Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprinting's potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such 'magic traits' easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster father's species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.     

Evidence of phenotypic and social assortative mating for anthropometric and physiological traits in couples from the Basque country (Spain)

This study examined 28 anthropometrical and physiological traits in 107 married couples living in the province of Biscay (Basque Country, Spain). The aim was to verify the existence of a phenotypic and/or social preference when choosing a mate. For this, correlations between pairs of spouses were estimated by maximum likelihood, and a model of familial transmission (path analysis) was applied in order to test if social homogamy between mates existed. The results provide significant evidence of phenotypic as well as social homogamy in several of the studied traits. Even if an assortment existed when choosing a mate for bony traits such as height, the effect of cohabitation cannot be discounted as the main causal factor for the high phenotypic resemblance observed between spouses for body composition traits. In addition, with the social homogeneity of the studied sample, significant evidence of the existence of social homogamy between mates was only found for 20% of the studied variables.     

Human Homogamy in Facial Characteristics

Human homogamy may be caused in part by individuals' preference for phenotypic similarities. Two types of preference can result in homogamy: individuals may prefer someone who is similar to themselves (self-referent phenotype matching) or to their parents (a sexual-imprinting-like mechanism). In order to examine these possibilities, we compare faces of couples and their family members in two ways. First, "perceived" similarity between a pair of faces is quantified as similarity ratings given to the pair. Second, "physical" similarity between two groups of faces is evaluated on the basis of correlations in principal component scores generated from facial measurements. Our results demonstrate a tendency to homogamy in facial characteristics and suggest that the tendency is due primarily to self-referent phenotype matching. Nevertheless, the presence of a sexual-imprinting-like effect is also partially indicated: whether individuals are involved in facial homogamy may be affected by their relationship with their parents during childhood.     

Sexual imprinting can induce sexual preferences for exaggerated parental traits

Sexual preferences in animals are often skewed toward mates with exaggerated traits. In many vertebrates, parents provide, through the learning process of "sexual imprinting," the model for the later sexual preference. How imprinting can result in sexual preferences for mates having exaggerated traits rather than resembling the parental appearance is not clear. We test the hypothesis that a by-product of the learning process, "peak shift", may induce skewed sexual preferences for exaggerated parental phenotypes. To this end, zebra finch (Taeniopygia guttata) males were raised by white parents, with beak color as the most prominent sexual dimorphism. We manipulated this feature with nail varnish. At adult age, each male was given a preference test in which he could choose among eight females with beak colors ranging from more extreme on the paternal to more extreme on the maternal side. The males preferred females with a beak of a more extreme color than that of their mothers, i.e., they showed a peak shift. Sexual imprinting can thus generate skewed sexual preferences for exaggerated maternal phenotypes, phenotypes that have not been present at the time of the learning. We suggest that such preferences can drive the evolution of sexual dimorphism and exaggerated sexual traits.     

The coevolution of sexual imprinting by males and females

Sexual imprinting is the learning of a mate preference by direct observation of the phenotype of another member of the population. Sexual imprinting can be paternal, maternal, or oblique if individuals learn to prefer the phenotypes of their fathers, mothers, or other members of the population, respectively. Which phenotypes are learned can affect trait evolution and speciation rates. “Good genes” models of polygynous systems predict that females should evolve to imprint on their fathers, because paternal imprinting helps females to choose mates that will produce offspring that are both viable and sexy. Sexual imprinting by males has been observed in nature, but a theory for the evolution of sexual imprinting by males does not exist. We developed a good genes model to study the conditions under which sexual imprinting by males or by both sexes can evolve and to ask which sexual imprinting strategies maximize the fitness of the choosy sex. We found that when only males imprint, maternal imprinting is the most advantageous strategy. When both sexes imprint, it is most advantageous for both sexes to use paternal imprinting. Previous theory suggests that, in a given population, either males or females but not both will evolve choosiness in mating. We show how environmental change can lead to the evolution of sexual imprinting behavior by both sexes in the same population.     

