Major histocompatibility complex and mate choice in a monogamous rodent

A growing number of studies indicate that females can increase the viability of their offspring by gaining direct benefits such as parental care or genetic advantages through selective mating with certain males. Among the best candidates for the genetic basis of mate choice in vertebrates are the genes of the major histocompatibility complex (MHC) because these highly polymorphic genes may increase offspring viability and provide direct cues for mate choice. A free-ranging, pair-living rodent was used as an example to investigate MHC-dependent mate choice in an obligate monogamous species, the Malagasy giant jumping rat Hypogeomys antimena. Two possible mechanisms of mate choice were tested. First, mate choice may occur to increase the heterozygosity of MHC genes in the progeny and, second, mates might choose each other according to the degree of dissimilarity of their functional MHC DRB (exon 2) proteins in order to maximise the allelic divergence in their offspring. Analyses of 65 Hypogeomys couples failed to confirm associations of mating patterns with the MHC genotype to increase heterozygosity or MHC allelic divergence in the progeny. Also, no evidence for mechanisms to increase the allelic divergence was found in sex-specific analyses where a male or female, respectively, migrated to and was accepted by a territory and burrow holder of the opposite sex. However, the frequency distribution of 0, 1 or 2 new alleles potentially available for the progeny differed significantly when a new male was chosen by a territory-holding female. In contrast to current models, genetically similar instead of dissimilar mates seem to be the preferred choice. This is the first study investigating the role of the MHC in mate selection in an obligate monogamous rodent.Communicated by G. Wilkinson     

Consequences of Low Mate Availability in the Rare Self-Incompatible Species Brassica insularis

Abstract:  Self-incompatibility systems prevent self-fertilization in angiosperms. Although numerous S alleles are usually maintained by negative frequency-dependent selection, the number of S alleles can be low in small populations, which limits mate availability and reduces fecundity in endangered populations of self-incompatible plants. Despite the increasing evidence of the negative effect of self-incompatibility in small populations, the direct link between the number and the distribution of S alleles and their reproductive consequences has been rarely reported. Brassica insularis is a rare self-incompatible species with medium to very small populations. Results of a previous study showed that the smallest population has very few S alleles. We investigated whether reduced mate availability affects reproduction in this species. We compared the pollination success and the fruit set in 4 populations differing in population size and number of S alleles. Our results suggest that reproduction may be negatively affected by the low S-allele diversity in the smallest population. Nevertheless, other populations also had reduced fruit set that could not be attributed to self-incompatibility alone.     

Olfactory cues,genetic relatedness and female mate choice in the agile antechinus (<Emphasis Type="Italic">Antechinus agilis</Emphasis>)

Females show mate preferences for males that are genetically dissimilar to themselves in a variety of taxa, but how females choose these males is not clearly understood. In this study, we examined the effects of olfactory stimuli and genetic relatedness on female mate choice in a small carnivorous marsupial, the agile antechinus (Antechinus agilis), during two breeding seasons. Captive female antechinus in oestrus were provided with a combination of male urine and body scent from two novel males, one more genetically similar and one more dissimilar to the females, in a Y-maze olfactometer. Genetic relatedness between females and pairs of males was determined using highly polymorphic, species-specific, microsatellite markers. Females consistently chose to visit the scents of males that were genetically dissimilar to themselves first, spent significantly more time near the source of those scents and showed more sexual and non-exploratory behaviours near those scents. These data demonstrate that chemosensory cues are important in mate choice in the agile antechinus and that females prefer males that are genetically dissimilar to themselves.     

UV wavelengths make female three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>) more attractive for males

Numerous fishes possess UV vision and show UV patterns, which often play a role in social communication, especially during courtship. UV light is scattered strongly in water and thus might be used for intra-specific close-range communication without being detected by predators. In addition to the red-belly colouration and blue-coloured iris, male three-spined sticklebacks possess UV reflectance on their skin, and females prefer males presented with UV light rather than without. To investigate whether UV also influences male visual preference for females in this species, we used a dichotomous mate choice design in which one female could be viewed by a male in two visual conditions. Courting male sticklebacks preferred females that were presented in full-spectrum conditions including UV to the same females presented in conditions lacking this light component. Furthermore, control trials with neutral-density filters indicated that male preference in the UV treatment was not affected by a difference in achromatic brightness between the UV+ and UV− stimuli. Reflectance measurements of gravid females suggest an enhanced UV contrast between the dark bar pattern, which is characteristic of gravid females, and silvery body parts.     

