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.     

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.     

A continent‐scale test of multiple hypotheses on the abundances of Neotropical birds

Explaining variation in the abundance of species remains a challenge in ecology. We sought to explain variation in abundance of Neotropical forest birds using a dataset of population densities of 596 species. We tested a priori hypotheses for the roles of species traits, environmental factors, and species interactions. Specifically, we focused on four factors: 1) body mass (trait), 2) habitat type (environmental factor), 3) net primary productivity (NPP; environmental factor) and 4) species richness of competitors (species interaction). Body size explained much variation in density, although only when analyzed at higher taxonomic levels. Habitat type was a strong predictor of density. The relationship between density and productivity was weak. Densities were related negatively to the species richness of heterospecifics. This trend was particularly strong within closely related groups. Our results show that the influence of energetic factors such as body size and productivity depends on phylogeny, and that they act through indirect relations with other variables; alternative ecological factors such as habitat structure and species interactions play a more direct and stronger role in determining abundance than previously thought.     

Conspecific-only experience during development reduces the strength of heterospecific song discrimination in Zebra Finches (Taeniopygia guttata): a test of the optimal acceptance threshold hypothesis

Conspecifics during development provide the most reliable sensory cues for species recognition in parental bird species. The Zebra Finch (Taeniopygia guttata) is a sexually dimorphic model species used for investigations of the behavioural cues and neurobiological substrates of species recognition. Regarding acoustic conspecific cues, theory predicts that exposure to both con- and heterospecific vocalisations and other environmental sounds results in more accurate auditory species discrimination, because diverse vocal cues during development shift optimal conspecific acceptance thresholds to be more restrictive to yield fewer acceptance errors. We tested the behavioural preferences of female and male Zebra Finches raised in an outdoor environment (Control) and female and male Zebra Finches reared in an indoor colony with exposure to Zebra Finches only (Restricted), to playbacks of songs of Zebra Finches, Zebra Finches cross-fostered by Bengalese Finches (Lonchura striata var. domestica), and Bengalese Finches. Several behavioural measures revealed minimal sexual dimorphism in discrimination but showed that Control subjects preferred conspecifics’ songs over either the songs of cross-fostered Zebra Finches or Bengalese Finches. Restricted Zebra Finches in contrast did not discriminate behaviourally between the three song types. These results support the concept of a shift in the species acceptance threshold in the restricted treatment resulting in more acceptance errors. We discuss future work to test the role of exposure to diverse vocal cues of both con- and heterospecifics in the ontogeny of song perception in this important laboratory model species for social recognition research.     

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.     

Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini)

Summary: Nestmate recognition was studied in the Neotropical stingless bee Melipona panamica, a species in which workers "sneak" their own reproductive eggs into 1 % of brood cells. We manipulated four factors that could influence individual recognition cues: the mother queen, the environment during the immature stage, the environment during the early adult stage, and worker age. We also simulated the action of natural enemies on colonies tested for discrimination of such worker characteristics. All factors that we tested affected responses of the discriminating workers, which could recognize sisters, nieces and unrelated workers. Previous exposure of unrelated callow bees to the odor of the host nest greatly increased chances of acceptance by the host colony. Probability of acceptance decreased, however, with increasing age of introduced bees or increasing disturbance of the host colony. These complexities in patterns of nestmate recognition and nest defense are adequately explained from the standpoint of inclusive fitness of the discriminating workers. Differences in nestmate recognition and worker egg laying among Meliponini are also discussed.     

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.     

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.     

SPECIES RECOGNITION AND PATTERNS OF POPULATION VARIATION IN THE REPRODUCTIVE STRUCTURES OF A DAMSELFLY GENUS

The selection pressures imposed by mate choice for species identity should impose strong stabilizing selection on traits that confer species identity to mates. Thus, we expect that such traits should show nonoverlapping distributions among closely related species, but show little to no variance among populations within a species. We tested these predictions by comparing levels of population differentiation in the sizes and shapes of male cerci (i.e., the clasper structures used for species identity during mating) of six Enallagma damselfly species. Cerci shapes were nonoverlapping among Enallagma species, and five of six Enallagma species showed no population variation across their entire species ranges. In contrast, cerci sizes overlapped among species and varied substantially among populations within species. These results, taken with previous studies, suggest that cerci shape is a primary feature used in species recognition used to discriminate conspecific from heterospecifics during mating.     

