Variation In Male Quality Research Articles

Multiple biological mechanisms result in correlations between pre- and post-mating traits that differ among versus within individuals and genotypes.

Reproductive traits involved in mate acquisition (pre-mating traits) are predicted to covary with those involved in fertilization success (post-mating traits). Variation in male quality may give rise to positive, and resource allocation trade-offs to negative, covariances between pre- and post-mating traits. Empirical studies have yielded mixed results. Progress is hampered as researchers often fail to appreciate that mentioned biological mechanisms can act simultaneously but at different hierarchical levels of biological variation: genetic correlations may, for example, be negative due to genetic trade-offs but environmental correlations may instead be positive due to individual variation in resource acquisition. We measured pre-mating (aggression, body weight) and post-mating (ejaculate size) reproductive traits in a pedigreed population of southern field crickets (Gryllus bimaculatus). To create environmental variation, crickets were raised on either a low or a high nymphal density treatment. We estimated genetic and environmental sources of correlations between pre- and post-mating traits. We found positive genetic correlations between pre- and post-mating traits, implying the existence of genetic variation in male quality. Over repeated trials of the same individual (testing order), positive changes in one trait were matched with negative changes in other traits, suggesting energy allocating trade-offs within individuals among days. These findings demonstrate the need for research on pre- and post-mating traits to consider the hierarchical structure of trait correlations. Only by doing so was our study able to conclude that multiple mechanisms jointly shape phenotypic associations between pre- and post-mating traits in crickets.

Male mate choice, male quality, and the potential for sexual selection on female traits under polygyny.

Observations of male mate choice are increasingly common, even in species with traditional sex roles. In addition, female traits that bear the hallmarks of secondary sexual characters are increasingly reported. These concurrent empirical trends have led to the repeated inference that, even under polygyny, male mate choice is a mechanism of sexual selection on female traits. It is often either assumed or argued that in these cases females are competing for males of superior "quality"; females might experience sexual selection under polygyny if they compete for mates that provide either direct or indirect benefits. However, the theoretical foundation of this testable hypothesis remains largely uninvestigated. We develop a population genetic model to probe the logic of this hypothesis and demonstrate that, contrary to common inferences, male mate choice, variation in male quality (in the form of a direct fecundity benefit to females), and female ornamentation can coexist in a population without any sexual selection on female ornamentation taking place at all. Furthermore, even in a "best case scenario" where high quality males with a preference for ornamented females are able to mate disproportionately more often with them, the evolution of female traits by sexual selection may be relatively weak. We discuss the implication of these findings for ongoing empirical and theoretical research on the evolution of sexual-signaling in females.

Sexual selection and genital evolution

AbstractMale genitalia show patterns of divergent evolution, and sexual selection is recognised as being responsible for this taxonomically widespread phenomenon. Much of the empirical support for the sexual selection hypothesis comes from studies of insects. Here, I synthesise the literature on insect genital evolution, and use this synthesis to address the debate over the mechanisms of selection most likely to explain observed patterns of macroevolutionary divergence in genital morphology. Studies of seven insect orders provide evidence that non‐intromittent genitalia are subject to sexual selection through their effects on mating success, while intromittent genitalia are subject to selection through their effects on fertilisation success. However, studies that use quantitative methods to analyse the form of selection are necessary to identify the mechanisms of sexual selection involved. Phylogenetic analyses from diverse taxonomic groups confirm that divergence in male genital morphology can be predicted from variation in the opportunity for sexual selection. Much debate revolves around the importance of female choice and sexual conflict in the evolution of male genitalia, the resolution of which lies in economic studies of mating interactions and in recognising sexual selection as a continuum between male competition, sexual conflict and female choice. The species isolating lock‐and‐key hypothesis is frequently dismissed as unimportant in genital evolution because in part of a perceived lack of variation in female genitalia across species. Increasingly, however, studies report species‐specific variation in female genital morphology and its coevolutionary divergence with male genital morphology. Contemporary views recognise a continuum between female choice that enforces species isolation and female choice that targets variation in male quality within populations, placing lock‐and‐key processes into the realm of sexual selection. Distinguishing between species‐isolating and directional forms of female choice will require studies that examine both the tempo and mode of divergence, both within and among species.

