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.     

Phenotypic variation and covariation indicate high evolvability of acoustic communication in crickets

Studying the genetic architecture of sexual traits provides insight into the rate and direction at which traits can respond to selection. Traits associated with few loci and limited genetic and phenotypic constraints tend to evolve at high rates typically observed for secondary sexual characters. Here, we examined the genetic architecture of song traits and female song preferences in the field crickets Gryllus rubens and Gryllus texensis. Song and preference data were collected from both species and interspecific F1 and F2 hybrids. We first analysed phenotypic variation to examine interspecific differentiation and trait distributions in parental and hybrid generations. Then, the relative contribution of additive and additive‐dominance variation was estimated. Finally, phenotypic variance–covariance ( P ) matrices were estimated to evaluate the multivariate phenotype available for selection. Song traits and preferences had unimodal trait distributions, and hybrid offspring were intermediate with respect to the parents. We uncovered additive and dominance variation in song traits and preferences. For two song traits, we found evidence for X‐linked inheritance. On the one hand, the observed genetic architecture does not suggest rapid divergence, although sex linkage may have allowed for somewhat higher evolutionary rates. On the other hand, P matrices revealed that multivariate variation in song traits aligned with major dimensions in song preferences, suggesting a strong selection response. We also found strong covariance between the main traits that are sexually selected and traits that are not directly selected by females, providing an explanation for the striking multivariate divergence in male calling songs despite limited divergence in female preferences.     

Intention versus behaviour in parental sex preferences among the Mukogodo of Kenya

The relationship between parents' stated sex preferences for children and actual parental behaviour towards sons and daughters is examined among the Mukogodo, a group of traditional pastoralists in rural Kenya. Although their cultural values are male-centered and they tend to express a preference for sons, Mukogodo parents actually appear to be more solicitous of daughters, and the Mukogodo have a strongly female-biased childhood sex ratio. Studies of stated sex preferences should therefore be coupled with attempts to assess actual parental investment in sons and daughters.     

Racism and sexism in medically assisted conception

Despite legislation and public education, racism and sexism are alive and well. Though pre-conceptive gender selection may enhance procreative liberty, this technology presents two disturbing questions. First, does sex selection represent underlying parental sexism? Second, by performing gender selection, do medical professionals perpetuate sexism? It will be maintained that pre-conceptive sex selection is sexist as it reflects parental anticipation of stereotypical gender based behavior. Perhaps even more incriminating, sex selection forces parents to prefer one sex over another, to place a value on gender. This emphasis on sex conflicts with societal goals which urge, and often legally require, individuals to ignore gender. We will assert that pre-conceptive gender selection exemplifies sexism in its purest most blatant form as prior to conception, before parents can possibly know anything about their child, gender dominates the calculus of a child’s worth. We will also emphasize that physicians, by facilitating sex selection, legitimize the motivations of their patients and provide de facto support of sexism. In a similar vein, arguments against pre-conceptive race selection will be made.     

Sexual imprinting on continuous variation: do female zebra finches prefer or avoid unfamiliar sons of their foster parents?

Sexual imprinting on discrete variation that serves the identification of species, morphs or sexes is well documented. By contrast, sexual imprinting on continuous variation leading to individual differences in mating preferences within a single species, morph and sex has been studied only once (in humans). We measured female preferences in a captive population of wild-type zebra finches. Individual cross-fostering ensured that all subjects grew up with unrelated foster parents and nest mates. Females from two cohorts (N = 113) were given a simultaneous choice between (two or four) unfamiliar males, one of which was a genetic son of their foster parents (SFP). We found no significant overall preference for the SFP (combined effect size d = 0.14 +/- 0.15). Additionally, we tested if foster parent traits could potentially explain between-female variation in preferences. However, neither the effectiveness of cooperation between the parents nor male contribution to parental care affected female preferences for the son of the foster father. We conclude that at least in zebra finches sexual imprinting is not a major source of between-individual variation in mating preferences.     

The question of adaptive sex ratio in outcrossed vertebrates.

Of various published theories of adaptive control of progeny sex ratio only two are plausible, a physiological theory by Trivers & Willard, and a demographic theory by Verner. The first applies to species in which sons and daughters impose different costs on parents, and in which only one or very few young are produced at once. They ought to show positive correlations in the sex of successive offspring and high sex-ratio variance among progenies. Verner's theory postulates a minimization of competition for mates in neighbourhoods subject to random fluctuation in sex ratio. Optimal progenies would exactly match the population's evolutionary equilibrium sex ratio. There would be little variance among progenies. Evidence from vertebrates is unfavourable to either theory and supports, instead, a non-adaptive model, the purely random (Mendelian) determination of sex. The apparent absence of parental control of progeny sex ratio is a serious theoretical difficulty.     