Facialmetric similarities mediate mate choice: sexual imprinting on opposite-sex parents

Former studies have suggested that imprinting-like processes influence the shaping of human mate preferences. In this study, we provide more direct evidence for assessing facial resemblance between subjects' partner and subjects' parents. Fourteen facial proportions were measured on 312 adults belonging to 52 families, and the correlations between family members were compared with those of pairs randomly selected from the population. Spouses proved to be assortatively mated in the majority of measured facial proportions. Significant correlations have been found between the young men and their partner's father (but not his mother), especially on facial proportions belonging to the central area of the face. Women also showed resemblance to their partner's mother (but not to their father) in the facial characteristics of their lower face. Replicating our previous studies, facial photographs of participants were also matched by independent judges who ascribed higher resemblance between partners, and subjects and their partners' opposite-sex parents, compared with controls. Our results support the sexual imprinting hypothesis which states that children shape a mental template of their opposite-sex parents and search for a partner who resembles that perceptual schema. The fact that only the facial metrics of opposite-sex parents showed resemblance to the partner's face tends to rule out the role of familiarity in shaping mating preferences. Our findings also reject several other rival hypotheses. The adaptive value of imprinting-related human mating is discussed, and a hypothesis is made of why different facial areas are involved in males' and females' search for resemblance.     

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.     

Sexual imprinting on a novel trait in the dimorphic zebra finch: sexes differ

We investigated the effect of a novel trait, a red feather on the forehead, on sexual imprinting in the dimorphic zebra finch, Taeniopygia guttata. Parents reared young in one of four imprinting groups: (1) both parents adorned with the red feather; (2) the father only adorned; (3) the mother only adorned; (4) both parents unadorned. After the young matured, we tested their preference for adorned and unadorned conspecifics of the opposite sex in simultaneous double-choice tests. Females but not males sexually imprinted on the red feather when their parents or father were adorned. In further tests, females that had sexually imprinted on the red feather did not generalize from the learned preference for a red feather to a preference for an orange or blue feather. Neither males nor females reared by unadorned parents showed a latent preference for potential mates adorned with a red, orange, or blue feather. Our results show that in the dimorphic zebra finch, only females sexually imprint on a novel trait. Sexual imprinting can support the evolution of novel male traits and would enhance the dimorphism in this species.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY,BODY SIZE,AND VIABILITY

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.     

Song, sex and sensitive phases in the behavioural devebpment of birds

A number of parallels can be drawn between song learning and sexual imprinting, but how do the two processes interact during development? In zebra finches, the only species for which there are data on both song learning and sexual imprinting, an important difference between the two processes is that song learning usually occurs after the birds have sexually imprinted. Does sexual imprinting influence subsequent song tutor choice? Recent work comparing the song and sexual preferences of individual males suggests that a male does not necessarily choose a song tutor who is of the same species as he has sexually imprinted on.     

Mating system and demographic constraints on the opportunity for sexual selection

In monogamous systems the fitness difference between males due to competition for mates is limited to one female. This constraint presumably impedes the action of sexual selection relative to polygynous systems. In this paper, we use formal selection theory to show how population size and the adult sex ratio constrain the force of sexual selection and phenotypic evolution under monogamy and polygyny. The force of sexual selection is ultimately constrained by the number of males in a population and the theoretical limit to the rate of male phenotypic evolution is realized if a single male mates with one or many females. These results imply that the force of sexual selection is not strictly constrained by monogamy. The constraint on female phenotypic evolution is typically higher than the constraint on males under polygyny and similar to selection on males in monogamous systems. The sexual asymmetry in the force of selection under polygyny--not necessarily weak sexual selection on males of monogamous systems--may explain the prominence of sexual dimorphism in polygynous systems.     

