Multiple cues in mate selection: The sexual interference hypothesis

Animals use multiple cues when choosing mates, but it is not yet clear why a single signal would not suffice. In this paper, drawing support from predation and “noise” effects on mate choice, marketing economics, and multiple signals models, a new hypothesis explaining multiple sexual signals is proposed: the sexual interference hypothesis. The hypothesis is based on three well-supported premises: (1) selectivity decreases when mate assessment costs increase, (2) assessment costs increase when the propagation or reception of sexual signals is more difficult, and (3) males not only exploit such circumstances by courting females when choice is more difficult, but actively interfere with females' preferences by making choice more difficult. The hypothesis argues that additional sexual signals evolve as a way for males to hinder female mate choice by interfering with the propagation and reception of other males' sexual signals. Females respond by evolving the ability to glean meaningful information from signals despite males' attempts at obfuscation. In turn, males respond by producing better interference signals and signals that are not so easily blocked. This co-evolutionary process increases the costs of assessment for females and the costs of signal production for males, and leads to a temporary equilibrium of honest advertising via multiple signals.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as ‘Fisherian runaway’. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

Precopulatory choice for cues of material benefits in tree crickets

The relative importance of direct and indirect benefits modelsof mate choice is a central question in sexual selection, butseparating the two models is very difficult because high qualitymales often provide both better direct benefits and better genes.In tree crickets, Oecanthus nigricornis, females have the opportunityto gain both directly and indirectly from mate choice. Femaletree crickets exercise premating choice for large males, butthe model underlying this choice is unknown. In this study weexamine the proximate cues used by female tree crickets to rejectmales, and show that the ability of males to provide food isa central cue. In contrast, we find no evidence that the relativesize of mates is important in mate rejection. The fact thatthe major phenotypic cues of male quality are related to foodprovisioning suggests that the role of genetic benefits in shapingfemale preferences is limited by the extent to which food provisioningsignals genetic quality.     

Conflicting preferences within females: sexual selection versus species recognition

Preferences for mates within and between species are often harmonious, as traits that females prefer are usually more developed in conspecifics than heterospecifics. This need not be the case, however. When it is not, conflict between these arenas of mate choice can be resolved if females attend to different cues for each task. But this raises the potential for correlations among preferences to limit the opportunity for these two processes to operate independently. Here, we show that, within individual female pygmy swordtails (Xiphophorus pygmaeus), directional preferences for conspicuous ornamentation are inversely associated with discrimination against a sympatric heterospecific, Xiphophorus cortezi. Thus, mate choice among and within species need not be separate, independent processes; instead, they can be mechanistically intertwined. As a consequence, different arenas of mate choice can constrain one another, even when females assess multiple cues.     

Mate preference for multiple cues: interplay between male and nest size in the sand goby, Pomatoschistus minutus

Female mating preferences are often based on more than one cue.In empirical studies, however, different mate choice cues aretypically treated separately ignoring their possible interactions.In the current work, we studied how male body size and sizeof the male's nest jointly affect mate preferences of femalesand gobies, Pomatoschistus minutus. The females were givena binary choice between males that differed either in body sizeor size of their nest or both. We found that neither body sizenor size of the nest alone affected male attractiveness, buttogether these 2 cues had a significant effect. Specifically,large males were more popular among females when they had alarge nest than when they occupied a small nest. The resultssuggest that if interaction effects between multiple mate choicecues are not considered, there is a danger of ignoring or underestimatingthe importance of these cues in sexual selection by female choice.     

