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.     

Male tree weta are attracted to cuticular scent cues but do not discriminate according to sex or among two closely related species

Recognition of conspecifics is an essential precursor of successful mating. Where related species coexist, species discrimination might be important, but because related species are similar, species signal recognition may actually be low. Chemical cues such as cuticular hydrocarbons (CHCs) are frequently used by insects to identify suitable sexual partners. We predicted that New Zealand tree weta (Hemideina spp.), a genus of nocturnal ensiferan Orthoptera that live both allopatrically and sympatrically, use chemical signals from either frass or CHCs to find mates. In a series of six laboratory trials using both H. thoracica and H. crassidens, we found that male tree weta, but not female tree weta, occupied cavities primed with female cuticular cues more often than cavities without. However, males did not discriminate between chemical cues of male and female conspecifics, or between conspecifics and heterospecifics. In field trials, tree weta did not occupy artificial cavities primed with either female frass or female cuticular cues more often than unscented cavities. However, in both trials weta preferentially returned to cavities that had already been occupied earlier in the trials. A final field trial confirmed the presence of mixed species harems during the mating season in one region of sympatry. Our results suggest that selection on sex and species specific chemical cues that could be used to find conspecific mates is weak. Mixed species aggregations suggest that identification of conspecific mating cues has not evolved to be species specific. We infer that for male tree weta, the cost of mating with heterospecifics is likely less than not mating at all.     

Character displacement and the evolution of mate choice: an artificial neural network approach

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.     

The mosaic distribution pattern of two sister bush‐cricket species and the possible role of reproductive interference

Reproductive interference can shape regional distribution patterns in closely related species, if prezygotic isolation barriers are weak. The study of such interaction could be more challenging in nuptial gift‐giving species due to the direct nutritional effects on both sexes of both species during copulation. We mapped the distribution of two sister bush‐cricket species, Pholidoptera aptera and Pholidoptera transsylvanica, at the northern margin of their overlapping ranges in Europe, and with a behavioral experiment, we tested the possibility of heterospecific mating. We found a very rare coexistence of species locally (0.5%, n = 391 sites) with mostly mutually exclusive distribution patterns, resulting in a mosaic pattern of sympatry, whereas they occupied the same climate niche in forest‐dominated mountain landscape. Over 14 days of a mating experiment with seven mixed groups of conspecifics and heterospecifics (n = 56 individuals in total), the number of received spermatophores per female was 3–6 in P. aptera and 1–7 in P. transsylvanica. In total, we found 8.1% of heterospecific copulations (n = 99 transferred spermatophores with genetic identification of the donor species), while we also confirmed successful transfer of heterospecific sperms into a female's reproductive system. Because bush‐cricket females also obtain required nutrition from a heterospecific spermatophylax what should increase their fitness and fecundity, we suggest that their flexibility to mate with heterospecifics is beneficial and drives reproductive interference. This may substantially limit the reproductive success of the less frequent species (P. transsylvanica), coupled with eventual detrimental effects from hybridization, and result in the competitive exclusion of that species from their areas of coexistence.     

Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps

Animals need to be able to identify other species, which iscrucial in competition for ecological resources, for using otherspecies as a cue in habitat selection, and for the establishmentand maintenance of parasite-host species associations in brood-parasiticspecies. The ability to discriminate between conspecifics andheterospecifics may be crucially important also in refinementof mating preferences during speciation and for premating isolationof sympatric species. It has long been hypothesized that speciesidentification ability is based on learned associations betweenmultiple features that distinguish species. Here I test thishypothesis using dual-choice song playback experiments withinterspecifically territorial male blackcaps (Sylvia atricapilla)that defend territories against male garden warblers (Sylviaborin). I show that male blackcaps can associate species-specificsongs with species-specific plumage and also that they retainthe memory of this association for an 8-month period withoutcontact with heterospecific rivals. Apparently, yearling maleblackcaps achieve this ability several months prior to theirfirst breeding attempt. This is the first time a long-term memoryof associations between species-specific signals from two differentsensory modalities (visual and auditory) has been shown to beimportant for distinguishing conspecifics from heterospecifics.     

