Surface glycoproteins in copepods: potential signals for mate recognition

The mechanism male copepods use to recognize mates is not well understood. Both chemical and mechanical cues have been implicated, but the relative importance of these is not known. This lack of knowledge is despite the belief that mate recognition has a critical role in maintaining reproductive isolation of many species and influences the direction of evolution. Glycoproteins are used as mating signals by a number of aquatic organisms including rotifers, ciliates, and algae. We have developed techniques for selectively probing surface glycoproteins in zooplankton using fluorescently labeled lectins. We examined surface glycoproteins on the urosomes of several species of marine and freshwater copepods to develop insight into their role in mate recognition. Calanoids Labidocera aestiva, Centropages hamatus, and Acartia tonsa were collected in the northern Gulf of Mexico and screened with 12 lectins representing a wide variety of carbohydrate affinities. The harpacticoid Coulana sp. originally collected from Florida was screened for the same 12 lectins. The freshwater calanoid Skistodiaptomus pygmaeus and the cyclopoid Mesocyclops edax also were investigated and compared to the marine species. The sites of lectin binding were consistent across species. Most fluorescence was observed in the urosome at the caudal rami, gonopore, margin of the genital segment, and urosome segment junctions. The signal contrast (signal/background ratio) along the urosome ranged from 3–51 which seems ample for males to discriminate a glycoprotein signal from noise. Our observations clearly demonstrate that glycoproteins on the urosome of females from all six species are present at sites expected to be important in mate recognition.     

Character displacement from the receiver's perspective: species and mate recognition despite convergent signals in suboscine birds

Many social animals use long-distance signals to attract mates and defend territories. They face the twin challenges of discriminating between species to identify conspecific mates, and between individuals to recognize collaborators and competitors. It is therefore often assumed that long-distance signals are under strong selection for species-specificity and individual distinctiveness, and that this will drive character displacement when closely related species meet, particularly in noisy environments. However, the occurrence of signal stereotypy and convergence in rainforest species seems to contradict these ideas, and raises the question of whether receivers in these systems can recognize species or individuals by long-distance signals alone. Here, we test for acoustically mediated recognition in two sympatric antbird species that are known to have convergent songs. We show that male songs are stereotyped yet individually distinctive, and we use playback experiments to demonstrate that females can discriminate not only between conspecific and heterospecific males, but between mates and strangers. These findings provide clear evidence that stereotypy and convergence in male signals can be accommodated by fine tuning of perceptual abilities in female receivers, suggesting that the evolutionary forces driving divergent character displacement in animal signals are weaker than is typically assumed.     

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.     

Generalization of predator recognition:Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

<正> Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk ofpredation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by thepredator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respondweakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarelyencountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, mostelapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvetgecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays generalisedanti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the behaviourof velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnalgolden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in trialsinvolving unscented cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemiaspischemicals, 50% and 63% of geckos spent long time periods ( 3 min) freezing whilst pressed flat against the substrate, respectively.Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Cacophis(67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our resultssupport the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes.Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar,dangerous predators [Current Zoology 56 (3): 337-342, 2010].     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

Postcrania and the specific mate recognition system

The Recognition Concept of Species is examined for its potential usefulness in discriminating speciation events in the hominid fossil record. Controversies over species-specific characteristics amongHomo erectus and archaicHomo sapiens have centred on traits of the skull, largely because this element is most commonly preserved. Modern humans have an intuitive knowledge of their own Specific Mate Recognition System (SMRS), and therefore have the opportunity to compare their own SMRS to that of fossil hominids and the extent pongids. Such comparison suggests that our own skeletal SMRS may depend less on features of the skull than on the morphology of the postcranial anatomy. We propose that these components be further examined in this regard. We tentatively conclude that examination of the Recognition Concept of Species indicates that from lateHomo erectus onwards, the same SMRS has been shared in common by all hominids, including modernHomo sapiens. This suggests that, following the SMRS criterion, none of these forms can be categorized as separate species.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Variation in mate recognition specificities among four Callosobruchus seed beetles

Differentiation of mate recognition systems is one of the important steps for speciation in animals. For some insects, a contact sex pheromone present on the cuticular surface is indispensable in discriminating reproductive partners. In Callosobruchus species (Coleoptera: Chrysomelidae: Bruchinae), contact sex pheromones have been found in two species, Callosobruchus chinensis (L.) and Callosobruchus maculatus (Fabricius). It was suggested, however, that these two species lacked the ability to discriminate their conspecific and/or heterosexual partners. To elucidate this inconsistency, we verified the existence of contact sex pheromones from two other species, Callosobruchus rhodesianus (Pic) and Callosobruchus analis (Fabricius). As a result, unlike C. chinensis and C. maculatus, the males of C. rhodesianus and C. analis were able to discriminate their heterosexual partners. Comparing cross‐copulation behavior, i.e., copulation behavior between two species, against these four species indicated that the mate recognition specificities were quite different. Males of C. rhodesianus and C. analis had highly species‐specific mating behavior, whereas males of C. chinensis and C. maculatus were much less specific. These results indicate that variation in mate recognition can arise even among congeneric species living in a sympatric environment, and this variation might have arisen during species differentiation. Based on our results in combination with previous reports on interspecific competition, we suggest that the observed asymmetric cross‐copulation behavior might be, at least partially, an adaptation for surviving interspecific competition.     