Sequential female choice and the previous male effect in sticklebacks

Summary Female choice, identified as a major force in sexual selection theory, has recently been demonstrated in a number of species. These tests concentrated on simultaneous choice situations although females have to compare males sequentially in most territorial species, which is the more demanding task. Here it is shown that female three-spined sticklebacks, Gasterosteus aculeatus L., rate sequentially presented males according to their brightness. With increasing costs of sampling the females become less choosy. Furthermore, a male's attractiveness has a significant effect on the female's rating of the next male; a given male is rated higher when preceded by a duller male than by a brighter one and vice versa. Female sticklebacks use a stochastic decision rule in sequential mate choice that is attuned to the attractiveness of the present and previously encountered male. This demonstration of a previous male effect not only indicates an efficient mechanism for finding the best of a number of males but also extends the applicability of sexual selection theory.Offprint requests to: T.C.M. Bakker     

Female preference for symmetry in computer-animated three-spined sticklebacks,<Emphasis Type="Italic"> Gasterosteus aculeatus</Emphasis>

Fluctuating asymmetries are subtle random deviations from perfect symmetry in bilateral traits caused by the inability of individuals to buffer their development against the disruptive effects of genetic and environmental stresses. The degree of asymmetry of secondary sexual characters is supposed to convey information about a male's phenotypic and/or genetic quality, and females may thus be expected to use bilateral symmetry as a cue in mate choice. We independently and simultaneously manipulated the length and the relative symmetry of the pelvic spines of computer-animated three-spined sticklebacks, Gasterosteus aculeatus. In all mate choice tests involving two male models differing in spine symmetry, females preferred the symmetric model, irrespective of spine length, though only significantly so when both male models had short spines. Females did not significantly discriminate between male models differing in spine length alone. The preference for symmetry was stronger the higher the females' physical condition. Our study demonstrates that female sticklebacks master the perceptual abilities required to discriminate between potential mates basing exclusively on small length differences between paired structures, and provides experimental evidence that spine symmetry is subject to sexual selection through female choice in this species.     

Sexual coercion by male chimpanzees shows that female choice may be more apparent than real

The extent to which active female mating preferences influence male reproductive success in mammals is unclear, particularly for promiscuously breeding species like chimpanzees (Pan troglodytes). Previous studies from multiple long-term study sites have shown that female chimpanzees mate more restrictively around ovulation, and this has been taken as evidence for female choice. However, none of these studies rigorously evaluated the alternative hypothesis that restrictive mating results not from unconstrained choice, but in response to coercive mate guarding, in which males use punishment and intimidation to reduce female promiscuity and promote their own mating interests. Nor did they consider evidence for the potential genetic or phenotypic benefits that females might be choosing. Using 11 years of data from the Kanyawara community in Kibale National Park, Uganda, we previously demonstrated that males achieve elevated mating success with those females toward whom they direct high levels of aggression. Here we extend those findings to show that even female copulatory approaches, which have previously been attributed to female choice, are correlated with male aggression. Specifically, individual females at our site initiated periovulatory copulations most frequently with the males who were most aggressive toward them throughout their cycles. Those males showed high rates of aggression toward females throughout estrus, despite achieving high copulation rates, demonstrating a continuing conflict of interest over the exclusivity of mating access. Because sexual coercion is potentially widespread in primates and other mammals, our results stress the importance of considering the influence of male aggression in studies of female choice.     

No evidence of mate discrimination against males carrying a sex ratio distorter in <Emphasis Type="Italic">Drosophila pseudoobscura</Emphasis>

Selfish genetic elements (SGEs) that spread by manipulating spermatogenesis often have highly deleterious effects on males that carry them. Females that mate with male carriers of SGEs can also suffer significant costs: they receive fewer and poorer-quality sperm, their offspring will inherit the deleterious allele, and the sex ratio of their offspring will be biased towards the more common sex. To counter these costs, females are therefore expected to prefer to mate with males that do not carry sex ratio distorters or other deleterious selfish genetic elements. However, despite the potential costs, there are few examples of female choice against males carrying SGEs. We searched for evidence of a female preference in fruit fly Drosophila pseudoobscura against males carrying a costly meiotic driving X-chromosome Sex Ratio (SR). In a series of five non-competitive mate preference experiments, we find no evidence that females prefer to mate with non-SR males. Our use of five separate experiments, involving more than 800 females, makes it unlikely that this lack of a difference was due to low power or simple chance. We suggest that the lack of female choice against SGE-carrying males may be due to strong selection on SGEs to be indistinguishable from alternative alleles. Furthermore, polyandry, either in direct response to receiving an ejaculate from an SGE-carrying male or carried out indiscriminately when at risk of mating with carriers, may be an alternative response by females to limit the exposure of their offspring to SGEs.     