PERSPECTIVE: INDIRECT MATE CHOICE,COMPETITION FOR MATES,AND COEVOLUTION OF THE SEXES

When Darwin first proposed the possibility of sexual selection, he identified two mechanisms, male competition for mates and female choice of mates. Extending this classification, we distinguish two forms of mate choice, direct and indirect. This distinction clarifies the relationship between Darwin's two mechanisms and, furthermore, indicates that the potential scope for sexual selection is much wider than thus far realized. Direct mate choice, the focus of most research on sexual selection in recent decades, requires discrimination between attributes of individuals of the opposite sex. Indirect mate choice includes all other behavior or morphology that restricts an individual's set of potential mates. Possibilities for indirect mate choice include advertisement of fertility or copulation, evasive behavior, aggregation or synchronization with other individuals of the same sex, and preferences for mating in particular locations. In each of these cases, indirect mate choice sets the conditions for competition among individuals of the opposite sex and increases the chances of mating with a successful competitor. Like direct mate choice, indirect mate choice produces assortative mating. As a consequence, the genetic correlation between alleles affecting indirect choice and those affecting success in competition for mates can produce self-accelerating evolution of these complementary features of the sexes. The broad possibilities for indirect mate choice indicate that sexual selection has more pervasive influences on the coevolution of male and female characteristics than previously realized.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES

The aim of this review is to consider variation in mating p among females. We define mating p as the sensory and behavioural properties that influence the propensity of individuals to mate with certain phenotypes. Two properties of mating p can be distinguished: (i) ‘preference functions’–the order with which an individual ranks prospective mates and (2)‘choosiness’ -the effort an individual is prepared to invest in mate assessment. Patterns of mate choices can be altered by changing the costs of choosiness without altering the preference function. We discuss why it is important to study variation in female mating behaviour and identify five main areas of interest: Variation in mating p and costs of choosiness could (i) influence the rate and direction of evolution by sexual selection, (2) provide information about the evolutionary history of female p, (3) help explain inter-specific differences in the evolution of secondary sexual characteristics, (4) provide information about the level of benefits gained from mate choice, (5) provide information about the underlying mechanisms of mate choice. Variation in mate choice could be due to variability in preference functions, degree of choosiness, or both, and may arise due to genetic differences, developmental trajectories or proximate environmental factors. We review the evidence for genetic variation from genetic studies of heritability and also from data on the repeatability of mate-choice decisions (which can provide information about the upper limits to heritability). There can be problems in interpreting patterns of mate choice in terms of variation in mating p and we illustrate two main points. First, some factors can lead to mate choice patterns that mimic heritable variation in p and secondly other factors may obscure heritable p. These factors are divided into three overlapping classes, environmental, social and the effect of the female phenotype. The environmental factors discussed include predation risk and the costs of sampling; the social factors discussed include the effect of male–male interactions as well as female competition. We review the literature which presents data on how females sample males and discuss the number of cues females use. We conclude that sexual-selection studies have paid far less attention to variation among females than to variation among males, and that there is still much to learn about how females choose males and why different females make different choices. We suggest a number of possible lines for future research.     

Multimodal signalling in the North American barn swallow: a phenotype network approach

Complex signals, involving multiple components within and across modalities, are common in animal communication. However, decomposing complex signals into traits and their interactions remains a fundamental challenge for studies of phenotype evolution. We apply a novel phenotype network approach for studying complex signal evolution in the North American barn swallow (Hirundo rustica erythrogaster). We integrate model testing with correlation-based phenotype networks to infer the contributions of female mate choice and male–male competition to the evolution of barn swallow communication. Overall, the best predictors of mate choice were distinct from those for competition, while moderate functional overlap suggests males and females use some of the same traits to assess potential mates and rivals. We interpret model results in the context of a network of traits, and suggest this approach allows researchers a more nuanced view of trait clustering patterns that informs new hypotheses about the evolution of communication systems.     

Antagonistic coevolution between hosts and sexually transmitted infections

Sexually transmitted infections (STIs) are predicted to play an important role in the evolution of host mating strategies, and vice versa, yet our understanding of host-STI coevolution is limited. Previous theoretical work has shown mate choice can evolve to prevent runaway STI virulence evolution in chronic, sterilizing infections. Here, I generalize this theory to examine how a broader range of life-history traits influence coevolution; specifically, how host preferences for healthy mates and STI virulence coevolve when infections are acute and can cause mortality or sterility, and hosts do not form long-term sexual partnerships. I show that mate choice reduces both mortality and sterility virulence, with qualitatively different outcomes depending on the mode of virulence, costs associated with mate choice, recovery rates, and host lifespan. For example, fluctuating selection—a key finding in previous work—is most likely when hosts have moderate lifespans, STIs cause sterility and long infections, and costs of mate choice are low. The results reveal new insights into the coevolution of mate choice and STI virulence as different life-history traits vary, providing increased support for parasite-mediated sexual selection as a potential driver of host mate choice, and mate choice as a constraint on the evolution of virulence.     

