial ornaments of more elaborate heterospecifics. However, preference for heterospecifics under natural conditions is relatively rare. We tested what factors affect behavioural mechanisms of species isolation using three species of estrildid finch (genus Uraeginthus) that occur in both sympatry and allopatry. These finches differ in degree of sexual dimorphism; male ornamentation; behavioural and morphological similarity; and phylogenetic distance. Paired mate-choice trials were used in which females were presented with a conspecific and heterospecific male to test which of the above between-species differences best predicted the degree of premating isolation. The three species differed in the degree of species-specific mate preference shown. Females from the brighter two species discriminated against dull males, independently of sympatry-allopatry, similarity and phylogenetic distance. Females from the dull species reacted to conspecific males and brighter heterospecific males equally strongly, independently of similarity and phylogenetic distance. In contrast to previous studies, an equal preference for heterospecific and conspecific males was found under natural conditions. It is suggested that differences between closely related species in male ornamentation affect the likelihood that premating isolation will occur due to the fact that sexual selection tends to drive preferences for exaggerated ornamentation.     

Females discriminate against heterospecific sperm in a natural hybrid zone

When hybridization is maladaptive, species‐specific mate preferences are selectively favored, but low mate availability may constrain species‐assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long‐term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement‐like process.     

Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish

The evolutionary outcome of interspecific hybridization, i.e. collapse of species into a hybrid swarm, persistence or even divergence with reinforcement, depends on the balance between gene flow and selection against hybrids. If female mating preferences are open-ended but sign-inversed between species, they can theoretically be a source of such selection. Cichlid fish in African lakes have sustained high rates of speciation despite evidence for widespread hybridization, and sexual selection by female choice has been proposed as important in the origin and maintenance of species boundaries. However, it had never been tested whether hybridizing species have open-ended preference rules. Here we report the first experimental test using Pundamilia pundamilia, Pundamilia nyererei and their hybrids in three-way choice experiments. Hybrid males are phenotypically intermediate. Wild-caught females of both species have strong preferences for conspecific over heterospecific males. Their responses to F1 hybrid males are intermediate, but more similar to responses to conspecifics in one species and more similar to responses to heterospecifics in the other. We suggest that their mate choice mechanism may predispose haplochromine cichlids to maintain and perhaps undergo phenotypic diversification despite hybridization, and that species differences in female preference functions may predict the potential for adaptive trait transfer between hybridizing species.     

Predation risk and the opportunity for female mate choice in a coral reef fish

The influence of predation risk on the opportunity for female mate choice was investigated in the tailspot wrasse Halichoeres melanurus at two sites on a coral reef in Okinawa, Japan. Females mated repeatedly with the nearest males, but they also changed mates frequently at both sites. Mate changes were seen not only in the context of spatiosocial changes (mate disappearance or shifts in male territories) but were also probably the result of actual mate choice by females. Females at one site (site A) changed mates more often and conducted longer spawning trips from their home ranges to male territories than at the other site (site B). Fish at site A were faced with a higher frequency of predators than that of site B. However, fish of site A suffered fewer attacks from predators because they had more shelter, suggesting lower predation risk in that site. These results suggest that females under higher predation risk had less opportunity to choose preferable mates and that they had to mate with the same, nearest males in most cases.     

Unilateral Mate Choice Causes Bilateral Behavioral Isolation Between Two Closely Related Phytophagous Ladybird Beetles (Coleoptera: Coccinellidae: Epilachninae)

Behavioral isolation between two sympatric and closely related phytophagous ladybird beetles, Henosepilachna vigintioctomaculata and Henosepilachana pustulosa, was studied in laboratory. Mating behavior was investigated using the male‐choice test. Males of H. vigintioctomaculata preferred conspecific females to heterospecific females as mates, whereas males of H. pustulosa did not show such preference. Females of H. vigintioctomaculata appeared more fastidious at mating than females of H. pustulosa, irrespective of the species of males. Males of neither species showed tenaciousness following rejection by females. The choice of conspecifics by H. vigintioctomaculata males and a difference in the intensity of rejection between H. vigintioctomaculata females (strong) and H. pustulosa females (weak) result in positive behavioral isolation in both directions of heterospecific matings. Our results thus indicated that positive unilateral mate choice yields bilateral behavioral isolation between these two species.     

The impact of social context on male mate preference in a unisexual--bisexual mating complex

Male sailfin mollies Poecilia latipinna were tested in five different treatments that varied in the relative frequency of heterospecific gynogens (Amazon molly Poecilia formosa) to conspecific females to determine whether social interactions among males within a population causes some males to mate with heterospecific females. Male P. latipinna inseminated a significantly higher proportion of conspecific females and fertilized a significantly higher number of conspecific eggs regardless of the treatment. Nonetheless, preference for conspecific females was not exclusive as a range of 20 to 50% of heterospecific females were fertilized. Social interactions among males may best explain the results and may therefore play an important role in the maintenance of unisexual--bisexual mating complexes.     