Variance in female quality, operational sex ratio and male mate choice in a bushcricket

Male bushcrickets, Kawanaphila nartee, exercise mate choice when nutrients are limited. Male mate choice is associated with a female-biased operational sex ratio (OSR) that arises from an increased relative paternal investment under nutrient limitation. However, increased male choosiness could be attributable to the fact that females vary more in fecundity, and consequently in mate quality, when nutrient limited. Our objective was to experimentally partition the influences of OSR (male or female bias) and variance in mate quality (high or low) and to assess their relative influence on the intensity of mate choice by male bushcrickets. Female quality was manipulated by controlled feeding regimes that directly affected female fecundity. We found that males and females engaged in sexual interactions sooner under a male-biased than a female-biased OSR. Males were more likely to reject females on their first encounter when variance in female quality was high. However, the effect of quality variance on the total number of rejections during a 4-h observation period was dependent on the perceived OSR. A male's prior experience of variance in female quality did not influence male choosiness. Our observed rates of mate rejection conformed well with those predicted from recent theoretical models of sexual differences in choosiness. In conclusion, our results show that the opportunity for selection via male mate choice is influenced by an interaction between OSR and the variance in mate quality that arises within nutrient-limited populations of females. Received: 5 January 1998 / Accepted after revision: 25 October 1998     

Sexual voyeurs and copiers: social copying and the audience effect on male mate choice in the guppy

In most mating systems, males and females are commonly within signalling and receiving distance of conspecifics during courtship and mating activities. Although it is well known that females who observe sexual interactions between conspecifics will use public information obtained from these interactions when making their own mating decisions, much less is known about whether males use this type of information in making mating decisions. We used the Trinidadian guppy (Poecilia reticulata) to test whether males use public information to (i) copy the apparent mate choice of another male and (ii) modify their mating preference for a given female in the presence of one or two sexual rivals (potential copiers). We show that males use public information to copy the mate choice of other males and that males alter their mating preferences in response to the presence of an audience of sexual rivals, but find no evidence of a stronger audience effect when the number of sexual rivals increases. Collectively, these results indicate that males pay attention to their immediate social environment in making mating decisions and suggest that they avoid having another male copy their mate choice by weakening or even reversing their initial mating preference in the presence of eavesdropping male sexual competitors. Our findings highlight the importance of social context and public information in male mate-choice decisions and have implications for the evolution of male mating preferences and of social information use in populations.     

No male agonistic experience effect on pre-copulatory mate choice in female earwigs

Mating with dominant males may confer considerable benefits, but also incur significant costs, hence intrasexual competitiveness is a likely target of mate choice. In addition to established modes of mate assessment, females may use cues or signals associated with agonistic experience effects to assess the relative competiveness of males. Experience effects, where the outcome of a fight increases the likelihood of a similar outcome in subsequent fights, may result from an animal’s altered state after conflict, but can also arise from strategic rival use of information perceived about this altered state. While females may similarly use this information in mate choice decisions, this potential consequence of male–male conflict has largely been neglected. Here, we investigate the effects of experience on subsequent agonistic performance in the earwig Euborellia brunneri by imposing winning or losing experiences on males and rematching them with naïve, size-matched rivals. We reveal a strong loser effect in subsequent fights, with nearly all previous “losers” losing against new rivals. In contrast, we found no equivalent winner effect, with previous “winners” exhibiting no increased likelihood of winning. We subsequently test whether the effects of male agonistic experience extend to pre-copulatory female mate choice. We show that females, when allowed to choose between naïve males and “winners” or “losers”, do not discriminate between males based on their recent agonistic experience. Therefore, while fighting history can play an important role in male–male interactions, females may not attend to this information.     

The artistic three-spined stickleback (<Emphasis Type="Italic">Gasterosteous aculeatus</Emphasis>)

We investigated whether female three-spined sticklebacks ( Gasterosteus aculeatus) are more attracted to a male whose nest contains colourful artificial material than to a nest that only contains algae. The purpose was to examine whether nest characters are of importance for female choice in the three-spined stickleback. Most studies on female preference in this species have focused on male morphological traits. In our study, on a marine population of three-spined stickleback on the West coast of Sweden, we found that males marked their nests' entrance with a deviant colour of algae — an apparent decoration. Moreover, males also decorated their nests with shiny and colourful foil sticks and spangles when provided with such, thereby apparently reducing the nest camouflage. In a mate choice experiment, females were more attracted to males with nests containing sticks and spangles than to males with undecorated nests. Nest decoration may be important for the evolution of paternal care in this species: if males advertise their paternal skills by ornamenting their nest they will receive more matings than males with dull nests.     