What is driving male mate preference evolution in Jamaican field crickets?

Male mating preferences are often a neglected aspect of studies on sexual selection. Male mating preferences may evolve if they provide males with direct‐fitness benefits such as increased opportunity to fertilize more eggs or indirect‐fitness benefits such as enhanced offspring survival. We tested these ideas using Jamaican field crickets, Gryllus assimilis, previously shown to exhibit male mating preferences. We randomly mated males to either their preferred or non‐preferred potential mates and then asked whether mating treatment influenced egg oviposition or offspring viability. Preferred females were not significantly more fecund and did not produce more viable eggs or offspring than non‐preferred females. Male mate preferences were therefore inconsistent with both the direct‐ and indirect‐fitness benefits hypotheses under the conditions of our experiment. Our null results leave us with an open question about what is driving the evolution of mating preferences in male crickets. Future research should explore the whether the offspring of preferred females are more attractive, have stronger immune systems, and/or experience higher adult longevity.     

Female mate choice and male–male competition in Tonkean macaques: Who decides?

The theory of sexual selection predicts that females should be discriminatory in the choice of sexual partners. Females can express their choice in two ways. In direct mate choice, they show preferences for certain partners. In indirect mate choice, they select partners by displaying sexually attractive traits, thus eliciting contest competition between males. We focused on a primate species in which females advertise the timing of their ovulation and studied the balance between these two choice strategies. We tested predictions related to three hypotheses about direct and indirect female choice, namely the best‐male, graded‐signal and weak‐selectivity hypotheses. We investigated the sexual and agonistic interactions occurring during oestrous periods in five captive groups of Tonkean macaques (Macaca tonkeana). The results showed that dominant males used mate guarding to monopolise sexual access to parous females that were in the fertile stage of their reproductive cycle, while lower‐ranking males monitored only nulliparous females. The distribution of sexual presentations indicated that females accepted different types of partners, supporting the weak‐selectivity hypothesis regarding direct mate choice. The analysis of behavioural sequences revealed that mate‐guarding males used mild coercive behaviours to prevent females from mating with other males at conception time. The distribution of mounts showed that females mainly mated with dominant males, which leads us to argue that the best‐male hypothesis provides the most parsimonious explanation regarding indirect mate choice in Tonkean macaques. At the individual level, it may be concluded that male competitive strategies prevented females from exercising direct mate choice. At the evolutionary level, however, female sexual advertising and thus indirect choice promoted competition between males. The outcome is that indirect mate choice appears more important than direct mate choice in female Tonkean macaques.     

THE EVOLUTION OF MATE PREFERENCES FOR MULTIPLE SEXUAL ORNAMENTS

Males of many species use multiple sexual ornaments in their courtship display. We investigate the evolution of female sexual preferences for more than a single male trait by the handicap process. The handicap process assumes that ornaments are indicators of male quality, and a female benefits from mate choice by her offspring inheriting “good genes” that increase survival chances. A new handicap model is developed that allows equilibria to be given in terms of selection pressures, independent of genetic parameters. Multiple sexual preferences evolve if the overall cost of choice is not greatly increased by a female using additional male traits in her assessment of potential mates. However, only a single preference is evolutionarily stable if assessment of additional male traits greatly increases the overall cost of choice (more than expected by combining the cost of each preference independently). Any single preference can evolve, the outcome being determined by initial conditions. The evolution of one preference effectively blocks the evolution of others, even for traits that are better indicators of male quality. Comparison is made with sexual selection caused by Fisher's runaway process in which male traits are purely attractive characters. This shows that sexual preferences for multiple Fisher traits are likely to evolve alongside preference for a single handicap trait that indicates male quality. This is a general difference in the evolutionary outcome of these two causes of sexual selection.     