Responses of larval dragonflies to conspecific and heterospecific predator cues

Abstract.  1. In cannibalistic populations, smaller individuals are subject to predation by larger conspecifics, and small individuals commonly alter their behaviour in response to cannibals. Little is known, however, about the underlying cues that trigger such responses and how the behavioural responses to conspecific cannibals differ from heterospecific predators.
2. This study tests which cues are used for the detection of conspecific predators in the larva of the dragonfly Plathemis lydia and how the behavioural response to cannibals differed from the response to heterospecific predators.
3. Individuals were exposed to chemical cues, visual cues, and a combination of both cues from conspecifics as well as no predator and heterospecific predator controls during which their activity and feeding rates were observed.
4. Individuals increased their activity, spatial movement and feeding behaviour in response to either visual or chemical cues from conspecific predators, which was opposite to responses displayed with cues from heterospecific predators. Interestingly, the responses to visual and chemical cues from conspecifics combined were weaker than to either cue in isolation and similar to the no cue control.
5. The results clearly indicate that individuals are able to use chemical and visual cues to detect even very subtle differences in phenotype of conspecific predators.
6. The opposite response in behaviour when exposed to conspecific cannibals vs. heterospecific predators suggests that the presence of cannibals will increase the mortality risk of small individuals due to heterospecific predation. This risk-enhancement is likely to have important consequences for the dynamics of predator–prey interactions.     

INTERSPECIFIC RECOGNITION AND DISCRIMINATION BASED UPON OLFACTORY CUES IN NORTHERN SWORDTAILS

Female Xiphophorus montezumae were attracted to olfactory cues from conspecific and heterospecific (X. cortezi and X. nigrensis) males when given a choice between the stimulus and water. When given a choice between conspecific and heterospecific cues, females only demonstrated a strong preference for the conspecific stimulus when it was matched against X. nigrensis. Female X. nigrensis were attracted to olfactory cues from their close relative, X. cortezi, but did not respond to cues from the more distantly related X. montezumae. They preferred the scent of their own males to the olfactory cues of both heterospecific species. Our results indicate that X. cortezi and X. nigrensis share an apomorphic change in some aspect of their olfactory cue-receiver system that is not shared with X. montezumae. We also uncovered an asymmetry in response based on olfactory stimuli in these fishes: X. montezumae is moderately attracted to the cue from X. nigrensis, whereas X. nigrensis does not respond to the cue from X. montezumae at all.     

Plasticity of the mate choice mind: courtship evokes choice‐like brain responses in females from a coercive mating system

Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole‐brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species‐level differences in female behavioral and brain molecular responses represent ‘canalized’ or ‘plastic’ traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole‐brain gene expression analyses of neuroserpin, egr‐1 and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning‐based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion‐driven mating systems.     

Reproductive isolation inProkelisia planthoppers (Homoptera: Delphacidae): Acoustic differentiation and hybridization failure

Males and females of Prokelisia marginata (Van Duzee) and Prokelisia dolusWilson communicate through substrate-transmitted vibrations. The acoustic signals (attraction and courtship calls) of these planthoppers are effective in mate location, attraction, and mate choice. Attraction calls are structurally distinct for both species and differ in pulse type, pulse repetition rate, and pulse duration. Using playback of prerecorded calls, individuals discriminated between conspecific and heterospecific signals. Depending on the sex and species, response calls were produced three to eight times more frequently to conspecifics than to heterospecifics. However, acoustic signals alone did not explain reproductive isolation and hybridization failure in these two congeners. Some heterospecific pairs called, courted, and attempted to join genitalia, but no connections were successful and no progeny were produced. Thus, acoustic behavior is not a guaranteed premating isolating mechanism in no-choice situations. Other courtship behaviors and possibly morphological differences in genitalia also contributed to their isolation. Females displayed a variety of rejection behaviors to conspecific and heterospecific males, suggesting that sexual selection (female choice), in addition to species recognition, may be an important force in the evolution of the acoustic signals of planthoppers. Although signal structure was not dependent on wing form (planthoppers exhibit wing dimorphism), the age when females first began to call was related to wing form. Brachypterous (flightless) females of both species began calling early in adult life (day 2), whereas macropterous (migratory) females began calling later in adult life (day 6). This pattern is consistent with the oogenesis-flight syndrome, in which reproductive maturity is delayed until after migration occurs.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.