Social feedback and attractiveness in zebra finches

The attractiveness of an individual (i.e. its ability to arouse interest in a potential mate) has important implications for its reproductive success. However, attractiveness is not a fixed trait. Previous work has shown that male birds can adjust the intensity of their courtship display in response to variation in female behaviour, but little is known about how males adjust their behaviour during mate choice in response to social feedback about their own attractiveness independent of their intrinsic quality. Such information may help to maximize the potential mating success of males. Here, we provide experimental evidence that the amount of attention given by male zebra finches to females is dependent upon the manipulated attractiveness of males. This demonstrates that, in this socially monogamous species of bird, attractiveness of males could be considered to be a social construct, at least partially determined via social feedback from females.     

Female association preferences based on olfactory cues in the guppy,<Emphasis Type="Italic"> Poecilia reticulata</Emphasis>

Guppies are highly sexually dimorphic. Females have been shown to mate preferentially with males with various visible traits and previous studies investigating mate choice have focussed on these visual cues. However, guppies have been shown to respond behaviourally to odour cues from conspecifics as well as from predators. Therefore, sexual selection in guppies may act on multiple sensory modalities, but so far only visual cues have been investigated. Here, we used a specially designed olfactory choice tank to determine whether females could detect other guppies on the basis of their olfactory cues only, and to determine whether females preferred to associate with males or females and whether they could distinguish between different males. We show that female guppies associated preferentially with other females when given a choice between water containing the odour cues from another fish and water containing no odour cues. When females were presented with olfactory cues from a male and a female, they investigated the female initially, but then most reversed their decision and swam to the male. Furthermore, we demonstrate that females associated preferentially with certain males based upon olfactory cues alone, but that this choice was in direct opposition to that made when the females received only visual cues from the same males.Communicated by: M. Abrahams     

Mate choice by female white-crowned sparrows in a mixed-dialect population

Summary It has been argued that the song dialects of white-crowned sparrows, Zonotrichia leucophrys, may function to restrict gene flow between dialect populations, thus promoting adaptation to local environmental conditions. One proposed mechanism whereby this may occur is if a female mates preferentially with males singing her natal dialect, typically the song type of her father. Previous field and laboratory studies of the role played by song differences in mate choice by female white-crowned sparrows have produced equivocal results. These investigations were conducted in populations in which a single song dialect was predominant. We examined mate choice in a population in which two song dialects are equally common. We found that songs of mates of individual females in successive years were no more likely to be of the same dialect than expected by chance. In addition, individual females did not mate preferentially with males whose songs matched those of their fathers. We conclude that, in this population, females choose mates on the basis of characteristics other than song type.     

Reversed parasite-mediated selection in sticklebacks from eutrophied habitats

Sexual selection is often assumed to increase the viability of populations by increasing the quality of offspring produced. Presently, human-induced environmental changes are altering the process of sexual selection by influencing male–male interactions and female mate choice. Here, we show that increased density of filamentous algae due to eutrophication reverses parasite-mediated selection during reproduction in threespine sticklebacks (Gasterosteus aculeatus). When we manipulated the density of artificial algae in a breeding area in the Baltic Sea, more males nested in dense than in sparse vegetation, but the males in dense vegetation were more parasitized. Interestingly, heavily parasitized males acquired more eggs than less parasitized males in dense vegetation but not in sparse vegetation. The higher probability of reproduction for parasitized males in dense algae growth could be due to impaired visibility relaxing male–male competition or reducing female choosiness. This could favour males in poor condition that often invest more in attracting females than males in good condition. In sparse vegetation, parasitized males may have a lower reproductive success due to intense male–male competition, careful female choice and high predation rate selecting against parasitized males. The results suggest that eutrophication could alter the fraction of the population that reproduces, which could have long-term evolutionary consequences.     