The Relationship between Adult Occupational Preferences and Childhood Gender Nonconformity among Samoan Women,Men, and <Emphasis Type="Italic">Fa</Emphasis>’<Emphasis Type="Italic">afafine</Emphasis>

Previous research has found that sex differences in occupational preferences are both substantial and cross-culturally universal. Androphilic males tend to display “gender-shifted” occupational preferences, with relatively female-typical interests. Past research has overwhelmingly relied on Western samples; this article offers new insights from a non-Western setting. Known locally as fa’afafine, androphilic males in Samoa occupy a third-gender category. Data were collected in Samoa from 103 men, 103 women, and 103 fa’afafine regarding occupational preferences and recalled childhood gender nonconformity (CGN). A substantial sex difference was observed in the occupational preferences of men and women (d = 2.04). Interestingly, women and fa’afafine did not differ in their preferences (p = 0.89), indicating a complete gender inversion of occupational preferences in the latter. Although there was no correlation between women’s CGN and masculine occupational preferences, there was a significant correlation (r = ?0.62) between these variables in both men and fa’afafine. Among males (both men and fa’afafine), increased CGN was associated with preference for feminine occupations. The present research corroborates past findings and furnishes support for the conclusion that female-typical occupational preferences are a cross-culturally invariant aspect of male androphilia.     

THE COMPLEX INTERPLAY OF SEX ALLOCATION AND SEXUAL SELECTION

It is well recognized that sex allocation strategies can be influenced by sexual selection, when females adjust offspring sex ratios in response to their mates’ attractiveness. Yet the reciprocal influence of strategic sex allocation on processes of sexual selection has only recently been revealed. Recent theoretical work demonstrates that sex allocation weakens selection for female preferences, leading to the decline of male traits. However, these results have been derived assuming that females have perfect knowledge of mate attractiveness and precise control over cost‐free allocation. Relaxing these assumptions highlights the importance of another feedback: that adaptive sex allocation must become difficult to maintain as traits and preferences decline. When sex allocation strategies erode not only traits and preferences but also their own selective advantage, predictions can no longer be expressed as a simple linear correlation between ornament exaggeration and adaptive sex allocation. Instead, strongest sex ratio biases may be found at intermediate trait levels.     

An experimental test of condition-dependent male and female mate choice in zebra finches

In mating systems with social monogamy and obligatory bi-parental care, such as found in many songbird species, male and female fitness depends on the combined parental investment. Hence, both sexes should gain from choosing mates in high rather than low condition. However, theory also predicts that an individual's phenotypic quality can constrain choice, if low condition individuals cannot afford prolonged search efforts and/or face higher risk of rejection. In systems with mutual mate choice, the interaction between male and female condition should thus be a better predictor of choice than either factor in isolation. To address this prediction experimentally, we manipulated male and female condition and subsequently tested male and female mating preferences in zebra finches Taeniopygia guttata, a songbird species with mutual mate choice and obligatory bi-parental care. We experimentally altered phenotypic quality by manipulating the brood size in which the birds were reared. Patterns of association for high- or low-condition individuals of the opposite sex differed for male and female focal birds when tested in an 8-way choice arena. Females showed repeatable condition-assortative preferences for males matching their own rearing background. Male preferences were also repeatable, but not predicted by their own or females' rearing background. In combination with a brief review of the literature on condition-dependent mate choice in the zebra finch we discuss whether the observed sex differences and between-studies differences arise because males and females differ in context sensitivity (e.g. male-male competition suppressing male mating preferences), sampling strategies or susceptibility to rearing conditions (e.g. sex-specific effect on physiology). While a picture emerges that juvenile and current state indeed affect preferences, the development and context-dependency of mutual state-dependent mate choice warrants further study.     

Does biology underlie the oldest profession? Prostitution and sex disparities in john behavior

This study considers a biosocial explanation of why johns, the purchasers of commercial sex exchanges, are almost exclusively male. Trivers's theory of parental investment and sexual selection predicts that differential parental investment by biological sex will lead to divergent sex-based reproductive instincts. The sex bearing the larger parental investment will tend to be choosier whereas the sex bearing the lesser investment will tend to be relatively indiscriminate and competitive for access to sexual resources. We hypothesized that men are more likely than women to offer objects of value in exchange for access to sexual resources. Using self-reports of sex-purchasing from Add Health data (N = 14,544), we found that maleness was a robust predictor of john behavior even after controlling for well-known criminogenic risk factors.     

