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.     

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.     

Drosophila melanogaster males respond differently at the behavioural and genome‐wide levels to Drosophila melanogaster and Drosophila simulans females

Drosophila melanogaster are found in sympatry with Drosophila simulans, and matings between the species produce nonfertile hybrid offspring at low frequency. Evolutionary theory predicts that females choose mates, so males should alter their behaviour in response to female cues. We show that D. melanogaster males quickly decrease courtship towards D. simulans females. Courtship levels are reduced within 5 min of exposure to a heterospecific female, and overall courtship is significantly lower than courtship towards conspecific females. To understand changes at the molecular level during mate choice, we performed microarray analysis on D. melanogaster males that courted heterospecific D. simulans females and found nine genes have altered expression compared with controls. In contrast, males that court conspecific females alter expression of at least 35 loci. The changes elicited by conspecific courtship likely modulate nervous system function to reinforce positive conspecific signals and dampen the response to heterospecific signals.     

Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas

Female and male mate choices can reinforce reproductive isolation after sympatric speciation. Using a binary choice design, we examine the importance of visual cues in female mate choice in all three sympatric species of pupfish on San Salvador Island. We also examine the importance of olfactory cues in female choice of the hard‐shelled invertebrate specialist (Cyprinodon brontotheroides). We examine male mate choice in two of the three species, the scale eater (C. desquamator) and the detritivore (C. variegatus). Females of all three species use visual cues and prefer conspecific males. C. brontotheroides females do not use olfactory cues to discriminate between conspecific and heterospecific males. Males of C. desquamator and C. variegatus also preferentially court conspecific females. Thus, mutual mate choice, where both females and males exhibit mate choice, acts as a strong behavioral pre‐mating isolation mechanism in these sympatrically speciated pupfish.     

Linking intra‐ and interspecific assortative mating: Consequences for asymmetric sexual isolation

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within‐species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male–male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.     

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.     

Incomplete behavioural isolation and asymmetric female preference in darter sister species (Percidae: Etheostoma)

In this study, female preferences and behavioural isolation were estimated in a pair of allopatric sister species, Etheostoma duryi and Etheostoma flavum. Dichotomous mate preference trials were conducted to determine whether females prefer to associate with conspecific over heterospecific males and free‐spawning assays were conducted to determine whether those preferences translated into behavioural isolation. Dichotomous mate choice trials revealed asymmetric female preference, as female E. flavum preferred conspecific males, whereas female E. duryi showed no preference. Free‐spawning assays indicated that behavioural isolation remains incomplete between E. duryi and E. flavum (I_B = 0·19). In addition to female mating preferences, male behaviour also appeared to influence mating outcomes as male E. flavum consistently courted conspecific females more often in free‐spawning assays whereas male E. duryi did not. The data therefore suggest that despite marked divergence in male nuptial colour, divergence in female preferences between these species may not be sufficient to maintain species boundaries upon secondary contact. These results contrast with similar work in a sympatric darter species pair and may be explained by considering the contributions of reinforcement and differences in colour pattern as well as colour value.     

Lack of species discrimination based on chemical cues by male sailfin mollies, <Emphasis Type="Italic">Poecilia latipinna</Emphasis>

When making mating decisions, individuals may rely on multiple cues from either the same or multiple sensory modalities. Although the use of visual cues in sexual selection is well studied, fewer studies have examined the role of chemical cues in mate choice. In addition, few studies have examined how visual and/or chemical cues affect male mating decisions. Male mate choice is important in systems where males must avoid mating with heterospecific females, as is found in a mating complex of Poecilia. Male sailfin mollies, Poecilia latipinna, are sexually parasitized by gynogenetic Amazon mollies, P. formosa. Little is known about the mechanism by which male sailfin mollies base their mating decisions. Here we tested the hypothesis that male sailfin mollies from an allopatric and a sympatric population with Amazon mollies use multiple cues to distinguish between conspecific and heterospecific females. We found that male sailfin mollies recognized the chemical cues of conspecific females, but we found no support for the hypothesis that chemical cues are by themselves sufficient for species discrimination. Lack of discrimination based on chemical cues alone may be due to the close evolutionary history between P. latipinna and P. formosa. Males from populations sympatric with Amazon mollies did not differentially associate with females of either of the two species when given access to both visual and chemical cues of the females, yet males from the allopatric population did associate more with conspecific females than with heterospecific females in the presence of both chemical and visual cues. The lack of discrimination by males from the sympatric population between conspecific and heterospecific females based on both chemical and visual cues suggests that these males require more complex combinations of cues to distinguish species, possibly due to the close relatedness of these species.     

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.     

