The Computational Mechanisms of Mate Choice

In many species, mating signals encode information important for both species recognition and mate quality assessment. I investigate how the computational mechanisms used by females to integrate the two sources of information can affect their mating decisions. First, I present a sequential analysis model of decision making based on a two‐component signal, in which the first component encodes information important for mate quality assessment and the second component for species recognition. When the components interact additively, the ability of females to discriminate between signals that differ in only the component important for mate‐quality assessment is the same independently of the value of the species‐recognition component. In contrast, when the components interact multiplicatively, discrimination in mate quality depends also on the species‐recognition component, which can either amplify or attenuate the perceived differences in mate quality. In the second part of the paper, I show results of a two‐choice phonotaxis experiment on female Italian treefrogs, Hyla intermedia, that confirm the model predictions by showing that directional preferences for call rate (important for mate‐quality assessment) are stronger when pulse‐rate and fundamental frequency (important for species recognition) are close to the preferred population mean than when they are either higher or lower than the mean.     

Computational mate choice: theory and empirical evidence

The present review is based on the thesis that mate choice results from information-processing mechanisms governed by computational rules and that, to understand how females choose their mates, we should identify which are the sources of information and how they are used to make decisions. We describe mate choice as a three-step computational process and for each step we present theories and review empirical evidence. The first step is a perceptual process. It describes the acquisition of evidence, that is, how females use multiple cues and signals to assign an attractiveness value to prospective mates (the preference function hypothesis). The second step is a decisional process. It describes the construction of the decision variable (DV), which integrates evidence (private information by direct assessment), priors (public information), and value (perceived utility) of prospective mates into a quantity that is used by a decision rule (DR) to produce a choice. We make the assumption that females are optimal Bayesian decision makers and we derive a formal model of DV that can explain the effects of preference functions, mate copying, social context, and females' state and condition on the patterns of mate choice. The third step of mating decision is a deliberative process that depends on the DRs. We identify two main categories of DRs (absolute and comparative rules), and review the normative models of mate sampling tactics associated to them. We highlight the limits of the normative approach and present a class of computational models (sequential-sampling models) that are based on the assumption that DVs accumulate noisy evidence over time until a decision threshold is reached. These models force us to rethink the dichotomy between comparative and absolute decision rules, between discrimination and recognition, and even between rational and irrational choice. Since they have a robust biological basis, we think they may represent a useful theoretical tool for behavioural ecologist interested in integrating proximate and ultimate causes of mate choice.     

Reproductive interference via display signals: the challenge of multiple receivers

Sexually selected traits important in both mate and competitor recognition provide an opportunity to understand the tradeoffs associated with reproductive and competitive interference. When co-occurring species compete over similar resources, selection may promote signal similarity to facilitate competitive interactions in opposition to selection for signal divergence to maintain assortative mating. Bird song provides a classic example of contrasting selection on signal design, because songs function both in mate discrimination and in territorial advertisement. Similarity in songs aids competitor recognition both within and across species, and song convergence or mixing is widespread in the songbirds. Two related mechanisms can maintain mate recognition in the face of song convergence. First, multiple recognition signals, both across and within signaling modalities, provide a basis for mate and competitor discrimination using different sets of cues. Second, stricter female song preferences may allow interspecific male–male competitive communication without compromising female mate discrimination. I suggest that increased understanding of the neurobiology underlying song recognition will provide insight into the relative importance and prevalence of these different mechanisms along a continuum of species divergence.     

REPRODUCTIVE CHARACTER DISPLACEMENT OF EPICUTICULAR COMPOUNDS AND THEIR CONTRIBUTION TO MATE CHOICE IN DROSOPHILA SUBQUINARIA AND DROSOPHILA RECENS

Interactions between species can alter selection on sexual displays used in mate choice within species. Here we study the epicuticular pheromones of two Drosophila species that overlap partially in geographic range and are incompletely reproductively isolated. Drosophila subquinaria shows a pattern of reproductive character displacement against Drosophila recens, and partial behavioral isolation between conspecific sympatric versus allopatric populations, whereas D. recens shows no such variation in mate choice. First, using manipulative perfuming experiments, we show that females use pheromones as signals for mate discrimination both between species and among populations of D. subquinaria. Second, we show that patterns of variation in epicuticular compounds, both across populations and between species, are consistent with those previously shown for mating probabilities: pheromone compositions differ between populations of D. subquinaria that are allopatric versus sympatric with D. recens, but are similar across populations of D. recens regardless of overlap with D. subquinaria. We also identify differences in pheromone composition among allopatric regions of D. subquinaria. In sum, our results suggest that epicuticular compounds are key signals used by females during mate recognition, and that these traits have diverged among D. subquinaria populations in response to reinforcing selection generated by the presence of D. recens.     

Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens

Most animal species use distinctive courship patterns to choose among potential mates. Over time, the sensory signaling and preferences used during courtship can diverge among groups that are reproductively isolated. This divergence of signal traits and preferences is thought to be an important cause of behavioral isolation during the speciation process. Here, we examine the sensory modalities used in courtship by two closely related species, Drosophila subquinaria and Drosophila recens, which overlap in geographic range and are incompletely reproductively isolated. We use observational studies of courtship patterns and manipulation of male and female sensory modalities to determine the relative roles of visual, olfactory, gustatory, and auditory signals during conspecific mate choice. We find that sex‐specific, species‐specific, and population‐specific cues are used during mate acquisition within populations of D. subquinaria and D. recens. We identify shifts in both male and female sensory modalities between species, and also between populations of D. subquinaria. Our results indicate that divergence in mating signals and preferences have occurred on a relatively short timescale within and between these species. Finally, we suggest that because olfactory cues are essential for D. subquinaria females to mate within species, they may also underlie variation in behavioral discrimination across populations and species.     

Reinforcement and learning

Evidence has been accumulating to support the process of reinforcement as a potential mechanism in speciation. In many species, mate choice decisions are influenced by cultural factors, including learned mating preferences (sexual imprinting) or learned mate attraction signals (e.g., bird song). It has been postulated that learning can have a strong impact on the likelihood of speciation and perhaps on the process of reinforcement, but no models have explicitly considered learning in a reinforcement context. We review the evidence that suggests that learning may be involved in speciation and reinforcement, and present a model of reinforcement via learned preferences. We show that not only can reinforcement occur when preferences are learned by imprinting, but that such preferences can maintain species differences easily in comparison with both autosomal and sex-linked genetically inherited preferences. We highlight the need for more explicit study of the connection between the behavioral process of learning and the evolutionary process of reinforcement in natural systems.     

Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): implications for mate choice and the evolution of communication systems

Signals used for mate choice and receiver preferences are often assumed to coevolve in a lock-step fashion. However, sender-receiver coevolution can also be nonparallel: even if species differences in signals are mainly quantitative, females of some closely related species have qualitatively different preferences and underlying mechanisms. Two-alternative playback experiments using synthetic calls that differed in fine-scale temporal properties identified the receiver criteria in females of the treefrog Hyla chrysoscelis for comparison with female criteria in a cryptic tetraploid species (H. versicolor); detailed preference functions were also generated for both species based on natural patterns of variation in temporal properties. The species were similar in three respects: (1) pulses of constant frequency were as attractive as the frequency-modulated pulses typical of conspecific calls; (2) changes in preferences with temperature paralleled temperature-dependent changes in male calls; and (3) preference functions were unimodal, with weakly defined peaks estimated at values slightly higher than the estimated means in conspecific calls. There were also species differences: (1) preference function slopes were steeper in H. chrysoscelis than in H. versicolor; (2) preferences were more intensity independent in H. chrysoscelis than in H. versicolor; (3) a synergistic effect of differences in pulse rate and shape on preference strength occurred in H. versicolor but not in H. chrysoscelis; and (4) a preference for the pulse shape typical of conspecific calls was expressed at the species-typical pulse duration in H. versicolor but not in H. chrysoscelis. However, females of H. chrysoscelis did express a preference based on pulse shape when tested with longer-than-average pulses, suggesting a hypothesis that could account for some examples of nonparallel coevolution. Namely, preferences can be hidden or revealed depending on the direction of quantitative change in a signal property relative to the threshold for resolving differences in that property. The results of the experiments reported here also predict patterns of mate choice within and between contemporary populations. First, intraspecific mate choice in both species is expected to be strongly influenced by variation in temperature among calling males. Second, simultaneous differences in pulse rate and pulse shape are required for effective species discrimination by females of H. versicolor but not by females of H. chrysoscelis. Third, there is greater potential for sexual selection within populations and for discrimination against calls produced by males in other geographically remote populations in H. chrysoscelis than in H. versicolor.     

