Hormonal Mechanisms of Mate Choice

SYNOPSIS. Mate choice is a critically important determinantof reproductive success. Because of its significance in theevolutionary process, it has received a great deal of attentionfrom animal behaviorists interested in ultimate causes of behavior.Much less effort has been directed at uncovering the physiologicalmechanisms of mate choice, including those operating duringontogeny that lead to adult mate preferences. As a result ofnatural and sexual selection, many aspects of mate choice aresexually dimorphic. How do adult males and females of the samespecies come to show different mating partner preferences? Onepossibility is that sex steroid hormones play important roles,acting either during early development to permanently establishsex differences or during adulthood to facilitate their expression,roles similar to the organizational and activational effectsof sex steroids on sexually dimorphic copulatory and courtshipbehavior patterns. This review (1) summarizes what is knownabout hormones and mate choice, highlighting those results mostrelevant to understanding proximate causation from an evolutionaryperspective; (2) describes recent work from the author's labtesting an organizational hormone hypothesis of mate choice,focusing on a particularly widespread and robust aspect of matechoice—preference for opposite sex partners—in apair bonding species—the zebra finch; and (3) suggestssome future directions for research that might integrate ultimateand proximate causation.     

Sexual Selection and Mate Choice

After a long period of dormancy, Darwin's theory of sexual selection in general, and mate choice in particular, now represents one of the most active fields in evolutionary research. After a brief overview of the history of ideas and a short introduction into the main mechanisms of sexual selection, I discuss some recent theoretical developments and empirical findings in the study of mate choice and review the various current models of mate choice, which can be grossly divided into adaptive models and nonadaptive models. I also examine whether available primate evidence supports various hypotheses concerning mate choice. Although primatologists were long aware that nonhuman primates have preferences for certain mating partners, until recently the functions and evolutionary consequences of their preferences remained obscure. Now there is growing evidence that mate choice decisions provide primates with important direct or indirect benefits. For example, several observations are consistent with the hypothesis that by direct or indirect mate choice female primates lower the risk of infanticide or enhance the chance of producing viable offspring. Nevertheless, there are also significant holes in our knowledge. How the male mandrill, one of Darwin's famous examples, got his brightly colored face, is still unknown.     

Mate Choice Copying in Humans

There is substantial evidence that in human mate choice, females directly select males based on male display of both physical and behavioral traits. In non-humans, there is additionally a growing literature on indirect mate choice, such as choice through observing and subsequently copying the mating preferences of conspecifics (mate choice copying). Given that humans are a social species with a high degree of sharing information, long-term pair bonds, and high parental care, it is likely that human females could avoid substantial costs associated with directly searching for information about potential males by mate choice copying. The present study was a test of whether women perceived men to be more attractive when men were presented with a female date or consort than when they were presented alone, and whether the physical attractiveness of the female consort affected women’s copying decisions. The results suggested that women’s mate choice decision rule is to copy only if a man’s female consort is physically attractive. Further analyses implied that copying may be a conditional female mating tactic aimed at solving the problem of informational constraints on assessing male suitability for long-term sexual relationships, and that lack of mate choice experience, measured as reported lifetime number of sex partners, is also an important determinant of copying.     

Mate Choice Near or Far

When strong positive heritability of fitness arises due to host-parasitecoevolution, consequent sosigonic mate preference underminesmonogamy through tendencies to extra-pair copulation. "Low"females bonded to "low" males try to parasitise their partnershipby obtaining fertilization, surreptitiously if possible, from"high" males: correspondingly, in the case of birds, "Low" malesmay parasite by encouraging egg dumping in their nests by "high"females who have allowed copulation. It follows that nests ofbirds of low status should sometimes show evidence at timesof both types of parasitism while nests of high status shouldshow faithful monogamy. Rather differently from the argument in Hamilton and Zuk (1982),showiness in monogamous species is more likely to be relatedto such extra-pair objectives than to pair—bonding fornesting. Venereal disease makes males cautious about copulating withany female. Although prevented by true monogamy, when monogamyis partial, venereal disease may become the incentive for increasingfemale sexual advertisement. In extreme cases it may combinewith other ecological factors to initiate sex role reversal,in which the female becomes the non-parenting sex of the species. As regards source of the heritability that backs the sosigonicselection assumed in such speculations, reasons are given forpreferring a coevolutionary cycling of ancient, preserved, parasite-defensealleles to the alternatives of an abundant stream of good newdefense mutations, or a process of elimination of purely deleteriousmutations.     

