Heritability of the algal-foraging ability: an indirect benefit of female mate preference for males' carotenoid-based coloration in the guppy, Poecilia reticulata

Several sexual selection theories assume certain benefits of female mate preference. The direct benefit, i.e., the direct contribution from males to their offspring and females, has been well tested empirically. However, the indirect benefit, i.e., the male's genetic contribution to their offspring, has been poorly demonstrated. Female preference for males' carotenoid-based coloration is known in some animals. Since animals must acquire carotenoids through foods, it is often hypothesized that the brightness of the carotenoid-based coloration is a reliable indicator of the male's foraging ability. Hence, females' indirect benefits, such as greater foraging ability in their offspring, through mate preference for the carotenoid-based coloration are assumed. However, the heritability of the foraging ability for foods that serve as carotenoid resources has not been tested. In this study, a maze experiment was performed in guppies (Poecilia reticulata) to examine the heritability of the foraging ability for algae, carotenoid resources in nature. The latency for completing algal-foraging tasks in this experiment showed high individual variation. Heritable estimates of the foraging ability were substantial (h ² = 0.57 – 0.66) and significant, suggesting a genetic contribution to the foraging ability from fathers to their offspring. This result may support the hypothesis that indirect benefits influence the evolution of female choice.     

The tactics of mutual mate choice and competitive search

A model of mutual mate choice is described, formulated as a dynamic game, which yields predictions about mating behaviour under the influence of time constraints, choice costs and competition for mates. These variables were examined because they may result in a change in the distribution of qualities among unmated individuals of both sexes over the course of the breeding season. The model predicts that mutual choice gives rise to assortative mating, although high costs of choice and/or inaccurate assessment both lead to lower overall correlations between the qualities (or the attractiveness) of mates. When all individuals are present from the start of the breeding season, the correlation between the qualities of individuals pairing at a given time declines throughout the season, so that mates are more closely matched among individuals who pair early than among those who pair late (and extra-pair copulation may thus be more common among the latter). Delayed arrival of lower-quality individuals may, however, lead to an increase in this correlation with time during the early part of the season. The mean quality of unmated males and females declines over time, because more attractive individuals tend to mate sooner. As a result of this decline, and because of time constraints, superior individuals become less choosy as the season progresses. If choice is costly, however, then inferior individuals become more selective with time during the early part of the season, and the level of choosiness peaks later for such individuals. Received: 28 March 1996 / Accepted after revision: 21 September 1996     

Female mate choice determines reproductive isolation between sympatric butterflies

Animal courtship rituals are important for species recognition, and a variety of cues might be utilized to recognize conspecific mates. In this paper, we investigate different species-recognition mechanisms between two sympatric butterfly sister species: the wood white (Leptidea sinapis) and Real’s wood white (Leptidea reali). We show that males of both species frequently court heterospecific females both under laboratory and field conditions. The long-lasting elaborate courtships impose energetic costs, since the second courtship of males that were introduced to two subsequent conspecific females lasted on average only one fourth as long as the first courtship. In this paper, we demonstrate that premating reproductive isolation is dependent on female unwillingness to accept heterospecific mates. We studied female and male courtship behavior, chemical signaling, and the morphology of the sexually dimorphic antennae, one of the few male traits visible for females during courtship. We found no differences in ultraviolet (UV) reflectance and only small differences in longer wavelengths and brightness, significant between-species differences, but strongly overlapping distributions of male L. sinapis and L. reali antennal morphology and chemical signals and minor differences in courtship behavior. The lack of clear-cut between-species differences further explains the lack of male species recognition, and the overall similarity might have caused the long-lasting elaborate courtships, if females need prolonged male courtships to distinguish between con- and heterospecific suitors.     

Sexual selection and the evolutionary effects of copying mate choice

We examine the evolutionary consequences of copying mate choice using models in which the preferences of younger females are affected by the mate choices that they observe older females making. We introduce two models of copying, termed single mate copying and mass copying, corresponding to situations in which immature females imprint on the choices of only one or of a very large number of older females, respectively. Female mating preferences are assumed to evolve only through cultural evolution, while the male trait on which they act is inherited either via a haploid autosomal or a Y-linked locus. Results show that the preference and male trait can rapidly coevolve, with a positive frequencey-dependent advantage to the more common male trait allele. This process can cause a display trait that lowers male viability to increase in a population. Mass copying results in stronger frequency dependence than does single mate copying. Mass copying and, under some conditions, single mate copying lead to two alterative stable equilibria for the male trait. Neither copying model supports variation at the male trait locus, and copying makes it more difficult for a novel male trait phenotype to spread. Correspondence to: M. Kirkpatrick     