Conspecific and heterospecific pheromone effects on female receptivity

Courtship pheromones play an important role in salamander reproductive behaviour. In salamanders of the family Plethodontidae, males deliver specialized pheromones to females during courtship interactions. These courtship pheromones increase female receptivity and may be involved in mate discrimination. In order to test hypotheses related to mate discrimination, we staged courtship encounters between male-female Plethodon shermani pairs in which the female received pheromones obtained from either conspecific (P. shermani) or heterospecific (P. yonahlossee orP. montanus ) males. Both conspecific and heterospecific pheromones increased female receptivity. Moreover, pheromones from both heterospecific species were as effective as the conspecific pheromone in increasing female receptivity inP. shermani females. Our results suggest that the courtship pheromone signal and function may be conserved across related species, with mate discrimination occurring before pheromone delivery. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Gender differences in species recognition and the evolution of asymmetric sexual isolation

Closely related sympatric species are expected to evolve strong species discrimination because of the reinforcement of mate preferences. Fitness costs of heterospecific matings are thought to be higher in females than in males, and females are therefore expected to show stronger species discrimination than males. Here, we investigated gender and species differences in sexual isolation in a sympatric species pair of Calopteryx damselflies. The genus Calopteryx is one of the classic examples of reproductive character displacement in evolutionary biology, with exaggerated interspecific differences in the amount of dark wing coloration when species become sympatric. Experimental manipulation of the extent of dark wing coloration revealed that sexual isolation results from both female and male mate discrimination and that wing melanization functions as a species recognition character. Female choice of conspecific males is entirely based on wing coloration, whereas males in one species also use other species recognition cues in addition to wing color. Stronger species discrimination ability in males is presumably an evolutionary response to an elevated male predation risk caused by conspicuous wing coloration. Gender differences in species discrimination and fitness costs of male courtship can thus shed new light on the evolution of asymmetric sexual isolation and the reinforcement of mate preferences.     

Genetic and behavioral components of the cryptic species boundary between Laupala cerasina and L. kohalensis (Orthoptera: Gryllidae)

Cryptic species are often hypothesized on the basis of differences in courtship signals. These signal differences suggest that mate recognition systems, which include both courtship signals and responses to those signals, have diverged between genetically isolated populations. Cryptic species are therefore thought to represent distinct genetic units, the boundaries of which are maintained by premating incompatibilities, specifically by receiver preferences for conspecific signals. Laupala cerasina and L. kohalensis are sympatric species of swordtail crickets endemic to the big island of Hawaii, that are distinguishable by differences in male courtship song. We first tested whether groupings hypothesized by acoustic similarity reflect genetic groupings, using AFLP data to estimate genetic relationships. Second, we tested whether genetic boundaries are maintained by female preferences for conspecific song characteristics. Phonotaxis trials were used to determine the extent of female preferences for conspecific male song. Results generally support both hypotheses, but suggest the presence of porous species boundaries.     

Effects of Courtship Song in Interspecific Crosses Among the Species of the Drosophila auraria Complex (Diptera: Drosophilidae)

The courtship behavior and the effects of courtship song in inter- and intraspecific crosses were studied in the four sympatric species of the Drosophila auraria complex: D. auraria, D. biauraria, D. subauraria, and D. triauraria. Orientation, tapping, and vibration (the repertoires of male courtship) were observed in both inter- and intraspecific crosses, suggesting that signals from heterospecific females were enough to elicit such male behaviors. The crossability tests with wingless or winged heterospecific males (tests for wing effects) revealed that winged heterospecific males copulated less than wingless ones in all four species but not all the pairwise cases. Since the crossability tests with aristaless females (deaf) or normal females showed essentially the same results as the tests for wing effects, we concluded that the sound produced by wing vibration plays an important role and that the wing movement itself is less important. These findings suggest that courtship songs are of great importance in mate discrimination and the sexual isolation between the species of this complex.     

Olfactory mate recognition in a sympatric species pair of three-spined sticklebacks

Mate recognition is critical to the maintenance of reproductiveisolation, and animals use an array of sensory modalities toidentify conspecific mates. In particular, olfactory informationcan be an important component of mate recognition systems. Weinvestigated whether odor is involved in mate recognition ina sympatric benthic and limnetic species pair of three-spinedsticklebacks (Gasterosteus spp.), for which visual cues andsignals are known to play a role in premating isolation. Weallowed gravid females of each species to choose between waterscented by a heterospecific male and water scented by a conspecificmale. Benthic females preferred the conspecific male stimuluswater significantly more often than the heterospecific malestimulus water, whereas limnetic females showed no preference.These species thus differ in their odor and may also differin their use of olfaction to recognize conspecific mates. Thesedifferences are likely a consequence of adaptation to disparateenvironments. Differences in diet, foraging mode, habitat, andparasite exposure may explain our finding that odor might bean asymmetric isolating mechanism in these sympatric sticklebackspecies.     