"Cryptic" direct benefits of mate choice: choosy females experience reduced predation risk while in precopula

Despite the central role that female mate choice plays in the production of biological diversity, controversy remains concerning its evolution and maintenance. This is particularly true in systems where females are choosy but do not receive obvious direct benefits such as nuptial gifts that increase a female's survival and fecundity. In the absence of such direct benefits, indirect benefits (i.e., the production of superior offspring) are often invoked to explain the evolution of mate choice. However, females may receive less obvious, or "cryptic," direct benefits, particularly in species with prolonged pre-mating interactions (e.g., precopulatory mate guarding). We assessed the “cryptic” direct benefits of female choice for large male size in two species of freshwater amphipods that do not receive obvious direct benefits. Females paired with large males experienced decreased predation from fish. However, we found that the size of a female’s mate did not affect her predation risk against predatory dragonflies or the harassment she received by single males while paired. Our results demonstrate that even when females receive no traditional direct benefits, female choice for large male size can still provide important direct benefits. Such “cryptic” direct benefits may be common, especially in species with prolonged mating interactions, and are likely important for fully understanding the evolution of mate choice.     

Responses of female lizards,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>, to males' chemical cues reflect their mating preference for older males

Female mate choice based on visual traits appears to be rare in lizards. Field observations suggest that females of the lizard Lacerta monticola preferred to mate with larger/older males. Although older males are usually green and larger, and younger males brown and smaller, there is some overlap in size and coloration between age classes. Thus, visual cues may not always be reliable indicators of a male's age. We hypothesized that female mate-choice preferences may be based on males' pheromones, which might transmit information about characteristics such as age. In a laboratory experiment, we analyzed the effect of age of males on attractiveness of their scents to females. When we offered scents of two males of different age, females associated preferentially with scents of older males. This suggested that females were able to assess the age of males by chemical signals alone, and that females preferred to be in areas scent-marked by older males. Thus, females may increase their opportunities to mate with males of high quality, or may avoid harassment by sneaking young males. This result agreed with field observations on females mating with old males, and rejection of advances by young males. Our results also suggested that female preference for older males may depend on their own body size. Large females showed a strong preference for older males, whereas smaller females were not so selective. This, together with males' preference for large females, might lead to size-assortative matings. We suggest that the quality and/or quantity of male pheromones could communicate to the female heritable male genetic quality (i.e. age) and thereby serve as the basis of adaptive female choice in lizards.Communicated by W.E. Cooper     

Manipulation of Olfactory Signaling and Mate Choice for Conservation Breeding: a Case Study of Harvest Mice

Abstract:  Mate choice by females can introduce difficulties to captive breeding programs because there may be a conflict between the conservation manager's choice of mate (based on random allocation or maximizing heterogeneity) and the females' own preferences, often resulting in incompatibility and aggression. Similar effects are caused by inappropriate social contexts at the time of pairing. We manipulated the social experience of male and female harvest mice ( Micromys minutus ) to investigate whether we could enhance compatibility between randomly allocated mates by altering female preferences. In one experiment, we used a choice test to identify female preferences between two males and then varied the competitive context of unpreferred males by transferring competitor's scent marks into their cages. The manipulation caused them to increase their investment in a form of olfactory signaling (scent marking), which female rodents use as an indicator of male quality when choosing mates. The manipulation increased their attractiveness relative to the initially preferred male when the choice test was repeated. In a second experiment, we tested the effect of females' familiarity with the odor of males by transfer of male scent marks to female cages. Females preferred familiar males in choice tests and were less aggressive toward them when pairs were introduced than females paired with unfamiliar males. This kind of approach can influence mate choice, and transferring scent marks between cages or collections is an effective and practical behavioral means of improving success in conservation breeding programs.     

Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (<Emphasis Type="Italic">Microcebus murinus</Emphasis>)

Sex-specific interests over the maximization of reproductive success lead to an inter-sexual conflict over the optimal mating system in a species. Traditionally, the outcome of this inter-sexual conflict has been studied from the male perspective but it also depends on female mating strategies, such as manipulating the temporal distribution of sexual activity, advertisement, and mate choice. We used a small nocturnal primate, the gray mouse lemur (Microcebus murinus) to determine the relative importance of female mating strategies on the outcome of this conflict in a species where females are solitary during their activity period. We studied their mating behavior over three consecutive annual mating seasons and determined the genetic relationships among more than 300 study animals to quantify individual reproductive success. We found that most females were receptive asynchronously. Females did not exhibit any obvious direct mate choice, probably due to a highly male-biased operational sex ratio and the corresponding costs of choosiness. However, females exercised indirect choice for multiple matings. They mated with 1–7 males up to 11 times during their single night of receptivity. As a result, mixed paternity was common but heavier males sired more offspring, meaning that indirect female choice for superior males cannot be excluded. Females exhibited a mixed mating strategy, avoiding costly direct mate choice but still counteracting male efforts to monopolize mating, successfully increasing genetic variability among offspring. Thus, females had a major influence on the outcome of the inter-sexual conflict despite male monopolization attempts.Communicated by J. Setchell