Measuring mate choice using correlation: the effect of female sampling behaviour

For intersexual selection to occur, it is necessary that females choose between males. It is now well appreciated that constraints exist, which preclude females sampling all the available males in a population. These constraints are likely to have caused the evolution of sampling rules (such as the “best-of-n” rule) by which females sample males. Here we investigate the impact of female subsampling of the male population, not on the evolution of sampling behaviour, but on the population-level correlation between a male trait and currencies such as reproductive success. This study is important as it illustrates when population-level correlations can be safely used to infer the presence and strength of sexual selection in the field. We find that the correlation between a male trait and a mate choice variable rises steeply as the number of males sampled by each female increases, flattening above seven to ten males sampled. This shape is found to be remarkably robust, and little affected by, for example, the mate choice variable used, by noise in assessment, by sampling behaviour depending on female quality, or by population size. The only variable found to have a large impact is male clumping according to their “quality”. If females are sampling about four males, the maximum correlation that can be found at the population level is in the range 0.4–0.6, perhaps as little as 0.1 if males are strongly clumped. A recent review of the literature suggests that four is the average number of males that females sample. Thus, the absence of a strong correlation cannot by itself be used to infer that sexual selection is weak, as it may be due to females sampling few males. Received: 18 May 1998 / Accepted after revision: 18 July 1998     

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     

Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance

Although contemporary animal contest theory emphasises the importance of physical asymmetries in resolving disputes, such asymmetries do not obviously settle fights in all groups. Territorial male butterflies, for example, compete via elaborate non-contact aerial interactions in which success is determined by relative persistence. Prior research suggests that the resolution of these contests is not clearly related to physical variables such as body size or energy reserves. However, given that the contests involve elaborate aerial manoeuvres, one long-standing suggestion is that asymmetries in flight performance, and thus flight morphology, may be important. We addressed this hypothesis via a manipulative investigation into the biophysical correlates of contest success in the speckled wood butterfly, Pararge aegeria. This species possesses the ability for significant adaptive phenotypic plasticity in relevant flight morphological parameters. We took advantage of this plasticity to rear 90 individuals of markedly varying flight morphologies, which we then pitted against each other in a semi-controlled experimental fashion. Multiple logistic and lognormal analyses provided little evidence for the relevance of morphological parameters, including relative flight musculature, wing loading and wing aspect ratio (wing length relative to area), to the outcome and/or duration of experimental contests. Instead, we found a positive effect of age upon contest success. Given that ability for high acceleration is strongly linked to variation in these morphological parameters, our findings suggest that flight performance is not a strong determinant of resource-holding potential in this notably territorial butterfly.     

Early nutritional conditions, growth trajectories and mate choice: does compensatory growth lead to a reduction in adult sexual attractiveness?

It is well documented that poor early nutrition can have profound negative effects on adult life-history traits. However, it has also been demonstrated that organisms can undergo compensatory resource allocation strategies (such as an accelerated growth rate) if food availability improves, so as to mitigate the effects of the poor early conditions. Previous research has indicated that elevated growth rates can incur costs in the longer term, such as an increased rate of senescence and shorter lifespan. We tested whether a phase of compensatory growth after a period of reduced food availability earlier in life affected the sexual attractiveness of adult male green swordtails Xiphophorus helleri, a species in which it has previously been documented that females prefer larger-bodied and longer-tailed males. The experiment compared the attractiveness of size-matched brothers that had experienced contrasting growth trajectories as juveniles; the experiments were initially conducted in the middle of a male’s sexually reproductive life and were then repeated towards the very end of life. At both ages, males that had undergone compensatory growth were equally as attractive as their brothers that had grown normally. These results suggest that the growth compensation benefits males through an increase in their attractiveness over that which they would have had if they had remained on their original growth trajectory. The lack of change in relative attractiveness with age indicates that the compensation does not cause greater deterioration in secondary sexual characters at older ages than in continuously well-fed males.     