Assortative aggression among males in a sympatric pair of Labeotropheus from Lake Malaŵi,Africa

Female mate choice has strong experimental support as a diversifying force in the speciation of the haplochromine cichlid fishes of Lake Malaŵi, Africa. Somewhat less understood is the role that male–male aggression might have played in the evolution of new species of these fishes. In the rock-dwelling haplochromines of Lake Malaŵi, primarily territory-holding males successfully court females; by determining which males gain territories, male–male aggression could support speciation by excluding less-fit males from the breeding population. To test the hypothesis that males should direct more aggression towards conspecific rivals, the aggression directed towards conspecific and heterospecific opponents was compared in a sympatric pair of cichlids of the genus Labeotropheus Ahl 1927 (Labeotropheus fuelleborni Ahl 1927 and Labeotropheus trewavasae Fryer 1956). It was found that when presented with a pair of rivals, males of both species did direct more aggression towards the conspecific opponent, and the amount of aggression increased when the conspecific opponent was larger than the heterospecific opponent. In addition, this study found a difference in the behavioural repertoire of the species: L. fuelleborni tends to rely on displays to intimidate opponents, whereas L. trewavasae employs more physical attacks to drive away opponents. Males of both species can thus recognize conspecifics and assess an opponent's relative threat to their ability to successfully reproduce, and use species-specific strategies to intimidate opponents.     

The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species

Closely related species of lycaenid butterflies are determinable, in part, by subtle differences in wing pattern. We found that female wing patterns can act as an effective mate‐recognition signal in some populations of two recently diverged species. In field experiments, we observed that males from a Lycaeides idas population and an alpine population of L. melissa preferentially initiate courtship with conspecific females. A morphometric study indicated that at least two wing pattern elements were important for distinguishing the two species: hindwing spots and orange crescent‐shaped pattern elements called aurorae. We deceived male L. idas into initiating courtship with computer generated paper models of heterospecific females when these pattern elements were manipulated, indicating that the wing pattern elements that define the diversity of this group can be effective mate recognition signals.     

Learned mate recognition and reproductive isolation in guppies

Research on learned species discrimination has focused on the consequences of early experience. However, in species where parental care is limited or absent, including most fish, juveniles have fewer opportunities to learn from adult conspecifics. We examined male mate recognition in Trinidadian guppies, Poecilia reticulata, and in their sister species, the swamp guppy, P. picta. Choice tests revealed that males from localities where their species is the only poeciliid present initially mated with conspecific and heterospecific females at random. In contrast, P. reticulata and P. picta found in sympatry preferred their own females. We then investigated the acquisition of mating discrimination by wild P. reticulata males from two allopatric populations. Males that were allowed to interact with females of both species learned within 4 days to distinguish conspecific partners, and within a week their species discrimination matched that of sympatric populations. This study confirms that learning is important in the acquisition of adult mating preferences and shows why learned mate preferences can be important in the last stages of speciation.     

Avoiding Male Harassment: Wing‐Closing Reactions to Flying Individuals by Female Small Copper Butterflies

Males of many butterfly species persistently court and attempt to mate with females even if the females reject courtship. This male harassment almost certainly has negative effects on female fitness. Therefore, females have likely evolved strategies to avoid such encounters. To investigate the harassment avoidance strategy of females of the small copper butterfly, Lycaena phlaeas daimio, I observed the reactions of females to other individuals flying nearby in the field. In response to the conspecific butterflies, females closed their wings if they had previously been open and did not exhibit any action if the wings had been closed. Females that closed their open wings in response to a conspecific received fewer mating attempts than did females that held their wings open. These results indicate that the wing‐closing behaviour of L. phlaeas females functions to deter male mating attempts. The wing‐closing reaction occurred primarily in mated females. Because females of L. phlaeas copulate only once during their lives, this behaviour is not considered an indirect mate choice but rather an attempt to avoid persistent mating attempts (i.e. sexual harassment) by males.     

REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT

Detailed studies of reproductive isolation and how it varies among populations can provide valuable insight into the mechanisms of speciation. Here we investigate how the strength of premating isolation varies between sympatric and allopatric populations of threespine sticklebacks to test a prediction of the hypothesis of reinforcement: that interspecific mate discrimination should be stronger in sympatry than in allopatry. In conducting such tests, it is important to control for ecological character displacement between sympatric species because ecological character divergence may strengthen prezygotic isolation as a by-product. We control for ecological character displacement by comparing mate preferences of females from a sympatric population (benthics) with mate preferences of females from two allopatric populations that most closely resemble the sympatric benthic females in ecology and morphology. No-choice mating trials indicate that sympatric benthic females mate less readily with heterospecific (limnetic) than conspecific (benthic) males, whereas two different populations of allopatric females resembling benthics show no such discrimination. These differences demonstrate reproductive character displacement of benthic female mate choice. Previous studies have established that hybridization between sympatric species occurred in the past in the wild and that hybrid offspring have lower fitness than either parental species, thus providing conditions under which natural selection would favor individuals that do not hybridize. Results are therefore consistent with the hypothesis that female mate preferences have evolved as a response to reduced hybrid fitness (reinforcement), although direct effects of sympatry or a biased extinction process could also produce the pattern. Males of the other sympatric species (limnetics) showed a preference for smaller females, in contrast to the inferred ancestral preference for larger females, suggesting reproductive character displacement of limnetic male mate preferences as well.     

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.