Mate Quality and Novelty Influence Post‐Copulatory Female Choice in Decorated Crickets, Gryllodes sigillatus

AbstractFemales of many taxa prefer to mate with novel males rather than previous mates, but also favor males that have traits indicative of higher genetic quality or compatibility. However, it may not be possible for females to simultaneously choose males that are both novel and of high quality, and the female response to this dilemma has not previously been examined. In this paper, we ask whether female decorated crickets, Gryllodes sigillatus, exert their choice for novel males via post‐copulatory choice (sperm ampulla removal) and whether male genetic background (variation in male quality) affects this decision. We found that after matings with inbred males, females removed the ampullae of familiar mates sooner than those of novel males, whereas after matings with outbred males, there was no difference in the ampulla‐retention times of familiar mates and novel partners. This suggests that when male do not vary in quality, females prefer novel partners. However, when males vary in quality, female preferences for male traits are more important than preferences for novel partners.

Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda

We analyzed patterns of paternity and male dominance rank in the Sonso community of wild East African chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Our major objective was to determine whether and how social rank influenced paternity success. We successfully genotyped 52 individuals at up to nine microsatellite loci, using DNA extracted from fecal samples. Of 24 offspring analyzed, we identified sires for 21. Paternity success was significantly correlated with social rank, with alpha males siring a disproportionate number of offspring. However, both middle- and low-ranking males also fathered offspring, and the priority-of-access model provided a relatively poor prediction of which males would be successful and under what circumstances. The concentration of paternities among only seven males and the tendency for high-ranking males to sire offspring of multiparous females suggest that both individual variation in male quality and the resource value of particular females may be mediating factors. In comparison with other chimpanzee studies, our results support the hypothesis that larger male cohort size reduces the ability of the alpha male to monopolize females, though within our study, male number did not affect the success of the alpha. Successful sires were not necessarily those who achieved the highest mating success with the females whose offspring they sired, but were those who demonstrated higher investment by spending significantly more time in association with these females. Finally, we estimate extra-group paternity at 0-5%, supporting other evidence that the community serves as the primary reproductive unit in chimpanzees.

Male Mating Constraints Affect Mutual Mate Choice: Prudent Male Courting and Sperm‐Limited Females

Costs of sperm production may lead to prudence in male sperm allocation and also to male mate choice. Here, we develop a life history-based mutual mate choice model that takes into account the lost-opportunity costs for males from time out in sperm recovery and lets mate competition be determined by the prevailing mate choice strategies. We assume that high mating rate may potentially lead to sperm depletion in males, and that as a result, female reproduction may be limited by the availability of sperm. Increasing variation in male quality leads, in general, to increased selective mate choice by females, and vice versa. Lower-quality males may, however, gain access to more fecund higher-quality females by lowering their courting rate, thus increasing their sperm reserves. When faced with strong male competition for mates, low-quality males become less choosy, which leads to assortative mating for quality and an increased mating rate across all males. With assortative mating, the frequency of antagonistic interactions (sexual conflict) is reduced, allowing males to lower the time spent replenishing sperm reserves in order to increase mating rate. This in turn leads to lower sperm levels at mating and therefore could lead to negative effects on female fitness via sperm limitation.

