Sexual selection and mate choice in evolutionary psychology

The importance of mate choice and sexual selection has been emphasized by the majority of evolutionary psychologists. This paper assesses three cases of work on mate choice and sexual selection in evolutionary psychology: David Buss on cross-cultural human mate preferences, Randy Thornhill and Steve Gangestad on the link between mate preferences and fluctuating asymmetry, and Geoffrey Miller on the role of Fisher’s runaway process in human evolution. A mixture of conceptual and empirical problems in each case highlights the general weakness of work in evolutionary psychology on these issues.

Sexual selection and condition-dependent mate preferences

The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.     

Sexual imprinting in human mate choice

Animal and human studies have shown that individuals choose mates partly on the basis of similarity, a tendency referred to as homogamy. Several authors have suggested that a specific innate recognition mechanism, phenotypic matching, allows the organism to detect similar others by their resemblance to itself. However, several objections have been raised to this theory on both empirical and theoretical grounds. Here, we report that homogamy in humans is attained partly by sexual imprinting on the opposite-sex parent during childhood. We hypothesized that children fashion a mental model of their opposite-sex parent's phenotype that is used as a template for acquiring mates. To disentangle the effects of phenotypic matching and sexual imprinting, adopted daughters and their rearing families were examined. Judges found significant resemblance on facial traits between daughter's husband and her adoptive father. Furthermore, this effect may be modified by the quality of the father-daughter relationship during childhood. Daughters who received more emotional support from their adoptive father were more likely to choose mates similar to the father than those whose father provided a less positive emotional atmosphere.     

Sexual display and mate choice in an energetically costly environment

Sexual displays and mate choice often take place under the same set of environmental conditions and, as a consequence, may be exposed to the same set of environmental constraints. Surprisingly, however, very few studies consider the effects of environmental costs on sexual displays and mate choice simultaneously. We conducted an experiment, manipulating water flow in large flume tanks, to examine how an energetically costly environment might affect the sexual display and mate choice behavior of male and female guppies, Poecilia reticulata. We found that male guppies performed fewer sexual displays and became less choosy, with respect to female size, in the presence of a water current compared to those tested in still water. In contrast to males, female responsive to male displays did not differ between the water current treatments and females exhibited no mate preferences with respect to male size or coloration in either treatment. The results of our study underscore the importance of considering the simultaneous effects of environmental costs on the sexual behaviors of both sexes.     

Sexual selection in a tropical fruit fly: role of a plant derived chemical in mate choice

The specific mechanisms by which selective pressures affect individuals are often difficult to resolve. In tephritid fruit flies, males respond strongly and positively to certain plant derived chemicals. Sexual selection by female choice has been hypothesized as the mechanism driving this behaviour in certain species, as females preferentially mate with males that have fed on these chemicals. This hypothesis is, to date, based on studies of only very few species and its generality is largely untested. We tested the hypothesis on different spatial scales (small cage and seminatural field‐cage) using the monophagous fruit fly, Bactrocera cacuminata. This species is known to respond to methyl eugenol (ME), a chemical found in many plant species and one upon which previous studies have focused. Contrary to expectation, no obvious female choice was apparent in selecting ME‐fed males over unfed males as measured by the number of matings achieved over time, copulation duration, or time of copulation initiation. However, the number of matings achieved by ME‐fed males was significantly greater than unfed males 16 and 32 days after exposure to ME in small cages (but not in a field‐cage). This delayed advantage suggests that ME may not influence the pheromone system of B. cacuminata but may have other consequences, acting on some other fitness consequence (e.g., enhancement of physiology or survival) of male exposure to these chemicals. We discuss the ecological and evolutionary implications of our findings to explore alternate hypotheses to explain the patterns of response of dacine fruit flies to specific plant‐derived chemicals.     

Balancing sexual selection through opposing mate choice and male competition

Male–male competition and female mate choice act contemporaneously in the cockroach Nauphoeta cinerea and the social pheromone of males influences the outcome of both forms of sexual selection. We therefore examined the joint and separate effects of male–male competition and female mate choice to determine if the selective optima for the pheromone were the same or different. Dominant males in a newly established hierarchy mated more frequently, but not exclusively. Manipulations of the multi-component social pheromone produced by males of N. cinerea showed that both long- and close-range attraction of females by males were influenced by the quantity and composition of the pheromone. The most attractive composition, however, differed from that which was most likely to confer high status to males. Since the outcome of male–male competition can conflict with mating preferences exhibited by females, there is balancing sexual selection on the social pheromone of N. cinerea. Such balancing selection might act to maintain genetic variation in sexually selected traits. We suggest that the different forms of sexual selection conflict in N. cinerea because females prefer a blend different to that which is most effective in male–male competition in order to avoid mating with overly aggressive males.     

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male-male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male-male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid-based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male-male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.     

Sexual conflict in Sepsis cynipsea: female reluctance, fertility and mate choice

Sexual conflict can elevate mating costs via male inflicted damage to females. Possible selective advantages to males include decreasing the likelihood that females remate and/or increasing females' current reproductive investment in a manner analogous to terminal reproductive investment. We investigated female mating behaviour relative to their number of previous copulations in the fly Sepsis cynipsea, and whether males accepted as first mates were more likely to be accepted again. Females were more likely to remate with new rather than original males, although there was no associated fitness benefit, and in contrast to theoretical predictions, females became less reluctant to remate as the number of previous copulations increased. Additionally, females did not increase reproductive investment as would be expected if they were ensuring their final reproductive efforts were maximized by remating. This suggests that damaging females is a pleiotropic effect which inadvertently leads to increased, not decreased, polyandry.     