Female differential allocation in response to extrapair offspring and social mate attractiveness

Renewed debate over what benefits females might gain from producing extra‐pair offspring emphasizes the possibility that apparent differences in quality between within‐pair and extra‐pair offspring are confounded by greater maternal investment in extra‐pair offspring. Moreover, the attractiveness of a female''s social mate can also influence contributions of both partners to a reproductive attempt. Here, we explore the complexities involved in parental investment decisions in response to extra‐pair offspring and mate attractiveness with a focus on the female point of view. Adult zebra finches paired and reproduced in a colony setting. A male''s early‐life diet quality and his extra‐pair reproductive success were used as metrics of his mating attractiveness. Females paired with males that achieved extra‐pair success laid heavier eggs than other females and spent less time attending their nests than their mates or other females. Extra‐pair nestlings were fed more protein‐rich hen''s egg than within‐pair nestlings. Females producing extra‐pair offspring had more surviving sons than females producing only within‐pair offspring. Collectively, results show that females differentially allocate resources in response to offspring extra‐pair status and their social mate''s attractiveness. Females may also obtain fitness benefits through the production of extra‐pair offspring.     

Fruit fly behavior in response to chemosensory signals

An important question in contemporary sensory neuroscience is how animals perceive their environment and make appropriate behavioral choices based on chemical perceptions. The fruit fly Drosophila melanogaster exhibits robust tastant and odor-evoked behaviors. Understanding how the gustatory and olfactory systems support the perception of these contact and volatile chemicals and translate them into appropriate attraction or avoidance behaviors has made an unprecedented contribution to our knowledge of the organization of chemosensory systems. In this review, I begin by describing the receptors and signaling mechanisms of the Drosophila gustatory and olfactory systems and then highlight their involvement in the control of simple and complex behaviors. The topics addressed include feeding behavior, learning and memory, navigation behavior, neuropeptide modulation of chemosensory behavior, and I conclude with a discussion of recent work that provides insight into pheromone signaling pathways.     

A cognitive framework for mate choice and species recognition

Mating decisions contribute to both the fitness of individuals and the emergence of evolutionary diversity, yet little is known about their cognitive architecture. We propose a simple model that describes how preferences are translated into decisions and how seemingly disparate patterns of preference can emerge from a single perceptual process. The model proposes that females use error-prone estimates of attractiveness to select mates based on a simple decision rule: choose the most attractive available male that exceeds some minimal criterion. We test the model in the tungara frog, a well-characterized species with an apparent dissociation between mechanisms of mate choice and species recognition. As suggested by our model results, we find that a mate attraction feature alters assessments of species status. Next, we compare female preferences in one-choice and two-choice tests, contexts thought to emphasize species recognition and mate choice, respectively. To do so, we use the model to generate maximum-likelihood estimators of preference strengths from empirical data. We find that a single representation of preferences is sufficient to explain response probabilities in both contexts across a wide range of stimuli. In this species, mate choice and species recognition are accurately and simply summarized by our model. While the findings resolve long-standing anomalies, they also illustrate how models of choice can bridge theoretical and empirical treatments of animal decisions. The data demonstrate a remarkable congruity of perceptual processes across contexts, tasks, and taxa.     

Signalling components of the house mouse mate recognition system

Subspecies-specific mate recognition may represent significant barrier to gene flow between diverged genomes potentially leading to speciation. In the house mouse, assortative mating involves the coevolution of several signals and receptors. We compared signalling ability of bedding material, faeces, urine, saliva, salivary androgen binding proteins (ABP) and combinations of urine with saliva and urine with ABP in mate choice in two wild-derived inbred strains (one of Mus musculus musculus and one of Mus musculus domesticus origin). We observed high levels of variation in assortative preferences between the two strains and sexes. The strongest preferences were observed in M. m. musculus-derived individuals in tests where urine was present either alone or as part of a composite signal target. M. m. domesticus-derived mice displayed strain-specific preferences for faeces. Saliva was the least preferred stimulus in both strains and sexes. No effect of two-compound cues was detected. We conclude that there is divergence across both the stimulus and preference parts of the recognition system for both house mouse strains. Of the tested stimuli, those that have the capacity to carry a signal for extended periods under natural conditions (such as urine and faeces) seem to be the most important substances in strain-specific recognition.     

Evolutionary experiments on mate recognition in the Drosophila serrata species complex

It is becoming increasingly apparent that at least some aspects of the evolution of mate recognition may be amenable to manipulation in evolutionary experiments. Quantitative genetic analyses that focus on the genetic consequences of evolutionary processes that result in mate recognition evolution may eventually provide an understanding of the genetic basis of the process of speciation. We review a series of experiments that have attempted to determine the genetic basis of the response to natural and sexual selection on mate recognition in the Drosophila serrata species complex. The genetic basis of mate recognition has been investigated at three levels: (1) between the species of D. serrata and D. birchii using interspecific hybrids, (2) between populations of D. serrata that are sympatric and allopatric with respect to D. birchii, and (3) within populations of D. serrata. These experiments suggest that it may be possible to use evolutionary experiments to observe important events such as the reinforcement of mate recognition, or the generation of the genetic associations that are central to many sexual selection models.     

The inheritance of female preference functions in a mate recognition system

Mate recognition systems (MRSs) play a major role in sexual selection and speciation, yet few studies have analysed both male and female components in detail. Here, female preference functions have been characterized for the tettigoniid bushcricket Ephippiger ephippiger, and the inheritance of male song and female preference functions followed in crosses between subspecies. Songs are disproportionately determined by sex-linked genes. However, there is no evidence for a role of maternally derived sex-linked genes in female preference or of maternal effects. At the genetic level, there is a mismatch between peak preferences and male song, consistent with an evolutionary history of persistent directional preferences. Such a pattern of inheritance could contribute to the process of speciation via the evolution of new MRSs.     

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.