Predators, reproductive parasites, and the persistence of poor males on leks

Lekking males are thought to face strong directional selection on secondary sexual traits. How variation in male traits can persist under these conditions remains problematic (the lek paradox). Here, we present several game-theoretic models that show that avoidance of costly and mobile predators, sneakers, or brood parasites (enemies) leads to variation in female choice. This can result in maintenance of variation in male quality. ‘‘Enemies’’ will congregate around higher quality males. Females must then trade-off the benefits of mating with high-quality males against the increased risk of enemies. At equilibrium, the models predict a positive correlation between the quality of a male and the proportions of both enemies and females visiting him. In the first model, we use this framework to predict the lowest quality male on the lek that will receive any matings. In the second model, we examine the influence of this female-enemy game on the maintenance of variation in male quality. Low-quality males are likely to persist when enemies are costly to females or occur at high density, and when there is some spatial structure on the lek, so that neighboring males are typically of similar quality. If enemies are more costly to males than to females, high-quality males may benefit from receiving fewer female visits. In the third model, we consider the special case when enemies are male reproductive parasites. These models illustrate the importance of considering the simultaneous decisions of multiple players in mate choice games. Key words: alternative reproductive tactics, genetic variation, harassment, predation risk, sexual selection. [Behav Ecol]

FEMALE SOLDIER BEETLES DISPLAY A FLEXIBLE PREFERENCE FOR SELECTIVELY FAVORED MALE PHENOTYPES

In Georgia (USA) the soldier beetle, Chauliognathus pennsylvanicus (Coleoptera; Cantharidae), exhibits clinal variation in the length of the spot on its elytron. This suggests that the viability of phenotypes varies by habitat. Evidence of viability selection comes from within-site changes in the spot length distribution across a breeding season. When males with spots of intermediate length became less frequent, they became disproportionately less likely to mate, consistent with either a loss of vigor among remaining males or female rejection of disfavored phenotypes. Persistent, daily courtship by males provides females with the opportunity to track changes in male phenotype frequency and to exercise choice for phenotypes favored under natural selection. A laboratory experiment in which the frequency of one spot morph (long) or the other (short) was increased from 25% to 75% over a period of 30 days revealed that females possess a flexible preference that leads them to prefer whichever spot type has become more common over time. A haploid genetic model demonstrates that a flexible female preference for the locally favored male phenotype can be selected for when different viability alleles, genetically correlated with the male trait, are favored in different habitats that are linked by gene flow. Thus, migration between different kinds of habitat patches of a metapopulation could maintain the variation in male quality. This variation favors female choice for any trait that is directly or indirectly favored by natural selection. Such choice imparts positive frequency-dependent selection that could rapidly fix traits pleiotropically linked to viability. Rapid fixation would cause differentiation between populations of colonizing species as females exercise choice for mates favored under new ecological conditions.

FEMALE SOLDIER BEETLES DISPLAY A FLEXIBLE PREFERENCE FOR SELECTIVELY FAVORED MALE PHENOTYPES

In Georgia (USA) the soldier beetle, Chauliognathus pennsylvanicus (Coleoptera; Cantharidae), exhibits clinal variation in the length of the spot on its elytron. This suggests that the viability of phenotypes varies by habitat. Evidence of viability selection comes from within-site changes in the spot length distribution across a breeding season. When males with spots of intermediate length became less frequent, they became disproportionately less likely to mate, consistent with either a loss of vigor among remaining males or female rejection of disfavored phenotypes. Persistent, daily courtship by males provides females with the opportunity to track changes in male phenotype frequency and to exercise choice for phenotypes favored under natural selection. A laboratory experiment in which the frequency of one spot morph (long) or the other (short) was increased from 25% to 75% over a period of 30 days revealed that females possess a flexible preference that leads them to prefer whichever spot type has become more common over time. A haploid genetic model demonstrates that a flexible female preference for the locally favored male phenotype can be selected for when different viability alleles, genetically correlated with the male trait, are favored in different habitats that are linked by gene flow. Thus, migration between different kinds of habitat patches of a metapopulation could maintain the variation in male quality. This variation favors female choice for any trait that is directly or indirectly favored by natural selection. Such choice imparts positive frequency-dependent selection that could rapidly fix traits pleiotropically linked to viability. Rapid fixation would cause differentiation between populations of colonizing species as females exercise choice for mates favored under new ecological conditions.

