Women's mating strategies

What does a woman want? The traditional evolutionist's answer to Freud's famous query is that a woman's extensive investment in each of her children implies that she can maximize her fitness by restricting her sexual activity to one, or at most, a few high-quality males. Because acquiring resources for her offspring is of paramount importance, a woman will try to attract wealthy, high-status men who are willing and able to help her. She must be coy and choosy, limiting her attentions to men who are worthy of her and emphasizing her chastity so as not to threaten the paternity confidence of her mate. The lady has been getting more complicated of late, however. As Sarah Hrdy¹ predicted, we now have evidence that women, like other female primates, are also competitive, randy creatures. Women have been seen competing with their rivals using both physical aggression^2,3 and more subtle derogation of competitors.⁴ While they are still sometimes coy and chaste, women have also been described recently as sexy and sometimes promiscuous creatures, manipulating fatherhood by the timing of orgasm^5,6 and using their sexuality to garner resources from men. The real answer to Freud's query, of course, is that a woman wants it all; a man with the resources and inclination to invest, and with genes that make him attractive to other women so that her sons will inherit his success. Her strategies for attaining these somewhat conflicting aims, and her success in doing so, are shaped by her own resources and options and by conflicts of interest with men and other women.     

Age-specific mating and reproductive senescence in the seven-spotted ladybird, Coccinella septempunctata

Abstract:  Adults of the seven-spotted ladybird, Coccinella septempunctata Linnaeus (Col., Coccinellidae) were paired for mating from very young to old age (1–50 days) to record the willingness to mate, attainment of sexual maturity and onset of reproductive senescence in both the sexes. Mating commenced after 4 and 2 days of emergence of male and female, respectively, and 100% mating was achieved at the young age in both cases (10 days). Willingness to mate decreased with increase in the age from 40 to 50 days of both the sexes. Ladybird exhibited protandry. Mating duration, fecundity and per cent viability of eggs of middle-aged males (20–30 days old) and females (20 days old) were the highest. Mating duration and per cent viability of eggs were male age dependent, whereas pre-oviposition and oviposition periods were mating stimulus dependent. Oviposition period and fecundity were female age-dependent responses. Fecundity was highest when 20-day-old female and 30-day-old male were paired. Onset of reproductive senescence started at the age of 30 days in males and 20 days in females. The present study confirms the effect of ageing on male and female C. septempunctata and supports the Hansen and Price [J. Evol. Biol. (1995) vol. 8, pp. 759–778] model that females mating with young and middle-aged males yield optimal quality progeny.     

Random mating with respect to mating status in the simultaneously hermaphroditic land snail Arianta arbustorum

In promiscuous species with sperm storage, males are expected to show a preference for mating with virgin and young females to reduce the risk of sperm competition. In the simultaneous hermaphrodite land snail Arianta arbustorum, sperm production precedes egg production by 2–4 weeks, resulting in a short period of protandric hermaphroditism before shell growth is completed. In natural populations, copulating pairs involving individuals which have not yet completed shell growth (virgins) have been observed. We ran a series of mate-choice experiments to examine whether virgin and nonvirgin (experienced) individuals of A. arbustorum discriminate between virgin and nonvirgin mating partners. We also assessed the number of sperm delivered to partners with different mating status. Neither virgin nor nonvirgin snails showed any preference for mating with a virgin partner. In all test situations mating was random and the number of sperm delivered was not adjusted to the mating status of the partner. Mating success was mainly determined by the activity of the individual. The random mating pattern does not imply random fertilization of eggs because the presence of a sperm-digesting organ and the morphology of the sperm storage organ allow a selective storage and use of sperm in A. arbustorum.     

Facultative pupal mating in Heliconius erato: Implications for mate choice,female preference,and speciation

Mating systems have broad impacts on how sexual selection and mate choice operate within a species, but studies of mating behavior in the laboratory may not reflect how these processes occur in the wild. Here, we examined the mating behavior of the neotropical butterfly Heliconius erato in the field by releasing larvae and virgin females and observing how they mated. H. erato is considered a pupal‐mating species (i.e., males mate with females as they emerge from the pupal case). However, we observed only two teneral mating events, and experimentally released virgins were almost all mated upon recapture. Our study confirms the presence of some pupal‐mating behavior in H. erato, but suggests that adult mating is likely the prevalent mating strategy in this species. These findings have important implications for the role of color pattern and female mate choice in the generation of reproductive isolation in this diverse genus.     