Enhancement of reproductive success through mate choice in a social rock-wallaby, Petrogale assimilis (Macropodidae) as revealed by microsatellite markers

The reason why a female who is socially paired to one particular male seeks extra-pair copulations (EPCs) with others has important implications in life history models and to the study of behaviour. The Allied rock-wallaby, Petrogale assimilis, lives in spatially isolated colonies in tropical north Queensland, Australia. Extensive observations of a colony at Black Rock showed that intense behavioural bonding occurs between pairs of adult males and females; about two-thirds of males paired with one female, the remainder paired with two females simultaneously. Single-locus microsatellite profiling determined the paternity of 63 offspring from 21 females for which long-term behavioural data were available. One-third of the young were fathered by males which were not paired socially with the mother. The mating system was heterogeneous: (1) all offspring of 11 females were fathered by the mother's partner, (2) all young of 5 females were fathered by extra-pair males, and (3) only some of the young of 5 females were fathered by their regular consort. Analysis of individual longitudinal demographic records showed that females whose young were always fathered by their consort had higher reproductive success than those whose young were always fathered as a result of (EPCs). However, females with some offspring fathered by their regular consort and others via EPCs had the highest probability of raising young to independence. These females were significantly more likely to have an offspring fathered as a result of an EPC if their previous young had failed to survive to pouch emergence. These results are consistent with the hypothesis that females choose mates for their genetic quality. Comparison of the males with which these females sought EPCs and the regular consorts suggested that arm length rather than body weight or testes size was used as the index of genetic quality. Results from a second colony of rock-wallabies in which the reproductive rate was accelerated were also consistent with the genetic-quality hypothesis. These results imply that by choosing better-quality fathers irrespective of social pairing, females are able to maximise their overall lifetime reproductive success, and presumably, those of their offspring. Received: 8 June 1997 / Accepted after revision: 28 February 1998     

No evidence for female mate choice based on genetic similarity in the túngara frog Physalaemus pustulosus

In most sexually reproducing animals, the behavior of one or both sexes during courtship critically influences the success at mating of the opposite sex. This behavior is often interpreted as “mate choice,” and there is great interest in why such choices are exercised. The explanation for the evolution of mate choice that has received the most attention and generated the most controversy is based on assumed genetic effects. In this study, we investigated whether female túngara frogs, which choose mates based on acoustic cues, have a preference for genetically less related males. Specifically, we determine if there is disassortive mating based on microsatellite markers, if there is information in the advertisement call that could be used to assess genetic similarity, and if females exhibit acoustic-based mating preferences that would promote choice for genetic diversity. Using seven microsatellite markers, we found no correlation of male call similarity and male genetic relatedness. Female choice experiments showed no female preference for calls of less related males, and there was no evidence for inbreeding avoidance in the field. Our results do not support the hypothesis of mate choice based on information about genetic relatedness conveyed by acoustic signals in túngara frogs.     

The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex)

We studied the effect of male coloration on interspecific female mate choice in two closely related species of haplochromine cichlids from Lake Victoria. The species differ primarily in male coloration. Males of one species are red, those of the other are blue. We recorded the behavioral responses of females to males of both species in paired male trials under white light and under monochromatic light, under which the interspecific differences in coloration were masked. Females of both species exhibited species-assortative mate choice when colour differences were visible, but chose non-assortatively when colour differences were masked by light conditions. Neither male behaviour nor overall female response frequencies differed between light treatments. That female preferences could be altered by manipulating the perceived colour pattern implies that the colour itself is used in interspecific mate choice, rather than other characters. Hence, male coloration in haplochromine cichlids does underlie sexual selection by direct mate choice, involving the capacity for individual assessment of potential mates by the female. Females of both species responded more frequently to blue males under monochromatic light. Blue males were larger and displayed more than red males. This implies a hierarchy of choice criteria. Females may use male display rates, size, or both when colour is unavailable. Where available, colour has gained dominance over other criteria. This may explain rapid speciation by sexual selection on male coloration, as proposed in a recent mathematical model. Received: 11 April 1997 / Accepted after revision: 27 July 1997     

Fitness benefits of multiple mating versus female mate choice in the cellar spider (Pholcus phalangioides)