Cannibalism and Intraguild Predation Among Phytoseiid Mites: Are Aggressiveness and Prey Preference Related to Diet Specialization?

We tested whether specialist and generalist phytoseiid mites differ in aggressiveness and prey choice in cannibalism and intraguild predation. Specialists tested were Galendromus occidentalis, Neoseiulus longispinosus, Phytoseiulus persimilis, and P. macropilis; tested were Amblyseius andersoni, Euseius finlandicus, E. hibisci, Kampimodromus aberrans, Neoseiulus barkeri, N. californicus, N. cucumeris, N. fallacis, and Typhlodromus pyri. Aggressiveness of cannibalistic females against larvae was not related to diet specialization except that highly aggressive species were exclusively generalists. Seldom to moderately cannibalizing species occurred in both generalist and specialist phytoseiids. In contrast to aggressiveness in cannibalism, generalists and specialists differed in aggressiveness in intraguild predation. Adult females of specialists were only slightly aggressive against heterospecific larvae, whereas adult females of all generalists except T. pyri were highly aggressive. Adult females of generalists were able to discriminate between con- and heterospecific larvae and preferentially consumed the latter when given a choice. Adult females of specialists except G. occidentalis showed no preference when given a choice between con- and heterospecific larvae. We conclude that aggressiveness in intraguild predation, species recognition and subsequent preferential consumption of heterospecifics when given a choice is common in generalist but not specialist phytoseiids. We discuss the evolutionary pathways that might have led to the difference between specialists and generalists in species discrimination.     

Infochemical-mediated intraguild interactions among three predatory mites on cassava plants

Carnivorous arthropods exhibit complex intraspecific and interspecific behaviour among themselves when they share the same niche or habitat and food resources. They should simultaneously search for adequate food for themselves and their offspring and in the meantime avoid becoming food for other organisms. This behaviour is of great ecological interest in conditions of low prey availability. We examined by means of an olfactometer, how volatile chemicals from prey patches with conspecific or heterospecific predators might contribute to shaping the structure of predator guilds. To test this, we used the exotic predatory mites Typhlodromalus manihoti and T. aripo, and the native predatory mite Euseius fustis, with Mononychellus tanajoa as the common prey species for the three predatory mite species. We used as odour sources M. tanajoa-infested cassava leaves or apices with or without predators. T. manihoti avoided patches inhabited by the heterospecifics T. aripo and E. fustis or by conspecifics when tested against a patch without predators. Similarly, both T. aripo and E. fustis females avoided patches with con- or heterospecifics when tested against a patch without predators. When one patch contained T. aripo and the other T. manihoti, females of the latter preferred the patch with T. aripo. Thus, T. manihoti is able to discriminate between odours from patches with con- and heterospecifics. Our results show that the three predatory mite species are able to assess prey patch profitability using volatiles. Under natural conditions, particularly when their food sources are scarce, the three predatory mite species might be involved in interspecific and/or intraspecific interactions that can substantially affect population dynamics of the predators and their prey.     

Individual odour similarities across species parallel phylogenetic relationships in the S. ehrenbergi superspecies of mole-rats

Research using habituation techniques has shown that rodents from the same kin group, population, or species share similarities in their individual odours that covary with shared genetic similarities between them, that is, the closer their genetic relatedness, the more similar their odours. We assessed similarities in individual odours across four sibling species of subterranean mole-rats from the Spalax ehrenbergi superspecies in Israel. Mole-rats were habituated to the urine odour of a same-sex individual from one species then tested with urine odours of individuals from two different species of the superspecies. Subjects treated urine odours of individuals from more closely genetically related species as similar compared with the odours of individuals from a less closely related species, showing that the covariance between odours and genes extends across species. These similarities in odour also paralleled genetic similarities determined by molecular analysis: odours of descendent species were perceived as similar to those of their closest ancestral species, suggesting that some qualities of the odour of the ancestral species persist in the descendent species. It is generally assumed that during speciation incipient species develop species-specific markers, including, for example, odour markers, to facilitate discrimination of conspecifics from close ancestral heterospecifics. Our findings indicate that similarities in odours across species are more salient than species-specific odour markers. Such findings may also have important implications for mechanisms of species recognition. Copyright 2000 The Association for the Study of Animal Behaviour.     