Genetic and environmental sources on familial transmission in Biscayan families – III. The dynamometric strength

The present research analyses a cross-sectional sample of 284 individuals (86 fathers, 86 mothers, 54 sons and 58 daughters) in 86 nuclear families living in the province of Biscay (Basque Country, Spain), with the aim of estimating both transmissible and non-transmissible components acting on familial resemblance for the maximum dynamometric strength of both hands, by means of a path analysis. Standardised data of each generation and sex were adjusted to a BETA model of path analysis independent of sex effects, allowing nevertheless the possibility to differentiate between transmissible (genetic and cultural) and non-transmissible (environmental) components acting on the observed phenotypic variance in Biscayan offspring. The results supported the full model of familial transmission for the two variables, in addition to other reduced models that gave rise to transmission effects regardless of any influence from the siblings' shared environment on the environmental transmitted component from their parents (b = 0), and without social homogamy between mates (u = 0). The most parsimonious model created, based on the previous ones, was accepted for both traits. The total transmissible variance (t²) explained between 21% (right hand) and 44% (left hand) of the observed phenotypic variation. These values are close to those from the literature (t² = 37%). However, we should take into account that these kinds of estimations are specific for each group or population.     

Differential facial resemblance of young children to their parents: who do children look like more?

In humans, paternal investment is highly variable and is modulated by paternity uncertainty. Facial phenotypic similarity between a father and a child is one possible paternity indicator. However, whether such paternal-biased traits are expressed in children is unclear, as previous empirical results are contradictory. Therefore, we quantified the facial resemblance between a child and each of his or her parents, from birth to 6 years old. Resemblance was assessed from pictures of the face by nonrelated judges. We found that, at all ages, children resemble both their parents more than would be expected by chance, although there is a differential resemblance toward one or the other parent depending on the age and sex of the child. For newborns, boys and girls resemble their mothers more, this differential resemblance persisting through time for girls. For boys, an inversion occurs and they resemble their fathers more between 2 and 3 years of age. The resemblance ascribed by the parents shows that, at birth, mothers ascribe a resemblance to the father, as previously found, although assessment by external judges revealed the opposite. These results suggest that facial appearance is a cue for kin recognition between a father and a child. Patterns of differential resemblance are discussed within the context of evolutionary theories on parental investment.     

Assortative mating can limit the evolution of phenotypic plasticity

Phenotypic plasticity, the ability to adjust phenotype to the exposed environment, is often advantageous for organisms living in heterogeneous environments. Although the degree of plasticity appears limited in nature, many studies have reported low costs of plasticity in various species. Existing studies argue for ecological, genetic, or physiological costs or selection eliminating plasticity with high costs, but have not considered costs arising from sexual selection. Here, we show that sexual selection caused by mate choice can impede the evolution of phenotypic plasticity in a trait used for mate choice. Plasticity can remain low to moderate even in the absence of physiological or genetic costs, when individuals phenotypically adapted to contrasting environments through plasticity can mate with each other and choose mates based on phenotypic similarity. Because the non-choosy sex (i.e., males) with lower degrees of plasticity are more favored in matings by the choosy sex (i.e., females) adapted to different environments, directional selection toward higher degrees of plasticity is constrained by sexual selection. This occurs at intermediate strengths of female choosiness in the range of the parameter value we examined. Our results demonstrate that mate choice is a potential source of an indirect cost to phenotypic plasticity in a sexually selected plastic trait.     

Pedigrees, assortative mating and speciation in Darwin's finches

Pedigree analysis is a useful tool in the study of speciation. It can reveal trans-generational influences on the choice of mates. We examined mating patterns in a population of Darwin's medium ground finches (Geospiza fortis) on Daphne Major Island to improve our understanding of how a barrier to the exchange of genes between populations arises in evolution. Body sizes of mates were weakly correlated. In one year, the smallest females were paired non-randomly with the males of similar size, and in another year the largest males were paired with the largest females. An influence of parental morphology on the choice of mates, as expected from sexual imprinting theory, was found; the body size of mates was predicted by the body sizes of both parents, and especially strongly by the father's. These associations imply that the seeds of reproductive isolation between species are present within a single variable population. The implication was subject to a natural test: two exceptionally large birds of the study species, apparently immigrants, bred with each other, as did their offspring, and not with the members of the resident population. The intense inbreeding represents incipient speciation. It parallels a similar phenomenon when another species, the large ground finch, immigrated to Daphne and established a new population without interbreeding with the resident medium ground finches.     