A test of the cognitive social learning model of type A behavior

Portions of the cognitive social learning model proposed by Price as an explanation for the development and maintenance of Type A behavior were examined empirically. Specifically, the hypothesis that Type A behavior is fostered by various beliefs and fears and that these same beliefs and fears arise, in part, as the result of certain parental characteristics was investigated. A questionnaire assessing Type A behavior and the beliefs, fears, and parental characteristics proposed by Price was constructed and administered to a sample of males and females. The results indicated moderate associations between the variables examined for both males and females, with no significant gender differences in the pattern of relationships. The findings are congruent with relationships proposed by Price's model. Implications of the model are discussed in terms of additional research needed.     

The evolution of parental care in shorebirds: life histories, ecology, and sexual selection

Parental care is expected to evolve according to a trade-offbetween the benefits of increased survival of offspring andcosts of reduced survival and future reproduction of adults.Here we investigate the components of this life-history trade-offin shorebirds (Charadriides, excluding Laroidea), an avian infraorderdisplaying an unusual diversity in extent of care by each sex.We show that evolutionary increases in the duration of carein one sex are associated with decreased care by the other.We found no evidence that various hypothesised benefits of careprovide a general explanation for the duration of care by eitheror both sexes, although parental feeding of the young was tooconservative for comparisons. Sexual dimorphism in body sizehad a similar relationship to parental care in both sexes: reductionsin duration of care by either sex were matched by increasesin the size of that sex relative to the other. Whereas thispattern could be explained by sexual selection in males, itwas retained within socially monogamous females. Reduced carein males (but not in females) appears to have facilitated theevolution of greater migration distances. These results suggestthat parental care has had different causes and consequencesin each sex. Benefits of desertion due to sexual selection aremore clearly demonstrable for males, whereas correlates of careare less clear for females     

Serial Monogamy as Polygyny or Polyandry?

Applications of sexual selection theory to humans lead us to expect that because of mammalian sex differences in obligate parental investment there will be gender differences in fitness variances, and males will benefit more than females from multiple mates. Recent theoretical work in behavioral ecology suggests reality is more complex. In this paper, focused on humans, predictions are derived from conventional parental investment theory regarding expected outcomes associated with serial monogamy and are tested with new data from a postreproductive cohort of men and women in a primarily horticultural population in western Tanzania (Pimbwe). Several predictions derived from the view that serial monogamy is a reproductive strategy from which males benefit are not supported. Furthermore, Pimbwe women are the primary beneficiaries of multiple marriages. The implications for applications of sexual selection theory to humans are discussed, in particular the fact that in some populations women lead sexual and reproductive lives that are very different from those derived from a simple Bateman-Trivers model.     

Sleep/wake patterns and circadian typology in preschool children based on standardized parental self-reports

We studied the sleep/wake patterns and circadian typology of Japanese preschool children living in the Tokyo metropolitan area (193 boys and 190 girls, 4–6 years of age) from June to July 2012 based on a standardized parental self-reporting questionnaire. Our major findings are as follows: (1) sleep/wake timing was delayed, and the duration of nocturnal sleep (sleep period as well as time in bed) increased from that on scheduled days (weekdays) to that on free days (weekends) for all ages. (2) The duration of daily sleep (24?h), including daytime nap, was longer for 4-year-old children compared with that in 5- to 6-year-old children, but not significantly different between scheduled and free days within each age group. (3) The distribution of chronotypes was 36.3% for morning (M)-type, 48.8% for neither (N)-type and 11.2% for evening (E)-type, and this distribution was independent of sex or age. (4) Sleep/wake timing delays were observed from M-type and N-type to E-type during scheduled and free days. (5) The duration of nocturnal sleep decreased but increased for 24-h sleep time from M-type and N-type to E-type on scheduled days. (6) Sleep durations did not differ among chronotypes on free days. (7) Chronotypes were associated with parents’ diurnal preferences, mealtimes and attendance at kindergartens or childcare centers but not with sex, age, season of birth, exposure to multimedia or exposure to morning sunlight in their bedrooms. When these results were compared with those for older children and adolescents, similar sleep/wake patterns and circadian typology were observed, although to a lesser degree, in children as young as 4–6 years of age. Napping may compensate, in part, for an accumulated weekday sleep deficit. The distribution of chronotypes was associated with differences in sleep/wake timing and duration and was influenced by the parents’ diurnal preferences and lifestyles. Further research on preschool children is required to investigate whether circadian typology affects their behavioral, emotional and cognitive development.     