Environmental change mediates mate choice for an extended phenotype,but not for mate quality

Sexual cues, including extended phenotypes, are expected to be reliable indicators of male genetic quality and/or provide information on parental quality. However, the reliability of these cues may be dependent on stability of the environment, with heterogeneity affecting how selection acts on such traits. Here, we test how environmental change mediates mate choice for multiple sexual traits, including an extended phenotype–‐the structure of male‐built nests – in stickleback fish. First, we manipulated the dissolved oxygen (DO) content of water to create high or low DO environments in which male fish built nests. Then we recorded the mate choice of females encountering these males (and their nests), under either the same or reversed DO conditions. Males in high DO environments built more compact nests than those in low DO conditions and males adjusted their nest structure in response to changing conditions. Female mate choice for extended phenotype (male nests) was environmentally dependent (females chose more compact nests in high DO conditions), while female choice for male phenotype was not (females chose large, vigorous males regardless of DO level). Examining mate choice in this dynamic context suggests that females evaluate the reliability of multiple sexual cues, taking into account environmental heterogeneity.     

No Inbreeding Avoidance by Female Burying Beetles Regardless of Whether They Encounter Males Simultaneously or Sequentially

Inbreeding avoidance reduces the probability that an individual will mate with a related partner, thereby lowering the risk that it produces inbred offspring suffering from inbreeding depression. Inbreeding avoidance can occur through several mechanisms, including active mate choice, polyandry and sex‐biased dispersal. Here, we focus on the role of active mate choice as a mechanism for inbreeding avoidance. Recent evidence suggests that the experimental design used in mate choice experiments (i.e. simultaneous versus sequential choice) can have a strong impact on the strength of the reported mating preferences. In this study, we examine whether similar effects of experimental design also apply in the context of inbreeding avoidance. To this end, we designed two experiments on the burying beetle Nicrophorus vespilloides that matched two different contexts under which females encounter potential mates in the wild; that is, when females encounter males simultaneously and sequentially. We found that females were as likely to mate with related and unrelated males regardless of whether they encountered male partners simultaneously or sequentially. Thus, our study provides no evidence for inbreeding avoidance in this species, and suggests that the number of mates present did not influence the degree of inbreeding avoidance. We discuss potential explanations for the lack of inbreeding avoidance through mate choice, including lack of mechanisms for recognizing close relatives, low costs and/or low risks of inbreeding and the presence of other inbreeding avoidance mechanisms, such as sex‐biased dispersal and polyandry coupled with post‐copulatory mate choice.     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

The evolution of experience-mediated plasticity in mate preferences

Experience of sexual signals can alter mate preferences and influence the course of sexual selection. Here, we examine the patterns of experience-mediated plasticity in mate preferences that can arise in response to variation in the composition of mates in the environment. We use these patterns to test hypotheses about potential sources of selection favouring experience-mediated plasticity. We manipulated signal experience of female Enchenopa treehoppers (Hemiptera: Membracidae) in a vibrational playback experiment with the following treatments: silence; two types of non-preferred signals; preferred signals; and a mixture of preferred and non-preferred signals. This experiment revealed plasticity in mate preference selectivity, with greatest selectivity in the mixed signal treatment, followed by the preferred signal treatment. We found no plasticity in peak preference. These results suggest that females have been selected to adjust preference selectivity according to the variability of potential mates in their social environment, as well as to the presence/absence of preferred mates. We discuss how experience-mediated plasticity in mate preferences can influence the strength of selection on male signals and can result in evolutionary dynamics between variation in preferences and signals that either promote the maintenance of variation or facilitate rapid trait fixation.     

Sexual selection

Competition over mates takes many forms and has far-reaching consequences for many organisms. Recent work suggests that relative reproductive rates of males and females, sperm competition and quality variation among mates affect the strength of sexual selection. Song, other display, body size, visual ornaments and material resource offerings are often sexually selected. There is much empirical evidence of mate choice, and its evolution is clarified by mathematical models. Recent advances in theory also consider costs of choice, effects of deleterious mutations, fast and slow evolution of preferences and preferred traits, and simultaneous preferences for several traits. Contests over mates are important; so is sperm competition, scrambles, endurance rivalry, and coercion. The latter mechanisms have received less attention than mate choice. Sexual selection may explain puzzling aspects of plant pollination biology.