Female competition and its evolutionary consequences in mammals

Following Darwin's original insights regarding sexual selection, studies of intrasexual competition have mainly focused on male competition for mates; by contrast, female reproductive competition has received less attention. Here, we review evidence that female mammals compete for both resources and mates in order to secure reproductive benefits. We describe how females compete for resources such as food, nest sites, and protection by means of dominance relationships, territoriality and inter‐group aggression, and by inhibiting the reproduction of other females. We also describe evidence that female mammals compete for mates and consider the ultimate causes of such behaviour, including competition for access to resources provided by mates, sperm limitation and prevention of future resource competition. Our review reveals female competition to be a potentially widespread and significant evolutionary selection pressure among mammals, particularly competition for resources among social species for which most evidence is currently available. We report that female competition is associated with many diverse adaptations, from overtly aggressive behaviour, weaponry, and conspicuous sexual signals to subtle and often complex social behaviour involving olfactory signalling, alliance formation, altruism and spite, and even cases where individuals appear to inhibit their own reproduction. Overall, despite some obvious parallels with male phenotypic traits favoured under sexual selection, it appears that fundamental differences in the reproductive strategies of the sexes (ultimately related to parental investment) commonly lead to contrasting competitive goals and adaptations. Because female adaptations for intrasexual competition are often less conspicuous than those of males, they are generally more challenging to study. In particular, since females often employ competitive strategies that directly influence not only the number but also the quality (survival and reproductive success) of their own offspring, as well as the relative reproductive success of others, a multigenerational view ideally is required to quantify the full extent of variation in female fitness resulting from intrasexual competition. Nonetheless, current evidence indicates that the reproductive success of female mammals can also be highly variable over shorter time scales, with significant reproductive skew related to competitive ability. Whether we choose to describe the outcome of female reproductive competition (competition for mates, for mates controlling resources, or for resources per se) as sexual selection depends on how sexual selection is defined. Considering sexual selection strictly as resulting from differential mating or fertilisation success, the role of female competition for the sperm of preferred (or competitively successful) males appears particularly worthy of more detailed investigation. Broader definitions of sexual selection have recently been proposed to encompass the impact on reproduction of competition for resources other than mates. Although the merits of such definitions are a matter of ongoing debate, our review highlights that understanding the evolutionary causes and consequences of female reproductive competition indeed requires a broader perspective than has traditionally been assumed. We conclude that future research in this field offers much exciting potential to address new and fundamentally important questions relating to social and mating‐system evolution.     

Variation in male effects on female fecundity in Drosophila melanogaster

In many species, males have the capacity to directly influence (either positively or negatively) the fitness of their mates and offspring, not only via parental care contributions and/or precopulatory resource provisioning, but also via the post‐copulatory activity of those substances passed on to their mates in their ejaculates. Here, we examine how an individual male's identity may be related to phenotypic variation in short‐term female fecundity in the model species, Drosophila melanogaster. The effect of male identity on short‐term fecundity stimulation of females was repeatable across time and accounted for over a fifth of the total observed phenotypic variation in fecundity in two independent populations. The functional explanations for these results and the implications for our understanding of the factors that contribute to the adaptive significance of mating preferences and/or sexual conflict are discussed.     

Sex-specific responses to sexual familiarity,and the role of olfaction in Drosophila

Studies of mating preferences have largely neglected the potential effects of individuals encountering their previous mates (‘directly sexually familiar’), or new mates that share similarities to previous mates, e.g. from the same family and/or environment (‘phenotypically sexually familiar’). Here, we show that male and female Drosophila melanogaster respond to the direct and phenotypic sexual familiarity of potential mates in fundamentally different ways. We exposed a single focal male or female to two potential partners. In the first experiment, one potential partner was novel (not previously encountered) and one was directly familiar (their previous mate); in the second experiment, one potential partner was novel (unrelated, and from a different environment from the previous mate) and one was phenotypically familiar (from the same family and rearing environment as the previous mate). We found that males preferentially courted novel females over directly or phenotypically familiar females. By contrast, females displayed a weak preference for directly and phenotypically familiar males over novel males. Sex-specific responses to the familiarity of potential mates were significantly weaker or absent in Orco¹ mutants, which lack a co-receptor essential for olfaction, indicating a role for olfactory cues in mate choice over novelty. Collectively, our results show that direct and phenotypic sexual familiarity is detected through olfactory cues and play an important role in sex-specific sexual behaviour.