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in apopulation may have important consequences for mate choice,with the information gathered about males influencing boththe preference function and degree of choosiness of females.Sexual selection may be affected as a result. Sampling of particularsubsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequencein which males are sampled may also be important in specieswithout traditional, active mate choice, such as when sexualselection involves sexual conflict over mating. This wouldoccur if the likelihood of a female mating with a male of acertain phenotype changes as a result of previous encounters.We examined the effects of encountering males differing inbody size, a sexually selected phenotype, in the seaweed flyCoelopa frigida. Sexual selection occurs in this species asa result of a sexual conflict over mating. We show that theoutcome of the sexual conflict is independent of the orderin which males are encountered by female seaweed flies, withthe overall mating advantage to large males being unaffected.In addition, we explored female preference functions and evaluatethe heterogeneity in female willingness to mate. We suggestthat consideration of mate sampling theory is valuable whenexamining mate choice in species in which sexual selectionis driven by sexual conflict.     

Estimating sexual selection and sexual isolation effects from mating frequencies

Abstract.— Sexual selection (defined as the change in genotypic or phenotypic frequencies of mated versus total population frequencies) and sexual isolation (defined as the deviation from random mating in mated individuals) show different evolutionary consequences and partially confounded causes. Traditionally, the cross-product estimator has been used to quantify sexual selection, whereas a variety of indexes, such as Yule V , Yule Q, YA , joint I , and others have been used to quantify sexual isolation. Because the two types of estimators use different scales, the effects of both processes cannot be monitored simultaneously. We describe three new related statistics that quantify both sexual selection ( PSS ) and sexual isolation ( PSI ) effects for every mating pair combination in polymorphic traits, as well as measure their combined effects ( PTI = PSI X PSS ). The new statistics have the advantage of providing information on every mating pair combination, quantifying the effects of sexual selection and isolation in the same units, and detecting asymmetry in sexual isolation. The ability of the new statistics to ascertain the biological causes of sexual selection and sexual isolation are investigated under different models involving distinct marginal frequencies, mate propensity, and mate choice coefficients. We also studied the use of classical isolation indexes applied on PSI coefficients, instead of on raw data. The use of the classical indexes applied to PSI coefficients considerably reduces the statistical bias of the estimates, revealing the good estimation properties of the new statistics.     

Repeatability of extra-pair mating in tree swallows

Models of sexual selection assume that female mating preferences are heritable and, thus, repeatable for individual females across multiple mating episodes. Previous studies of the repeatability of female preference have examined individuals in captivity and focused presumably on social mate choice. However, extra-pair mating is widespread and can also influence sexual selection. We examined the repeatability of extra-pair mating in a wild population of tree swallows (Tachycineta bicolor) by experimentally inducing females to lay two clutches in rapid succession within the same season. We found that the proportion of extra-pair young and the number of extra-pair sires were highly repeatable for individual females. However, the repeatability of specific extra-pair sires was low. We suggest that this unusual pattern of mating may be due to females maximizing the heterozygosity of their offspring.     

Roving females and patient males: a new perspective on the mating strategies of chimpanzees