Female mate preferences on high‐dimensional shape variation for male species recognition traits

Females in many animal species must discriminate between conspecific and heterospecific males when choosing mates. Such mating preferences that discriminate against heterospecifics may inadvertently also affect the mating success of conspecific males, particularly those with more extreme phenotypes. From this expectation, we hypothesized that female mate choice should cause Enallagma females (Odonata: Coenagrionidae) to discriminate against conspecific males with more extreme phenotypes of the claspers males use to grasp females while mating – the main feature of species mate recognition in these species. To test this, we compared cerci sizes and shapes between males that were captured while mating with females to males that were captured at the same time but not mating in three Enallagma species. In contrast to our hypothesis, we found only one of forty comparisons of shape variation that was consistent with females discriminating against males with more extreme cerci shapes. Instead, differences in cerci shape between mating and single males suggested that females displayed directional preferences on 1–4 aspects of cerci shape in two of the species in our samples. These results suggest that whereas some directional biases in mating based on cerci shape occur, the intraspecific phenotypic variation in male cerci size and shape is likely not large enough for females to express any significant incidental discrimination among conspecifics with more extreme shapes.     

Early Learning and the Recognition of Conspecific Cocoons by Carpenter Ants (Camponotus spp.)

Groups of newly-eclosed workers of two carpenter ant species (Camponotus floridanus and C. tortuganus) were reared in the presence of conspecific cocoons, cocoons of the other species, or were kept without cocoons. Groups of older workers (> 20 days), previously exposed to conspecific brood in their natal nest, were familiarized with either conspecific or heterospecific cocoons. After 14 days of exposure, groups were subjected to short-term (5 min) and long-term (10 day) preference tests. Young and older workers retrieved and retained many cocoons of both species, familiar and unfamiliar. However, a pattern of non-exclusive discrimination emerged: (1) Young workers exposed to conspecific cocoons picked up and retrieved conspecifics before unfamiliar heterospecifics, and retained conspecifics longer. (2) Young workers generally required experience with conspecifics to develop this preference, as those exposed to only heterospecifics and those deprived of cocoons were impartial in short-term tests. However, in long-term tests (5–10 days), naive young workers significantly preferred unfamiliar conspecifics. (3) Older workers preferred conspecific cocoons, whether familiar or unfamiliar, in short-term tests, but their tolerance for heterospecifics in the longer term (5 days) could be increased by recent familiarization. In no case did young or older ants significantly prefer familiar heterospecifics to conspecifics. These results confirm a role for early learning in brood recognition by carpenter ants, but suggest that it is less important than in Formica species studied by previous authors.     

Mate-guarding in a promiscuous insect: species discrimination influences context-dependent behaviour

Mating strategy is often informed by social context. However, information on social environment may be sensitive to interference by nearby heterospecifics, a process known as reproductive interference (RI). When heterospecific individuals are present in the environment, failures in species discrimination can lead to sub-optimal mating behaviours, such as misplaced courtship, misplaced rivalry behaviours, or heterospecific copulation attempts. All aspects of mating behaviour that are influenced by social context may be prone to RI, including copulatory behaviours associated with mate-guarding in the presence of possible competitors. Here we investigate the effect of three heterospecifics on the mate-guarding behaviour of male Lygaeus equestris seed bugs. We find that, despite previously reported heterospecific mating harassment amongst these species of lygaeid bug, male L. equestris are able to effectively distinguish rival conspecific males from heterospecifics. Thus, heterospecific mating attempts in this group may reflect selection on males to mate opportunistically, rather than a failure of species discrimination.     

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.     

Interspecific Response to Playback of Bird Song

Responses to bird song have usually only been studied at the intraspecific level. I experimentally tested whether playback of the song of the black wheatear Oenanthe leucura in an area in S Spain resulted in responses from conspecifics as well as heterospecific birds by comparing the numbers of individuals singing before and after playback. The number of singing male black wheatears increased considerably, but also the number of singing males of five other passerine species increased significantly. The heterospecific response to playback may be due (1) to interspecific territoriality, (2) to black wheatear song signalling the absence of predators, or (3) to heterospecifics confusing the species-identity of the singer. The second alternative is considered more likely, since an ecologically wide array of species increased their song rate following playback. The conspicuous dawn (and dusk) chorus of bird song may be augmented by social facilitation due to the singing of conspecifics as well as heterospecifics.     

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     

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.     

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.     