The evolution of mate choice and the potential for conflict between species and mate-quality recognition

Understanding how individuals select mates becomes complex when high-quality conspecifics resemble heterospecifics. Individuals facing such a situation may be unable to effectively identify both conspecifics (species recognition) and high-quality mates that can confer fitness benefits to the choosy individual or its offspring (mate-quality recognition). Here I suggest when a conflict may occur between species and mate-quality recognition, discuss the evolutionary consequences stemming from this conflict, and present a model of mate-preference evolution in response to heterospecifics. Determining how species and mate-quality recognition interact to shape mate-choice decisions is important for understanding the diversification of sexually selected traits among closely related taxonomic groups, the use of complex sensory systems for detecting mates, and seemingly inappropriate mate-choice decisions.     

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.     

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.     

Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study

When interactions with heterospecifics prevent females from identifying conspecific mates, natural selection can promote the evolution of mating behaviours that minimize such interactions. Consequently, mating behaviours may diverge among conspecific populations in sympatry and in allopatry with heterospecifics. This divergence in conspecific mating behaviours-reproductive character displacement-can initiate speciation if mating behaviours become so divergent as to generate reproductive isolation between sympatric and allopatric conspecifics. We tested these ideas by using artificial neural networks to simulate the evolution of conspecific mate recognition in populations sympatric and allopatric with different heterospecifics. We found that advertisement calls diverged among the different conspecific populations. Consequently, networks strongly preferred calls from their own population to those from foreign conspecific populations. Thus, reproductive character displacement may promote reproductive isolation and, ultimately, speciation among conspecific populations.     

Testing the heterospecific attraction hypothesis with time-series data on species co-occurrence

The distributional patterns of actively moving animals are influenced by the cues that the individuals use for choosing sites into which they settle. Individuals may gather information about habitat quality using two types of strategies, either directly assessing the relevant environmental factors, or using the presence of conspecifics or heterospecifics as an indirect measure of habitat quality. We examined patterns of heterospecific attraction with observational time-series data on a community of seven waterbird species breeding in artificial irrigation ponds. We fitted to the data a multivariate logistic regression model, which attributes the presence–absence of each species to a set of environmental and spatial covariates, to the presence of con- and heterospecifics in the previous year and to the presence of heterospecifics in the same year. All species showed a clear tendency to continue breeding in the same sites where they were observed in the previous year. Additionally, the presence of heterospecifics, both in the previous year and in the same year, generally increased the probability that the focal species was found breeding on a given pond. Our data thus give support for the heterospecific attraction hypothesis, though causal inference should be confirmed with manipulative experiments.     

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     

A password for species recognition in a brood-parasitic bird

Recognition of conspecifics is an essential precursor of sexual reproduction. Most mammals and birds learn salient features of their parents or siblings early in ontogeny and later recognize individuals whose phenotypes match the mental image (template) of relatives closely enough as conspecifics. However, the young of brood parasites are reared among heterospecifics, so social learning will yield inappropriate species recognition templates. Initially, it was inferred that conspecific recognition in brood parasites depended on genetically determined templates. More recently it was demonstrated that learning plays a critical role in the development of parasites' social preferences. Here we propose a mechanism that accommodates the interaction of learned and genetic components of recognition. We suggest that conspecific recognition is initiated when a young parasite encounters some unique species-specific signal or "password" (e.g. a vocalization, behaviour or other characteristic) that triggers learning of additional aspects of the password-giver's phenotype. We examined the possibility that nestlings of the obligately brood-parasitic brown-headed cowbird (Molothrus ater) could use a species-specific vocalization, the "chatter", as a password. We found that six-day-old nestlings responded (begged) significantly more frequently to playbacks of chatters than to other avian sounds and that two-month-old fledglings approached playbacks of chatters more quickly than vocalizations of heterospecifics. Free-living cowbird fledglings and adults also approached playbacks of chatters more often than control sounds. Passwords may be involved in the ontogeny of species recognition in brood parasites generally.     

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.