Mate Choice in Non-Human Primates

Mate choice has been observed in many species of non-human primates.There are few definitive studies, however, due to the long lifespans, complex social behavior, and cognitive abilities of theseanimals. Here I review the current literature on mate choicein primates. Females typically prefer complex behavioral traitssuch as social status, familiarity, personality, and parentalcare abilities. This tendency to prefer behavioral traits isconsistent with the non-primate mammalian data. A female's abilityto express preferences, however, is often constrained by hersocial environment—in particular male mating tactics andfemalefemale competition. Males exhibit preferences for high-ranking females. In severalspecies, high-ranking females produce more offspring than low-rankingfemales. In addition, females may also influence male dominancerank and in doing so reduce male-male competition and increasemale mating success.     

The Computational Mechanisms of Mate Choice

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

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ² = 27.43, df = 3, p < 0.0001; 2001: χ² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.     

Male Mate Choice in Trichogramma Turkestanica

In most animals it is the sex that invests the most in reproduction, generally the female, that expresses mate choice. However, in numerous species, males or both males and females are choosy. We investigated mate choice in males of the egg parasitoid Trichogramma turkestanica Meyer (Hymenoptera: Trichogrammatidae). We tested the impact of age and feeding status of males on their capacity to choose between virgin or mated and kin or non-kin females. As expected, males showed no preference between kin and non-kin mates, but inseminated virgin females over mated ones. No effect of age on the level of choosiness was found, but unfed males were choosier than fed ones. This is the first study to show an effect of feeding status of males on mate choice in insect parasitoids.     

Parasites and Mate Choice in Gray Treefrogs, Hyla versicolor

A fundamental assumption of the Hamilton and Zuk (1982) modelof sexual selection is that parasite-free males should producemate attracting displays that are substantially more vigorousand effective than those of their parasitized counterparts.Further, the model predicts that parasite-free males shouldbe preferred as mating partners by females and, as a consequence,should have higher reproductive success than their parasitizedcompetitors. Gray treefrogs (Hyla versicolor) constitute anideal species for testing both assumptions and predictions ofthe Hamilton-Zuk model in that: (i) mate attraction by malesrequires the production of energetically costly calls and (ii)males of this species have been shown to harbor a wide rangeof helminth parasites. The present paper summarizes resultsof analyses of calling and mating behavior by male gray treefrogsin relation to their parasite infection levels. In general,these analyses revealed no consistent relationship between thenumber and kinds of parasites harbored by males and either theduration or duty-cycle (a direct measure of energetic cost)of their calls. Furthermore, males found in amplexus (i.e.,males actually selected as mating partners by females) showeda slightly higher prevalence of parasite infection (but a slightlylower intensity of infection) than did a comparable sample ofunmated males. In sum, the present study failed to support themajor within-species prediction of the Hamilton-Zuk model ofsexual selection and also calls into question one of the fundamentalassumptions of the model.     

Mate Choice and the Origin of Menopause

Human menopause is an unsolved evolutionary puzzle, and relationships among the factors that produced it remain understood poorly. Classic theory, involving a one-sex (female) model of human demography, suggests that genes imparting deleterious effects on post-reproductive survival will accumulate. Thus, a ‘death barrier’ should emerge beyond the maximum age for female reproduction. Under this scenario, few women would experience menopause (decreased fertility with continued survival) because few would survive much longer than they reproduced. However, no death barrier is observed in human populations. Subsequent theoretical research has shown that two-sex models, including male fertility at older ages, avoid the death barrier. Here we use a stochastic, two-sex computational model implemented by computer simulation to show how male mating preference for younger females could lead to the accumulation of mutations deleterious to female fertility and thus produce a menopausal period. Our model requires neither the initial assumption of a decline in older female fertility nor the effects of inclusive fitness through which older, non-reproducing women assist in the reproductive efforts of younger women. Our model helps to explain why such effects, observed in many societies, may be insufficient factors in elucidating the origin of menopause.     

