Fitness Benefits of Mate Choice for Compatibility in a Socially Monogamous Species

Research on mate choice has primarily focused on preferences for quality indicators, assuming that all individuals show consensus about who is the most attractive. However, in some species, mating preferences seem largely individual-specific, suggesting that they might target genetic or behavioral compatibility. Few studies have quantified the fitness consequences of allowing versus preventing such idiosyncratic mate choice. Here, we report on an experiment that controls for variation in overall partner quality and show that zebra finch (Taeniopygia guttata) pairs that resulted from free mate choice achieved a 37% higher reproductive success than pairs that were forced to mate. Cross-fostering of freshly laid eggs showed that embryo mortality (before hatching) primarily depended on the identity of the genetic parents, whereas offspring mortality during the rearing period depended on foster-parent identity. Therefore, preventing mate choice should lead to an increase in embryo mortality if mate choice targets genetic compatibility (for embryo viability), and to an increase in offspring mortality if mate choice targets behavioral compatibility (for better rearing). We found that pairs from both treatments showed equal rates of embryo mortality, but chosen pairs were better at raising offspring. These results thus support the behavioral, but not the genetic, compatibility hypothesis. Further exploratory analyses reveal several differences in behavior and fitness components between “free-choice” and “forced” pairs.     

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.     

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 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.     

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.     

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.     

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.     

Orange Spots as a Visual Cue for Female Mate Choice in the Guppy (Poecilia reticulata)

Previous studies have suggested that orange pigment in the color patterns of male guppies is a cue for female choice. This paper describes a manipulative experiment designed to test this hypothesis. The color patterns perceived by females were manipulated by varying the color of light used to illuminate the experimental aquaria. Orange light dramatically reduces the conspicuousness of orange spots to human observers, and probably also to female guppies. As in previous experiments, female guppies discriminated among males based on differences in the extent of orange pigment, under white, blue, and green light conditions. Under orange light, however, females no longer appeared to discriminate on the basis of orange spots. These results support the hypothesis that orange spots, rather than other correlated characteristics, are a basis for female choice under normal lighting conditions.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

Mate choice by either sex may vary with changes in the associated costs and benefits, determined by factors such as the availability of potential mates and variation in mate quality. We examined seasonal variation in operational sex ratio, courtship behavior, spermatophore mass, egg count, and the relationship between morphological traits and mating success in Photinus ignitus fireflies to determine if mate choice in either sex varied with the availability and relative reproductive investment of fertilizable females and sexually active males. Successfully mating males had larger lanterns than unsuccessful males when the operational sex ratio was male‐biased. In addition, female responsiveness to male signals increased as the number of courting males decreased, and male spermatophore mass decreased with body size across the mating season. Successfully mating females had larger body mass than unsuccessful females. Female body mass predicted egg count and female rejection by males increased as the season progressed and female size decreased. These results suggest that both male and female P. ignitus exhibit mate choice, and that such choice is influenced by seasonal variation in the abundance and quality of potential mates.     

Mate Choice for Non-siblings in Wild House Mice: Evidence from a Choice Test and a Reproductive Test

Two experiments were designed to test whether wild house mice discriminate between olfactory cues from different kin and, if so, whether given preferences would relate to actual reproductive decisions. Experimental animals were mice born to the offspring of wild-caught house mice. Litter-mates stayed together until 60 d of age and were then housed individually. In a choice test, animals were placed in the middle of an arena with 4 openings which led to small cages containing bedding material from opposite-sex animals of known kinship (full-sib, cousin, unrelated) or clean material. Test animals (11 oestrous females, 11 males tested with oestrous females' bedding, 8 males tested with material from non-oestrous females) preferred conspecific to control bedding. Males tested with oestrous females' bedding significantly preferred unrelated to full-sib odours. In a second experiment, 34 males were each mated simultaneously to 3 females (sister, cousin, unrelated) and these groups were then housed together for 5, 10, and 15 d. Females were checked for litters during the next 20 d. Reproductive rate increased significantly in the 15 d cohabitation group, and significantly more cousin and unrelated females than sisters gave birth to a litter.     

Mate Choice and Colored Beak Spots of King Penguins

The theory of sexual selection explains sexual dimorphisms in ornaments used in mate choice. Mutual mate choice is a form of sexual selection that might explain sexually monomorphic ornamental traits. Under mutual mate choice, both sexes select partners based on the same ornament. We tested the mutual mate choice hypothesis in a mutually ornamented seabird, the king penguin (Aptenodytes patagonicus), through observations of the pair formation process in the field. Penguins that were ready to mate formed displaying pairs at the edge of the colony. Some of these pairs moved into the breeding colony and produced an egg (definitive pairs), while other pairs separated and often switched to another potential partner (temporary pairs). Colored ornaments were quantified using color vision modeling. We predicted that birds would mate assortatively by their elaborate ornamental traits (specifically, colors of beak spots, auricular patches of feathers, and breast patch of feathers). We also predicted that definitive pairs would exhibit more elaborate ornaments than temporary pairs. The mutual mate choice hypothesis was supported by assortative pairing for color of the beak spots, but not for color or size of the auricular patches or for the color of the breast patch. An alternative hypothesis was also consistent with our results, that female choice for a male ornamental trait and superior female condition associated with the same trait produced assortative pairing patterns. More UV‐ and yellow‐colored beak spots for females in definitive than temporary pairs supported the female choice hypothesis over the mutual mate choice hypothesis, but previous experimental results from altered beak spot colors supported the latter. Evidence to date thus supports both the mutual mate choice and female choice hypotheses.     

Video Playback Versus Live Stimuli for Assessing Mate Choice in a Pipefish

Synopsis In this study, I investigated the application of the video playback technique to studies on mate choice in the pipefish, Syngnathus typhle. In this sex-role reversed species, the males are predominately the choosing sex, and given a choice, prefer to mate with larger females. As such, I tested if this known mate preference remained when using this novel experimental technique. Specifically, I compared the response of males to video images of females to that of live females. Results revealed that male pipefish showed a stronger preference for the larger female in the video playback treatment than in the clear glass (two-way interaction) live female treatment. This experiment has, therefore, demonstrated that the pipefish respond in the predicted direction in response to video playback, and as such proves to be a reliable method to study mate preferences in this species.     

Mate Choice and Mating Pattern in a Stream Goby of the Genus Rhinogobius

The mate choice and mating pattern of a benthic goby Rhinogobius sp. CB (cross band type) were investigated in the Kamo River, Shikoku, Japan. During the breeding season, gravid females assumed a nuptial color and either males or females initiated a courtship display. Males preferentially courted a female of similar size to lead her to his nest, whereas females courted more frequently when they encountered a large male. Eggs in any one nest were always at the same developmental stage. Sampling data of nesting males and females indicated that, in more than half the nests, males gathered more than one female before spawning. In some nests with eggs, two or three females had spent ovaries, indicating that the eggs were laid by multiple females within a short span of time. However, a comparison between the total number of eggs which females would spawn in one nest and the number of eggs actually deposited suggested that eggs were contributed by one female in most nests. This low level of polygyny in spite of multiple female availability is attributed to a limited available spawning area of the nest.