Mating strategies are sets of decisions aimed at maximizing reproductive success. For male animals, the fundamental problem that these strategies address is attaining mating access to females in a manner that maximizes their chances of achieving paternity. For chimpanzees (Pan troglodytes), despite substantial interest in mating strategies, very little attention has been paid to the most fundamental problem that mating strategies need to solve: finding mates. Only a single model, Dunbar's general model of male mating strategies, exists to explain mate‐searching behaviour in chimpanzees. Under this model, males in most populations are regarded as pursuing a ‘roving’ strategy: searching for and sequestering fertile females who are essentially passive with respect to mate searching. The roving mating strategy is an assumption deeply embedded in the way chimpanzee behaviour is considered; it is implicit in the conventional model for chimpanzee social structure, which posits that male ranging functions both to monitor female reproductive state and to ward these females from other groups of males through collective territoriality: essentially, ranging as mating effort. This perspective is, however, increasingly at odds with observations of chimpanzee behaviour. Herein, I review the logic and evidence for the roving‐male mating strategy and propose a novel alternative, a theoretical framework in which roving is a strategy pursued by female chimpanzees in order to engage successfully in promiscuous mating. Males, unable to thwart this female strategy, instead maximise the number of reproductive opportunities encountered by focusing their behaviour on countering threats to health, fertility and reproductive career. Their prolonged grooming bouts are seen, in consequence, as functioning to mitigate the negative impacts of socially induced physiological stress. In this new framework, the roving‐male strategy becomes, at best, a ‘best of a bad job’ alternative for low‐ranking males when faced with high levels of competition for mating access. Male chimpanzees do not search for mates, but for one another, for food, and, at times, for rivals in other communities. To the extent that female promiscuity functions to counter infanticide risk, mate searching by female chimpanzees—and any associated costs—can be seen as an unavoidable consequence of male sexual coercion. This novel framework is a better fit to the available data than is the conventional account. This review highlights the desperate need for additional work in an area of chimpanzee biology that has been somewhat neglected, perhaps in part because assumptions of roving males have remained unquestioned for too long. It also highlights the need, across taxa, to revisit and revise theory, and to test old assumptions, when faced with contrary data.     

Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies

The avoidance of familiar individuals as mates can act to maximizethe benefits of polyandry or might help to minimize inbreedingin small or highly philopatric populations. As previous matesare also familiar, the effects of familiarity and mating historycan often be confounded. Here, we disentangle these effectson mating decisions in the guppy, Poecilia reticulata, and examinetheir influence on sexual selection. In 3 experiments, malesand females were 1) able to mate, 2) had visual and olfactorycontact, or 3) had visual contact only. Familiarity was successfullyacquired via visual cues, and females were in all cases morelikely to mate with unfamiliar than with familiar males, indicatingthat familiarity is a more important determinant of mating outcomethan mating history. Males did not court unfamiliar femalesany more than familiar females and did not differentially allocatesperm. Familiarity did not alter the strength of sexual selectionon male coloration: we found overall positive selection forbright, large males. Female preferences for unfamiliar malesand ornamental traits may therefore be largely independent.     

Polyandry and alternative mating tactics

Many species in the animal kingdom are characterized by alternative mating tactics (AMTs) within a sex. In males, such tactics include mate guarding versus sneaking behaviours, or territorial versus female mimicry. Although AMTs can occur in either sex, they have been most commonly described in males. This sex bias may, in part, reflect the increased opportunity for sexual selection that typically exists in males, which can result in a higher probability that AMTs evolve in that sex. Consequently, females and polyandry can play a pivotal role in governing the reproductive success associated with male AMTs and in the evolutionary dynamics of the tactics. In this review, we discuss polyandry and the evolution of AMTs. First, we define AMTs and review game theoretical and quantitative genetic approaches used to model their evolution. Second, we review several examples of AMTs, highlighting the roles that genes and environment play in phenotype expression and development of the tactics, as well as empirical approaches to differentiating among the mechanisms. Third, ecological and genetic constraints to the evolution of AMTs are discussed. Fourth, we speculate on why female AMTs are less reported on in the literature than male tactics. Fifth, we examine the effects of AMTs on breeding outcomes and female fitness, and as a source, and possibly also a consequence, of sexual conflict. We conclude by suggesting a new model for the evolution of AMTs that incorporates both environmental and genetic effects, and discuss some future avenues of research.     