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences

Sexual selection of high-quality mates can conflict with species recognition if traits that govern intraspecific mate preferences also influence interspecific recognition. This conflict might be resolved by developmental plasticity and learned mate preferences, which could drive preference divergence in populations that differ in local species composition. We integrate field and laboratory experiments on two calopterygid damselfly species with population genetic data to investigate how sex differences in developmental plasticity affect population divergence in the face of gene flow. Whereas male species recognition is fixed at emergence, females instead learn to recognize heterospecifics. Females are therefore more plastic in their mate preferences than males. We suggest that this results from sex differences in the balance between sexual selection for high-quality mates and selection for species recognition. As a result of these sex differences, females develop more pronounced population divergence in their mate preferences compared with males. Local ecological community context and presence of heterospecifics in combination with sex differences in plasticity and canalization therefore shape population divergence in mate preferences. As ongoing environmental change and habitat fragmentation bring formerly allopatric species into secondary contact, developmental plasticity of mate preferences in either or both sexes might facilitate coexistence and prevent local species extinction.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

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.     

The role of chemical communication in mate choice

Chemical signals are omnipresent in sexual communication in the vast majority of living organisms. The traditional paradigm was that their main purpose in sexual behaviour was to coordinate mate and species recognition and thus pheromones were conserved in structure and function. In recent years, this view has been challenged by theoretical analyses on the evolution of pheromones and empirical reports of mate choice based on chemical signals. The ability to measure precisely the quantity and quality of chemicals emitted by single individuals has also revealed considerable individual variation in chemical composition and release rates, and there is mounting evidence that prospecting mates respond to this variation. Here, we review the evidence for pheromones as indicators of mate quality and examine the extent of their use in individual mate assessment. We begin by briefly defining the levels of mate choice--species recognition, mate recognition and mate assessment. We then explore the degree to which pheromones satisfy the key criteria necessary for their evolution and maintenance as cues in mate assessment; that is, they should exhibit variation across individuals within a sex and species; they should honestly reflect an individual's quality and thus be costly to produce and/or maintain; they should display relatively high levels of heritability. There is now substantial empirical evidence that pheromones can satisfy all these criteria and, while measurements of the actual metabolic cost of pheromone production remain to some degree lacking, trade-offs between pheromone production and various fitness-related characters such as growth rate, immunocompetence and longevity have been reported for a range of species. In the penultimate section, we outline the growing number of studies where the consequences of chemical-based mate assessment have been investigated, specifically focussing on the reported direct and genetic benefits accrued by the receiver. Finally, we highlight potential areas for future research and in particular emphasise the need for interdisciplinary research that combines exploration of chemical, physiological and behavioural processes to further our understanding of the role of chemical cues in mate assessment.     

Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process

Zebra finches are monogamous birds living in large assemblies, which represent a source of confusion for recognition between mates. Because the members of a pair use distance calls to remain in contact, call-based mate recognition is highly probable in this species. Whereas it had been previously demonstrated in males [Vignal, C., Mathevon, N., Mottin, S., 2004. Audience drives male songbird response to mate's voice. Nature 430, 448-451], call-based mate recognition remained to be shown in females. By analysing the acoustic structure of male calls, we investigated the existence of an individual signature and identified the involved acoustic cues. We tested to see if females can identify their mates on the basis of their calls alone, and performed preliminary experiments using modified signals to investigate the acoustic basis of this recognition. Playback tests carried on six individuals showed that a female zebra finch is able to perform the call-based recognition of its mate. Our experiments suggested that the female uses both the energy spectrum and the frequency modulation of the male signal. More experiments are now needed to decipher precisely which acoustic cues are used by females for recognition.     

The evolution of female preferences for multiple indicators of quality

In a variety of species, females exhibit preferences for multiple male ornaments. Several hypotheses have been proposed to explain this phenomenon. Which, if any, of these hypotheses is the most plausible in general remains largely unresolved based on the available empirical data. Yet theoretical studies conclude that the evolution of preferences for multiple signals of male quality is unlikely, especially when the use of an additional cue in mate choice strongly increases the overall cost of choice. This would imply that most male courtship characters do not reflect the male's genetic quality but instead evolved through Fisherian sexual selection. However, the existing models focus on ornaments that signal overall genetic quality and do not address the possibility that different ornaments provide information about different aspects of quality. Therefore, we develop a model in which the ornaments act as signals for distinct quality components. When the ornaments provide overlapping information about these quality components, we retrieve the results of earlier models. However, when the ornaments provide independent information, preferences for multiple ornaments may evolve, even when exhibiting multiple preferences is costly. We discuss our results in relation to the multiple-message and redundant-signal hypotheses for ornament diversity and identify parallels between Fisherian and good-genes mechanisms for the evolution of multiple ornaments.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