Desired family size and sex of children in Nigeria

During 1981, sex ratio data and preferences for family size and for combinations and permutations of children were provided by 333 Nigerian students at the University of Ilorin, Ilorin, Nigeria. For the present and parental generations combined, the secondary sex ratio was estimated to be 95.8 males:100 females. In the projected families, preferences for family sizes resulted in an average of 4.88 children per family. The most preferred family consisted of four children--a 2m2f combination in a mfmf order, whereas the second most preferred family consisted of five children--3m2f combination in a mfmfm order. Also expressed was a strong preference for permutations of sexes, resulting in a male child as first-born followed by an alternation of sexes. A greater preference for male children was indicated by the combined sex ratio of 167 males:100 females for the preferred families.     

Bill Color Preferences of Zebra Finches

Bill color varies with age and sex in zebra finches. Among birds of similar age and condition, males' bills tend to be redder and darker than those of females, but there is overlap in the phenotypic expression of the sexes. The bills of young birds are paler and less red than those of older birds. There is also interindividual variation within age and sex class. Experiments were performed to measure heterosexual and isosexual (= same sex) preferences of finches. Females preferred to associate with males with the reddest, brightest bills; they even preferred males whose bills were exaggerated through color applications of non-toxic marking pen. Males preferred to associate with females with bill colors in the middle of the phenotypic range. Females thus have “directional” preferences for male bill color, whereas male preference is “stabilizing” with regard to female bill color. In isosexual tests, neither sex showed a consistent preference for particular bill colors. Both sexes, however, displayed a tendency toward individual variability in preference. Bill color appears to be more important in heterosexual than in isosexual interactions. Several authors have recently suggested that organisms prefer brightly colored mates because bright coloration indicates superior physical condition. Results reported here do not support this hypothesis. Alternative functional explanations for the observed preferences are that bill color signals mating status, age or reproductive value. None of these appears to be a cogent explanation for the trends. Preferences do not appear to result from sexual imprinting. The possibility that the preferences are aesthetic and non-functional is discussed.     

Sexual selection and sex linkage

Some animal groups, such as birds, seem prone to extreme forms of sexual selection. One contributing factor may be sex linkage of genes affecting male displays and female preferences. Here we show that sex linkage can have substantial effects on the genetic correlation between these traits and consequently for Fisher's runaway and the good-genes mechanisms of sexual selection. Under some kinds of sex linkage (e.g. Z-linked preferences), a runaway is more likely than under autosomal inheritance, while under others (e.g., X-linked preferences and autosomal displays), the good-genes mechanism is particularly powerful. These theoretical results suggest empirical tests based on the comparative method.     

Staying with the young enhances the fathers’ attractiveness in burying beetles

Studying the relationship between parental and mating effort helps us to understand the evolution of parental care and, consequently, has been the subject of many theoretical and empirical investigations. Using burying beetles as a model, we found no correlation between the intensity of a sexual signal (sex pheromone quantity) and the amount of care provided by males. However, males that were given the opportunity to breed and care for young went on to produce a higher amount of their sexual signal and attracted three times more females in the field than control males that were not given the opportunity to breed. The likely explanation for our finding is that specific aspects of care in burying beetles, that is the defense and preservation of a nutrient rich breeding resource, a small vertebrate cadaver, is not only beneficial for the offspring but also for the adults themselves. Obtaining a good carrion meal possibly enables males to store resources that they can subsequently allocate toward sexual signaling. Collectively, our results highlight that conditions can exist where male participation in brood care has a positive effect on its sexual attractiveness. This in turn might have facilitated the evolution of male assistance in parental care.     

Natural selection and sex differences in morbidity and mortality in early life

Both morbidity and mortality are consistently reported to be higher in males than in females in early life, but no explanation for these findings has been offered. This paper argues that the sex difference in early vulnerability can be attributed to the natural selection of optimal maternal strategies for maximizing lifetime reproductive success, as modelled previously by Trivers and Willard. These authors theorized that males and females offer different returns on parental investment depending on the state of the environment. Natural selection has therefore favoured maternal ability to manipulate offspring sex in response to environmental conditions in early life, as shown in variation in the sex ratio at birth. This argument can be extended to the whole period of parental investment until weaning. Male vulnerability in response to environmental stress in early life is predicted to have been favoured by natural selection. This vulnerability is most evident in the harsh conditions resulting from pre-term birth, but can also be seen in term infants, and manifests as greater morbidity and mortality persisting into early childhood. Malnutrition, interacting with infection after birth, is suggested as the fundamental trigger mechanism. The model suggests that whatever improvements are made in medical care, any environmental stress will always affect males more severely than females in early life.     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.