The effects of exposure to seaweed on willingness to mate, oviposition, and longevity in seaweed flies

Abstract  1. Large male seaweed flies (Diptera: Coelopidae) are more likely to mate than smaller males. This is due to sexual conflict over mating, by which females physically resist male attempts to copulate. In some species, large males are simply more efficient at overpowering female resistance.
2. Female reluctance to mate is likely to have evolved due to the costs of mating to females. In many dipterans, males manipulate female behaviour through seminal proteins that have evolved through sperm competition. This behavioural manipulation can be costly to females, for example forcing females to oviposit in sub-optimal conditions and increasing their mortality.
3. Previous work has failed to identify any ubiquitous costs of mating to female coelopids. The work reported here was designed to investigate the effects of exposure to oviposition sites ( Fucus algae) on the reproductive behaviour of four species of coelopid. Algae deposition in nature is stochastic and females mate with multiple males in and around oviposition sites. Spermatogenesis is restricted to the pupal stage and there is last-male sperm precedence. It was predicted that males would avoid wasting sperm and would be more willing to mate, and to remain paired with females for longer, when exposed to oviposition material compared with control males. Females were predicted to incur longevity costs of mating if mating increased their rate of oviposition, especially in the presence of algae.
4. The behaviour of males of all four species concurred with the predictions; however mating did not affect female receptivity, oviposition behaviour, or longevity. Exposure to algae induced oviposition and increased female mortality in all species independently of mating and egg production. The evolutionary ecology of potential costs of mating to female coelopids are discussed in the light of these findings.     

Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice

Predictions of mating patterns in animals have focused on males and how they compete for fertilizations by controlling females. With reference to the Odonata, a taxon in which mating requires cooperation of the female, the active role that females play in mating decisions is often ignored, leading to the premature conclusion that male coercion of females is common. A critical review of the outcome of sexual conflict among odonates leads me to alternative explanations of female mating patterns that need to be refuted before concluding that males coerce matings. Because Anisoptera males have greater control over tandem formation, they have a greater potential for coercion than Zygoptera males. However, Anisoptera females may simply be willing to remate more often if they receive insufficient sperm to fertilize an entire egg clutch. Contrary to prior assumptions, in both suborders, male defence of oviposition sites does not preclude females from choosing among sites or among males. I find that the evolution of non-aggressive sexual signals by males is a reliable indication that sexual conflict has been resolved in favour of female interests. Although I predict that the benefits to females of choice of male phenotype should rarely exceed the cost of such discrimination in Odonata, female choice is most likely to evolve in territorial species whose males must endure high physiological stress in order to mate, and when site quality is not a reliable predictor of the genetic quality of a potential mate.     

STORM: software for testing hypotheses of relatedness and mating patterns

Storm is a software package that allows users to test a variety of hypotheses regarding patterns of relatedness and patterns of mate choice and/or mate compatibility within a population. These functions are based on four main calculations that can be conducted either independently or in the hypothesis-testing framework: internal relatedness; homozygosity by loci; pairwise relatedness; and a new metric called allele inheritance, which calculates the proportion of loci at which an offspring inherits a paternal allele different from that inherited from its mother. STORM allows users to test four hypotheses based on these calculations and Monte Carlo simulations: (i) are individuals within observed associations or groupings more/less related than expected; (ii) do observed offspring have more/less genetic variability (based on internal relatedness or homozygosity by loci) than expected from the gene pool; (iii) are observed mating pairs more/less related than expected if mating is random with respect to relatedness; and (iv) do observed offspring inherit paternal alleles different from those inherited from the mother more/less often than expected based on Mendelian inheritance.     

Intrasexual selection and male mating strategies in baboons and macaques

If baboon and macaque mating systems constitute a form of female defense polygyny, male mating strategies should be intrasexually selected and should vary in predictable ways with female defensibility, and demographic factors which affect the numbers of competing males per estrous female in populations. Substantial behavioral evidence exists for intrasexual selection of male mating strategies in baboons and macaques. Limited evidence also offers tentative support for theorybased predictions about the relationship between male mating strategy and female defensibility. Although male dominance rank generally predicts mating success, there are a number of factors which tend to increase the success of subordinate males above that expected from a simple dominance-based model of priority of access to mates.     