Conspecific and heterospecific information use in bumblebees

Heterospecific social learning has been understudied in comparison to interactions between members of the same species. However, the learning mechanisms behind such information use can allow animals to be flexible in the cues that are used. This raises the question of whether conspecific cues are inherently more influential than cues provided by heterospecifics, or whether animals can simply use any cue that predicts fitness enhancing conditions, including those provided by heterospecifics. To determine how freely social information travels across species boundaries, we trained bumblebees (Bombus terrestris) to learn to use cues provided by conspecifics and heterospecific honey bees (Apis mellifera) to locate valuable floral resources. We found that heterospecific demonstrators did not differ from conspecifics in the extent to which they guided observers'' choices, whereas various types of inorganic visual cues were consistently less effective than conspecifics. This was also true in a transfer test where bees were confronted with a novel flower type. However, in the transfer test, conspecifics were slightly more effective than heterospecific demonstrators. We then repeated the experiment with entirely naïve bees that had never foraged alongside conspecifics before. In this case, heterospecific demonstrators were equally efficient as conspecifics both in the initial learning task and the transfer test. Our findings demonstrate that social learning is not a unique process limited to conspecifics and that through associative learning, interspecifically sourced information can be just as valuable as that provided by conspecific individuals. Furthermore the results of this study highlight potential implications for understanding competition within natural pollinator communities.     

Do allopatric male Calopteryx virgo damselflies learn species recognition?

There is a growing amount of empirical evidence that premating reproductive isolation of two closely related species can be reinforced by natural selection arising from avoidance of maladaptive hybridization. However, as an alternative for this popular reinforcement theory, it has been suggested that learning to prefer conspecifics or to discriminate heterospecifics could cause a similar pattern of reinforced premating isolation, but this possibility is much less studied. Here, we report results of a field experiment in which we examined (i) whether allopatric Calopteryx virgo damselfly males that have not encountered heterospecific females of the congener C. splendens initially show discrimination, and (ii) whether C. virgo males learn to discriminate heterospecifics or learn to associate with conspecifics during repeated experimental presentation of females. Our experiment revealed that there was a statistically nonsignificant tendency for C. virgo males to show initial discrimination against heterospecific females but because we did not use sexually naïve individuals in our experiment, we were not able to separate the effect of innate or associative learning. More importantly, however, our study revealed that species discrimination might be further strengthened by learning, especially so that C. virgo males increase their association with conspecific females during repeated presentation trials. The role of learning to discriminate C. splendens females was less clear. We conclude that learning might play a role in species recognition also when individuals are not naïve but have already encountered potential conspecific mates.     

Aggression and nest spacing in single and mixed species groups of seabirds

When heterospecific seabirds are part of a nesting colony, there may be less opportunity for conspecifics to come in direct contact with each other, resulting in lower intraspecific aggressiveness. To determine if individuals spend less time in aggressive behavior when nesting in conspecific rather than heterospecific groups, we compared the behavior of black skimmers (Rhynchops niger) nesting with gull-billed terns (Sterna nilotica) in three mixed species subcolonies to those of black skimmers in three single species subcolonies. In contrast to our predictions, black skimmers spent significantly less time in aggressive behaviors when nesting in single species subcolonies than when nesting with heterospecifics. Although skimmers in mixed species subcolonies tended to have more aggressive interactions with skimmers than terns, this may be a function of subcolony composition; the proportions of aggressive interactions with conspecifics were similar to the proportions of conspecifics in each subcolony. However, within the mixed species subcolonies, skimmers that nested nearer to terns were involved in aggressive interactions significantly less than skimmers that nested closer to conspecifics. Also, skimmers nested closer to their nearest neighbor when it was a gull-billed tern than when it was another skimmer. Regardless of which species they nested closest to, skimmers were more aggressive towards other skimmers than to terns within the mixed species subcolonies. Distance to nearest neighbor's nest did not differ significantly between the colony types, and did not seem to influence the duration of aggressive activity in the single species subcolonies. In the mixed species subcolonies, however, the time spent in aggressive behavior increased as the distance to nearest neighbor increased. It appears that of the several benefits that have been proposed of mixed species colonies, reduced time spent in conspecific aggression is not among them. However, within a mixed species colony, an individual can reduce time spent in aggressive interactions by nesting near heterospecifics. Received: 16 September 1996 / Accepted: 24 February 1997     