Female resistance to male seduction in zebra finches

A recent revival of the theory of sexual conflict leads to new interest in the question of how much females control copulation. Using the zebra finch, Taeniopygia guttata, as a model, I investigated the mechanisms with which males tried to persuade females to copulate with them. Analysing the outcome of a large number of experimental male–female encounters, I concluded that apart from some effect of male choosiness (preference for certain females), females were fully in control of copulation. Males did not differ in their abilities to overcome female resistance, either in terms of sensory exploitation (variation in ornamentation and display) or coercion (use of aggression). Variation in beak colour had no influence on male mating success, but male song rate may be a sexually selected trait: males that sang more frequently obtained more copulations, but this was because other males missed opportunities by not even attempting to display to females. Whenever a male started displaying, female responsiveness, and hence male copulatory success, was not influenced by how persistently he sang. These findings support a theory of chase-away sexual selection, rather than a good-genes theory, which has typically been invoked to explain variation in male song rate. Between-individual differences in male song rate may reflect alternative reproductive strategies (mating effort versus parental effort) rather than variation in male quality. Finally, I found marked differences in sexual responsiveness between females, which is not anticipated by current models of sexual selection and hence urges further investigation.

Repeatability of mate choice in the zebra finch: consistency within and between females

Numerous studies have measured the mating preferences of female zebra finches, Taeniopygia guttata, using choice-chamber experiments, but no study has focused on how consistent individual females are in their choices and the extent to which females agree on their preferences, although these questions are of great conceptual importance. We conducted a large number of mate choice trials involving unmanipulated stimulus males, and found low but significant consistency (repeatability of time allocation by a female tested twice with the same set of males R = 0.29), and very low but significant between-female agreement (different females tested with the same set of males: R = 0.11). Although low individual consistency indicates that preferences were relatively weak or hard to measure, we found significant repeatability of individual preference functions with regard to beak colour, song rate and male aggressiveness when individual females were tested twice with different sets of males. This means that some females consistently preferred red-beaked males whereas others preferred orange-beaked males, some preferred high and others low song rates, and some preferred aggressive and others less aggressive males. Of these male traits, only song rate was positively related to average male attractiveness. Low between-female agreement did not seem to result from assortative mating for quality, because there was no repeatability of an individual female's preference for attractive or unattractive males. It is possible that disagreement follows from choice for genetic compatibility, but much of it could also result from weak preferences and little variation in male quality.

Repertoire size, sexual selection, and offspring viability in the great reed warbler: changing patterns in space and time

Only a few studies have focussed on the consistency of sexual selection patterns in space and time. One such case is the great reed warbler (Acrocephalus arundinaceus), for which studies in Germany in 1981–1982 and Sweden in 1987–1991 strongly suggested that the size of a male's song repertoire was the target of mate choice and sexual selection. Studying the same German population once again in 1994–2000, we investigated the consistency of these patterns over time as well as between populations. Our reanalysis of the data from 1981–1982 shows that male repertoire size was positively correlated with male pairing success (harem size) and with clutch size (adjusted for seasonal effects), whereas no such correlations were found during 1994–2000 in the same population. We suggest that the earlier correlations were probably caused indirectly by covariation with territory quality, and that a decline in population size has changed the role of territory quality. In the Swedish population, an earlier study found a striking correlation between the size of a male's repertoire and the viability of its offspring, suggesting good-gene effects. In contrast, we found no such correlation in the German population, neither in 1981–1982 nor in 1994–2000. We conclude that repertoire size does not seem to be a very reliable indicator of variation in male quality. Interestingly, the analysis of data from 1994–2000 showed that male pairing success was strongly correlated with measures of strophe length and immediate versatility, traits that have been found to reflect male longevity. Future studies will have to show whether these performance-related traits are more powerful indicators of male quality than is repertoire size.