Generalization and the evolution of symmetry preferences

Biological displays are often symmetrical, and there is growing evidence that receivers are sensitive to these symmetries. One explanation for the evolution of such sensitivity is that symmetry reflects the quality of the signaller. An alternative is that the sensitivity may arise as a by-product of general properties of biological recognition systems. In line with the latter idea, simulations of the recognition process based on simple, artificial neural networks have suggested that generalization can give rise to preferences for particular symmetrical stimuli. However, it is not clear from these studies exactly how the preferences emerge, and to what extent the results are relevant to biological recognition systems. Here, we employ a different class of recognition models (gradient interaction models) to demonstrate more clearly how generalization can generate a preference for symmetrical variants of a display. We also point out that the predictions of the gradient interaction and network-based models regarding the effects of generalization closely match the results from empirical studies of stimulus control. Our analysis demonstrates that the effects of generalization cannot be ignored when studying the evolution of symmetry preferences and symmetric signals.     

Interspecific genetics of mate recognition: inheritance of female acoustic preference in Hawaiian crickets

Abstract. Female mating behavior plays a fundamental role in the divergent evolution of mate recognition systems that may lead to speciation. Despite this important role, the phenotypic and genetic bases of female mating behavior remain poorly understood. In this study, I examine the shape of the female acoustic preference function and estimate values for pulse rate preference in two species of Hawaiian crickets, Laupala kohalensis and L. paranigra . In addition, I examine how preference differences are inherited in hybrid crosses between these species. Females expressed unimodal preference functions and were generally more attracted to pulse rates characterizing their own species. Unimodal preference functions also characterized F1 and backcross generations, with hybrid females expressing preferences for intermediate pulse rates. Pulse rate preferences segregated in the backcross generation. Mean pulse rate preference matched mean pulse rate in both parental and hybrid generations. Based on F1 hybrids and segregation patterns in backcross females, I show that changes in both signal and receiver components of the mate recognition system are consistent with a multilocus model of change through incremental steps. The results therefore suggest that ancestors of the current species also expressed unimodal preference functions and that changes in acoustic communication signals occurred through shifts in mean pulse rates and pulse rate preferences among populations.     

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.     

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     

Parental preferences for the facial traits of their offspring's partners can enhance parental inclusive fitness

Physical appearance provides a wealth of information concerning an individual's biological fitness and reproductive quality, but we do not know whether parents make use of this information when evaluating potential partners for their offspring. This is critical to our understanding of human mate choice, because parents frequently influence their offspring's mating decisions, either directly, for instance through arranged marriages, or indirectly, through manipulating their offspring's partner choice. Here, we used facial images that varied in attractiveness, masculinity, health, and symmetry to assess both reproductively-aged daughters' and their parents' preferences in potential mates for the daughters. In line with our predictions, both daughters and their parents had clear preferences for markers of genetic quality, although the daughters showed significantly stronger preferences for these markers than their parents. Contrary to previous research, parents and daughters did not have stronger preferences for markers of genetic quality if they perceived the daughter to be more attractive. Parents' preferences for the facial markers of genetic quality in their offspring's partner may help maximize inclusive fitness.     

Female Preferences for Male Song Characters in the Bush-Cricket Isophya camptoxypha (Orthoptera, Tettigonioidea)

Female preferences for two male song characters (duration of syllables [DS], syllable repetition period [SRP]) have been studied in Isophya camptoxypha, an Eastern European duetting bush-cricket. Songs with modified DS or SRP were presented to virgin females and their response songs were recorded and counted. Female preference functions were unimodal for both characters. But while in the case of SRP the obtained female preference function reached its maximum at the mean value of that character, in the case of DS females preferred modified songs with a DS slightly higher than the natural range of that character. A comparison between the obtained preference functions and the DS and SRP values measured in sympatric Isophya species (with similar song structure) suggests that the two examined characters and female preferences for them may be effective components of the species-specific mate recognition system of I. camptoxypha. Moreover DS values may also convey information about the quality of the singing male.