Environment-dependent selection on mate choice in a natural population of birds

Female mate choice acts as an important evolutionary force, yet the influence of the environment on both its expression and the selective pressures acting upon it remains unknown. We found consistent heritable differences between females in their choice of mate based on ornament size during a 25-year study of a population of collared flycatchers. However, the fitness consequences of mate choice were dependent on environmental conditions experienced whilst breeding. Females breeding with highly ornamented males experienced high relative fitness during dry summer conditions, but low relative fitness during wetter years. Our results imply that sexual selection within a population can be highly variable and dependent upon the prevailing weather conditions experienced by individuals.     

Sexual conflict and the energetic costs of mating and mate choice in water striders

ABSTRACT Analyses of intersexual conflicts of interest over courtship, mating, or mate guarding require an understanding of the physiological costs of sexual interaction. Repeated respirometric measures of energetic expenditure were taken on female Aquarius remigis while unladen and while carrying a mating male, a small metal weight, or a euthanized male. Unladen "cruising" locomotion consumed an average of 334.6 muW of energy ([Formula: see text]); this estimate of the cost of locomotion coincides with measures from voluntarily locomoting arthropods of similar mass and represents the first energetic measure of skating on a water surface. Cruising females carrying males or metal weights consumed 24% and 28% more energy than unladen females, respectively. Females engaged in "escape" locomotion consumed 43% more energy while carrying a male than while unladen. Further, our study shows that premating struggles, and therefore selective mating deccisions, are energetically costly. Struggling females consumed an average of 936.6 muW, a 126% increase compared to cruising, nonstruggling females, and 64% more than mating females engaged in escape locomotion. We develop a quantitative model showing that at a certain harassment rate threshold, accepting superfluous matings becomes the "best of a bad job" for females.     

First evidences of sexual selection by mate choice in marine zooplankton

Sexual selection is potentially important in marine zooplankton, presumably the most abundant metazoans on earth, but it has never been documented. We examine the conditions for sexual selection through mate choice and describe mating preferences in relation to size in a marine zooplankter, the pelagic copepod Acartia tonsa. Males produce spermatophores at a rate (~1 day⁻¹) much lower than known female encounter rates for most of the year and the decision to mate a particular female thus implies lost future opportunities. Female egg production increases with female size, and males mating larger females therefore sire more offspring per mating event. Similarly, females encounter males more frequently than they need to mate. Large males produce larger spermatophores than small males and the offspring production of female increases with the size of the spermatophore she receives. Additionally, large spermatophores allow females to fertilize eggs for a longer period. Thus, mating with large males reduces the female’s need for frequent matings and she may sire sons that produce more offspring because size is heritable in copepods. Finally, we show that both males and females mate preferentially with large partners. This is the first demonstration of sexual selection by mate choice in a planktonic organism.     

Stress hormones and mate choice

A few recent studies have suggested that glucocorticoid stress hormones can play a role in sexual selection. In terms of mate choice, these studies have shown that individuals can exhibit preferences for mates with either low baseline or peak glucocorticoid levels. This appears to occur because stress hormones can be key mediators of many condition-dependent, sexually selected traits that serve as honest signals of mate quality. We suggest that our understanding of how sexual selection can influence the glucocorticoid stress response will be expanded by studying the interactions among glucocorticoid stress hormones, sex steroids and body condition.     

HLA and mate selection

HLA types of the partners in 1017 couples were determined. It appeared that there was statistically significant occurrence of like types more frequently than predicted by chance. The existence of ethnic or racial groups with characteristically different frequencies of the HLA types might explain the result.     

Designing mate choice experiments

The important role that mate choice plays in the lives of animals is matched by the large and active research field dedicated to studying it. Researchers work on a wide range of species and behaviours, and so the experimental approaches used to measure animal mate choice are highly variable. Importantly, these differences are often not purely cosmetic; they can strongly influence the measurement of choice, for example by varying the behaviour of animals during tests, the aspects of choice actually measured, and statistical power. Consideration of these effects are important when comparing results among studies using different types of test, or when using laboratory results to predict animal behaviour in natural populations. However, these effects have been underappreciated by the mate choice literature to date. I focus on five key experimental considerations that may influence choice: (i) should mating be allowed to occur, or should a proxy behavioural measure of preference be used instead? (ii) Should subjects be given a choice of options? (iii) Should each subject be tested more than once, either with the same or different stimuli? (iv) When given a choice, how many options should the subject choose between? (v) What form should the experimental stimuli take? I discuss the practical advantages and disadvantages of common experimental approaches, and how they may influence the measurement of mate choice in systematic ways. Different approaches often influence the ability of animals to perceive and compare stimuli presented during tests, or the perceived costs and benefits of being choosy. Given that variation in the design of mate choice experiments is likely unavoidable, I emphasise that there is no single ‘correct’ approach to measuring choice across species, although ecological relevance is crucial if the aim is to understand how choice acts in natural populations. I also highlight the need for quantitative estimates of the sizes of potentially important effects, without which we cannot make informed design decisions.