Optimal divorce and re-mating strategies for monogamous female birds: a simulation model

Although the extensive variation in divorce rates among monogamous bird species has stimulated several theoretical accounts, the mechanisms underlying divorce strategies remain poorly understood. Here, we use an individual-based simulation model to investigate the adaptiveness of mechanisms of mate choice in the context of remating. Our model compares the fitness of females that choose a mate during each breeding season using one of two different decision rules; “best-of-n” females sample n potential partners and then select the male with the highest quality, whereas “better option” females choose a mate whose quality is maximal among the non-mated individuals they sampled the season before. It is assumed in the model that best-of-n females have no a priori information about the quality of potential partners and systematically decide to divorce at the beginning of each breeding season before searching for a new mate. Conversely, better option females use the information they gained the season before, and may retain their previous partner if they have no opportunity to mate with an individual of better quality. Results from simulations indicate that the best-of-n decision rule should be favoured when there is a large variation in male quality and low costs of mate sampling. On the other hand, the probability that the better option rule may invade the population is predicted to increase with male survival rate. However, changes in male mortality had no marked influence on the expected proportion of divorcing pairs, contrary to previous theoretical expectations.

The significance of hotspots to lekking topi antelopes (Damaliscus lunatus)

Controversy has surrounded the question of why lek-breeding has evolved in certain ungulate species. Can the behavior be explained simply by males mapping onto a female distribution that is determined by factors unrelated to mating? Or are leks created because estrous females distinguish between males and favor males who cluster? Here I address these questions by looking at spatial distribution in lekking topi antelopes (Damaliscus lunatus). Contrary to the predictions of a model assuming male clustering in the zone of maximum female range overlap, territories were highly clustered also within this zone, and lek size correlated positively with population density. In support of models derived from the ideal free distribution of males onto female dispersion, leks were in areas with high female density during the rut. However, models not taking into account both individual variation in male quality and female mate preferences failed to explain the extreme male clumping also within high density areas, which was revealed by a strongly male-biased sex-ratio on leks. Additional support for the female preference-based model came from the finding that estrous females concentrated onto leks. Female preference for clustered males may develop if males initially follow an ideal free distribution of unequal competitors with high quality males slightly clustered at density hotspots; positive feedback between female benefits of preference for clustered males and male benefits of clustering could lead to contraction of the territorial network and lek behavior. Thus only the female preference-based model correctly predicted a negative correlation between male mating rate and resource density.

Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus.

Although much attention has been recently directed to sexual selection arising after insemination from sexual promiscuity, little is known about the mechanisms determining reproductive success after insemination, and the way these mechanisms interact with each other and with selective mechanisms occurring before insemination: mate choice and mate acquisition. Here, we briefly review the findings of an on-going study investigating the mechanisms generating variation in reproductive success at both a pre- and a post-insemination stage in the domestic fowl. Female preference consistently favours socially dominant males before and after insemination. However, although social status mediates the number of sperm that a male inseminates into a female, dominant males may inseminate sperm of lower fertilising quality than their subordinates. We argue that mitochondrial genes may contribute to determine sperm quality, and speculate that the maternal control of mitochondrial genes may prevent sexual selection from operating on males, thus explaining both the lack of a positive correlation between social dominance and sperm quality and the maintenance of variation in male quality in the fowl.

The influence of potential reproductive rate and variation in mate quality on male and female choosiness in the sand goby, Pomatoschistus minutus

Recent models of choosiness in mate choice have identified two particularly important factors: the potential reproductive rate (PRR) of the choosing sex relative to that of the chosen sex, and the variation in quality of potential mates. This experimental study tested how these factors affected choosiness in male and female sand gobies, Pomatoschistus minutus. We manipulated relative PRR by means of water temperature, and mate quality by means of body length. The choosing male or female was offered a choice between two mates with either a small or a large difference in body length representing a small or a large variation in mate quality. Choosiness was measured as (1) preference for the larger mate, and (2) as whether or not spawning occurred with the smaller mate, while the larger mate was visible but screened off. We found that females preferred large males, and that their level of choosiness was affected by variation in male quality, but not by their own relative PRR. Males, on the other hand, seemed unselective in all treatments and were in general more likely than females to spawn with their provided partner. This suggests that in the sand goby, variation in male mate quality has a greater influence than relative PRR on facultative changes in female choosiness. However, a general difference in PRR between males and females may be one important factor explaining the observed sex difference in choosiness.

Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression

In some species, females choose mates possessing ornaments that predict offspring survival1,2,3,4,5. However, sexual selection by female preference for male genetic quality6,7,8 remains controversial because conventional genetic mechanisms maintain insufficient variation in male quality to account for costly preference and ornament evolution9,10. Here we show that females prefer ornaments that indicate genetic quality generated by transmission conflict between the sex chromosomes. By comparing sex-ratio distributions in stalk-eyed fly (Cyrtodiopsis) progeny we found that female-biased sex ratios occur in species exhibiting eye-stalk sexual dimorphism11,12 and female preferences for long eye span13,14. Female-biased sex ratios result from meiotic drive15, the preferential transmission of a ‘selfish’ X-chromosome. Artificial selection for 22 generations on male eye-stalk length in sexually dimorphic C. dalmanni produced longer eye-stalks and male-biased progeny sex ratios in replicate lines. Because male-biased progeny sex ratios occur when a drive-resistant Y chromosome pairs with a driving X chromosome15, long eye span is genetically linked to meiotic drive suppression. Male eye span therefore signals genetic quality by influencing the reproductive value of offspring16.

Variation in Male Mating Success on Leks

Studies of variation in male mating success within populations have been instrumental in shaping perspectives of the role of female choice in sexual selection. We present simple models to quantify the potential contributions to such variation from a variety of processes: average male mating success (equivalent to the number of female matings per male), variation in male and territory quality, male attendance times at leks, and degree of female synchrony, aggregation, and copying. If matings occur by chance, we expect variance in male mating success to increase proportionately with mean mating success. Increasing average mating success results in a superproportionate increase in variance when males or their territories differ in quality, when males differ in time spent at the lek, when females copy each other, or when females aggregate and mate as a group. In contrast, when females arrive in synchrony there is a subproportionate increase in variance with respect to mean male mating success. A review of 36 field studies from 20 species indicates that all studied leks exhibit greater variance in male mating success than expected by chance. Furthermore, the slope of a regression between variance and mean success is significantly greater than unity, as predicted by the models of variation in male quality, attendance at leks, female aggregation, and female copying. In studies of four leks in which we were able to partition the component of variance attributable to differences among males in attendance at leks, approximately 60% of the variance remained unexplained and was attributable to female copying, aggregation, or variation in male quality. The framework presented here allows a quantified breakdown of variation among males in mating success and facilitates comparisons among studies of the potential for sexual selection.

Forced extra-pair copulation and mate guarding in the white-cheeked pintail: timing and trade-offs in an asynchronously breeding duck

Abstract. Males employing a mixed reproductive strategy may increase their fitness through extra-pair copulations (EPCs), but also risk lost paternity when they leave their own mate unguarded. How males maximize the effectiveness of forced extra-pair copulation (FEPC) attempts while minimizing the risk of cuckoldry was studied in a non-migratory population of the white-cheeked pintail, Anas bahamensis bahamensis, a tropical species with extended breeding seasons. Despite substantial asynchrony in the laying dates of females, males directed FEPC attempts primarily at females in fertile condition. The rate of pair copulations also peaked during the female's fertile period, but 23.1% of all successful copulations with laying females were FEPCs. Males guarded their paternity by vigorously defending their mates from males attempting FEPC, by escorting females to their nests, by defending a territory, and by forcing copulation on their own mates after they had been subjected to an FEPC attempt by another male. Contrary to expectation, males did not temporally partition mate guarding and FEPC activity but pursued FEPCs primarily during the period when their own mates were fertile. There was no evidence, however, of a trade-off between FEPC activity and the quality of male mate guarding. Females paired to males with the highest FEPC rates were rarely subjected to FEPCs themselves. In addition, although females that abandoned nesting efforts suffered a high frequency of FEPC attempts, their mates were much less active in FEPCs than the mates of females that nested successfully. These results suggest substantial variation in male quality: some males excelled at both guarding their mates and achieving FEPCs, while others neither pursued FEPCs nor mate-guarded effectively.