Oddity,predation risk and social decisions in aquatic invertebrates

Group living is widespread across animal taxa, incurring benefits such as increased foraging efficiency or an enhanced chance of surviving a predator's attack. The chances of escaping a predator are often lower for odd‐looking individuals, as these are detected at a higher rate than uniform looking group members. While this “oddity effect” shall operate in animals differing in any given phenotype, including colour, size or species identity, it has been experimentally tested mainly for odd‐coloured individuals. We examined the oddity effect and swarming preferences in two differently sized species of freshwater planktonic crustaceans (large Daphnia magna and small Daphnia pulex). We experimentally investigated whether odd individuals in a swarm of heterospecific Daphnia were more vulnerable to predation by a common predator, the three‐spined stickleback (Gasterosteus aculeatus). Furthermore, Daphnia's swarming preference was tested by giving individuals the opportunity to choose between conspecific/heterospecific odour and a neutral control. In contrast to the predictions of the oddity effect, odd individuals were not always preyed on earlier; instead three‐spined stickleback preferentially predated large, more nutritious individuals. Daphnia of both species reacted towards the perception of con‐ and heterospecifics odours. While D. pulex generally avoided the smell of other daphnids, D. magna avoided conspecifics but tended to prefer heterospecifics over the neutral control. These findings provide new insights into swarming strategies and social preference of an invertebrate and how this behaviour can influence predation risk.     

Host acceptance and sex allocation of Nasonia wasps in response to conspecifics and heterospecifics

Species recognition is an important aspect of an organism''s biology. Here, we consider how parasitoid wasps vary their reproductive decisions when their offspring face intra- and interspecific competition for resources and mates. We use host acceptance and sex ratio behaviour to test whether female Nasonia vitripennis and Nasonia longicornis discriminate between conspecifics and heterospecifics when ovipositing. We tested pairs of conspecific or heterospecific females ovipositing either simultaneously or sequentially on a single host, using strains varying in their recent history of sympatry. Both N. vitripennis and N. longicornis rejected parasitized hosts more often than unparasitized hosts, although females were more likely to superparasitize their own species in the sequential treatment. However, sex ratio behaviour did not vary, suggesting similar responses towards conspecifics and heterospecifics. This contrasts with theory predicting that heterospecifics should not influence sex ratios as their offspring do not influence local mate competition, where conspecifics would. These non-adaptive sex ratios reinforce the lack of adaptive kin discrimination in N. vitripennis and suggest a behavioural constraint. Discrimination between closely related species is therefore context dependent in Nasonia. We suggest that isolating mechanisms associated with the speciation process have influenced behaviour to a greater extent than selection on sex ratios.     

The Effects of Density on the Learned Recognition of Heterospecific Alarm Cues

Numerous species, both aquatic and terrestrial, use alarm cues to mediate predation risk. These cues may be either intentionally or inadvertently released, and may be received by either conspecifics or heterospecifics. In aquatic systems, alarm cues are often chemical in nature and are released when an organism is disturbed or damaged by a predator. In some cases the recognition of alarm cues from conspecifics, or closely related heterospecifics, is innate, while the recognition of alarm cues from distantly related species must be learned. Many studies have documented the use of heterospecific alarm cues, but few have explored the manner in which these cues come to be recognized as an indication of predation. In the current study, we examined the fathead minnow (Pimephales promelas)/brook stickleback (Culaea inconstans) alarm system. We tested the effect of density on the ability of minnows to learn to recognize stickleback alarm cues as a threat. We hypothesized that the ability of minnows to learn to recognize stickleback alarm cues should increase with increasing stickleback density because there would be more opportunity for minnows to associate the heterospecific alarm cue with the threat. To test this hypothesis we stocked minnows into large outdoor pools with no stickleback, low numbers of stickleback, or high numbers of stickleback. All pools contained a predator (pike, Esox lucius) known to the minnows. Following a 14 d conditioning period, minnows were tested for a response to skin extract from stickleback, minnow, and an unknown heterospecific (swordtail, Xiphophorus helleri). Minnows from pools with large numbers of stickleback learned to respond to stickleback alarm cues while minnows from pools with low numbers of stickleback, or no stickleback, did not.