Spatio-Temporal Dynamics of Field Cricket Calling Behaviour: Implications for Female Mate Search and Mate Choice

Amount of calling activity (calling effort) is a strong determinant of male mating success in species such as orthopterans and anurans that use acoustic communication in the context of mating behaviour. While many studies in crickets have investigated the determinants of calling effort, patterns of variability in male calling effort in natural choruses remain largely unexplored. Within-individual variability in calling activity across multiple nights of calling can influence female mate search and mate choice strategies. Moreover, calling site fidelity across multiple nights of calling can also affect the female mate sampling strategy. We therefore investigated the spatio-temporal dynamics of acoustic signaling behaviour in a wild population of the field cricket species Plebeiogryllus guttiventris. We first studied the consistency of calling activity by quantifying variation in male calling effort across multiple nights of calling using repeatability analysis. Callers were inconsistent in their calling effort across nights and did not optimize nightly calling effort to increase their total number of nights spent calling. We also estimated calling site fidelity of males across multiple nights by quantifying movement of callers. Callers frequently changed their calling sites across calling nights with substantial displacement but without any significant directionality. Finally, we investigated trade-offs between within-night calling effort and energetically expensive calling song features such as call intensity and chirp rate. Calling effort was not correlated with any of the calling song features, suggesting that energetically expensive song features do not constrain male calling effort. The two key features of signaling behaviour, calling effort and call intensity, which determine the duration and spatial coverage of the sexual signal, are therefore uncorrelated and function independently.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

Turbidity Hampers Mate Choice in a Pipefish

European coastal waters have in recent years become more turbid as algal growth has increased, probably due to eutrophication, global warming and changes in fish communities. Turbidity reduces visibility, and such changes may in turn affect animal behaviour as well as evolutionary processes that are dependent on visual stimuli. In this study we experimentally manipulated water visibility and olfactory cues to investigate mate choice using the sex role‐reversed broad‐nosed pipefish Syngnathus typhle as our study organism. We show that males spent significantly longer time assessing females when they had access to full visual cues, compared to when visibility was reduced. Presence or absence of olfactory cues from females did not affect mate choice, suggesting that the possible use of smell could not make up for a reduction in visibility. This implies that mate choice is environmentally dependent and that an increased turbidity may affect processes of sexual selection through an impaired possibility for visually based mate choice.     

Song Repertoire and Mate Choice in Birds

In many species of birds, individual males possess "repertoires"of multiple versions of the species song. Females of severalof these species have been shown to respond preferentially incourtship to larger song repertoires. The female preferencefor large repertoires usually has little effect on female settlement,but is likely to affect mate choice in extra-pair copulations.A number of hypotheses have been proposed to explain the evolutionof the female preference. Some of these posit a natural selectiveadvantage for the preference, in securing for the female a betterterritory, better paternal care for the offspring, or a matewith good genes. Another hypothesis suggests the male traitand female preference have coevolved in a process of runawaysexual selection. Here I show that female common grackles (Quiscalus quiscula)court preferentially for repertoires of four song types comparedto equal numbers of repetitions of single song types.The femalepreference exists in common grackles despite the fact that malesin this species sing only one song type each. None of the usualhypotheses, based on natural or sexual selection, can explainthe occurrence of the female preference in a species in whichmales lack the preferred trait. Instead, the female preferencemay be a simple consequence of two properties of most responsesystems: habituation and stimulus specificity. If so, femalepreferences for repertoires may in general pre-date the evolutionof male song repertoires, which evolve to exploit the pre-existingfemale response bias.