Assortative mating by fitness and sexually antagonistic genetic variation

Recent documentations of sexually antagonistic genetic variation in fitness have spurred an interest in the mechanisms that may act to maintain such variation in natural populations. Using individual-based simulations, I show that positive assortative mating by fitness increases the amount of sexually antagonistic genetic variance in fitness, primarily by elevating the equilibrium frequency of heterozygotes, over most of the range of sex-specific selection and dominance. Further, although the effects of assortative mating by fitness on the protection conditions of polymorphism in sexually antagonistic loci were relatively minor, it widens the protection conditions under most reasonable scenarios (e.g., under heterozygote superiority when fitness is averaged across the sexes) but can also somewhat narrow the protection conditions under other circumstances. The near-ubiquity of assortative mating in nature suggests that it may contribute to upholding standing sexually antagonistic genetic variation in fitness.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

Do female Nicrophorus vespilloides reduce direct costs by choosing males that mate less frequently?

Sexual conflict occurs when selection to maximize fitness in one sex does so at the expense of the other sex. In the burying beetle Nicrophorus vespilloides, repeated mating provides assurance of paternity at a direct cost to female reproductive productivity. To reduce this cost, females could choose males with low repeated mating rates or smaller, servile males. We tested this by offering females a dichotomous choice between males from lines selected for high or low mating rate. Each female was then allocated her preferred or non-preferred male to breed. Females showed no preference for males based on whether they came from lines selected for high or low mating rates. Pairs containing males from high mating rate lines copulated more often than those with low line males but there was a negative relationship between female size and number of times she mated with a non-preferred male. When females bred with their preferred male the number of offspring reared increased with female size but there was no such increase when breeding with non-preferred males. Females thus benefited from being choosy, but this was not directly attributable to avoidance of costly male repeated mating.     

Reproductive strategies of the larval parasitoid Microplitis croceipes

Mate choice may have important consequences for offspring sex ratio and fitness of haplodiploid insects. Mate preference of females of the solitary larval parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) for virgin and mated males, and vice versa, and the reproductive consequences (i.e., the sex ratio expressed as the proportion of male offspring) were examined in choice and non‐choice experiments. In addition, the effect of repeated rapid and daily copulation of an individual male on the sex ratio of offspring of the female mates was assessed. Males preferred virgins over mated females, whereas females copulated with a male irrespective of his mating status. In both the rapid and daily copulation assay, females copulating with a male that had copulated five times or more produced a higher sex ratio than females that had copulated with a virgin male. Females that copulated with virgin males once or twice produced a significantly and considerably lower sex ratio than females that first copulated with a sperm‐depleted male followed by a virgin male. This indicates that copulating with a sperm‐depleted male has costs and limits acquisition by the female of sperm from virgin males.     

Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster

New theoretical work on kin selection and inclusive fitness benefits predicts that individuals will sometimes choose close or intermediate relatives as mates to maximize their fitness. However, empirical examples supporting such predictions are rare. In this study, we look for such evidence in a natural population of Drosophila melanogaster. We compared mating and nonmating individuals to test whether mating was nonrandom with respect to relatedness. Consistent with optimal inbreeding, males were more closely related to their mate than to randomly sampled females. However, all individuals collected mating showed higher relatedness and males were not significantly more related to their mate than to other mating females. We also found a negative relationship between relatedness and fecundity. Our results are consistent with the hypothesis that inclusive fitness benefits may drive inbreeding tolerance despite direct costs to fitness; however, an experimental approach is needed to investigate the link between mate preference and relatedness.     

Evolutionarily stable mating decisions for sequentially searching females and the stability of reproductive isolation by assortative mating

We consider mating strategies for females who search for males sequentially during a season of limited length. We show that the best strategy rejects a given male type if encountered before a time‐threshold but accepts him after. For frequency‐independent benefits, we obtain the optimal time‐thresholds explicitly for both discrete and continuous distributions of males, and allow for mistakes being made in assessing the correct male type. When the benefits are indirect (genes for the offspring) and the population is under frequency‐dependent ecological selection, the benefits depend on the mating strategy of other females as well. This case is particularly relevant to speciation models that seek to explore the stability of reproductive isolation by assortative mating under frequency‐dependent ecological selection. We show that the indirect benefits are to be quantified by the reproductive values of couples, and describe how the evolutionarily stable time‐thresholds can be found. We conclude with an example based on the Levene model, in which we analyze the evolutionarily stable assortative mating strategies and the strength of reproductive isolation provided by them.