Recent studies have demonstrated that mating with multiple males can be beneficial for females and her offspring even if males contribute nothing but sperm. This was mainly established for species in which sperm from several males mix in the reproductive tract of the female, thus allowing sperm competition and/or female sperm choice. However, in species with last male sperm precedence, female re-mating decides against the previous male by strongly limiting his reproductive success. We tested the effect of female re-mating behaviour using the cellar spider Pholcus phalangioides, which shows strong last males sperm precedence and moderate levels of polyandry under natural situations. We predicted that females prevented from remating even though they are receptive would show reduced reproductive success compared to females that accept two copulations and females that reject a second male, since the latter two treatments were allowed to behave according to their decisions. However, if the number of matings per se had an effect on oviposition or on offspring performance, double-mated females should perform better compared to both treatments of once-mated females. We measured female fecundity and fertility over a period of 140 days, comparable to the species' natural reproductive peak season. Two thousand one hundred and fifty-two offspring from 67 first egg sacs were reared under two feeding levels. We registered development time and survival, and measured offspring adult size and mass. We found a positive effect of double mating, as in this treatment, oviposition probability was higher compared to the other treatments. Interestingly, adult female offspring of the DM treatment that were raised under low food level had a higher condition index compared to those from FS and RM, but development time, size and mass at adulthood were not affected by mating treatment. Female choice only seemed to affect hatching latency of the offspring. Overall, the main predictor of female reproductive output and success was female body size.     

Protein content of spermatophores in relation to monandry/polyandry in butterflies

The evolution of a mating system, and specifically mating frequency, is dependent on the costs and benefits to both sexes of mating once or several times. In butterflies, males transfer a spermatophore that contains both sperm and accessory gland products. Accessory gland substances contain nutrients which, in some species, females use to increase their reproductive output and longevity. Nutrients contained in these packaged ejaculates represent investment by males in reproduction. Consequently, the nutritional composition of spermatophores may vary depending on the mating system. There are two lines of arguments concerning the evolution of the nutrient content of ejaculates. One hypothesis argues that male nuptial gifts evolved in the context of certainty of paternity and ease of finding mates; thus spermatophores of polyandrous males (with lower certainty of paternity and greater ease of finding mates) should contain less protein than those of monandrous males, since more spermatophores are produced on average. The other hypothesis argues that polyandry evolved in the context of maximization of male transfer of nutrients to females, and hence spermatophores of polyandrous males should contain more protein than those of monandrous males. In an attempt to distinguish between these two hypotheses, we determined how protein content of ejaculates varied with the degree of polyandry in nine species of pierid and two species of satyrid butterflies. We found that both relative ejaculate mass and protein content increased with the degree of polyandry. Hence our results are consistent with the view that polyandry has evolved in the context of male transfer of nutrients to females, and provides another example of a male adaptation to multiple mating in butterflies.     

Trade-off between fitness components in males of the polygynous butterfly Callophrys xami (Lycaenidae): the effect of multiple mating on longevity

The differential costs of mating paid by males and females influence the nature and strength of sexual selection. In butterflies, males invest a relatively large amount of time and resources in each mating, but male survival costs of mating have not been demonstrated. I present the results of experiments designed to measure the effect of different aspects of mating on male longevity in the polygynous butterfly Callophrys xami. In experiment 1, I compared the longevity of pairs of males that produced similar amounts of spermatophore, but that mated at different rates, a different numbers of times, and that produced spermatophores at different rates, and found that the longevity of ”low-mating-rate” males was not different from that of ”high-mating-rate” males. In experiment 2, the longevity of virgin males was not significantly different from that of multiply mated males. In experiment 3, I used resource-limited males resulting from experimental food limitation of last-instar larvae; resource-limited virgin males lived significantly more days than resource-limited multiply mated males. Since ecological costs of mating (e.g., disease transmission, predation risk) were excluded in the experiment, diminished male longevity was a product of physiological costs of sexual interactions. These results suggest that the cost of ejaculate production is an important cause of longevity reduction when there are resource limitations; however, the role of other possible physiological costs of mating in longevity reduction is still unknown. Received: 21 March 2000 / Accepted: 26 August 2000     

Sequential male mate choice in a fish,the Pacific blue-eye<Emphasis Type="Italic"> Pseudomugil signifer</Emphasis>

Mate choice is not just a female preoccupation. Under some circumstances, males may also be choosy. However, studies of male mate choice have generally been confined to situations where males can make direct comparisons between potential partners. In contrast, sequential male mate choice has largely been overlooked despite its biologically importance, especially if current investment in mate attraction diminishes a males future mating opportunities. Using the Pacific blue-eye fish Pseudomugil signifer, we show that males are capable of exercising sequential mate choice. When presented sequentially with large and small females, males spent more effort courting the former. However, males did not appear to modify the time spent courting a given female based on the size of the female encountered previously. We suggest that greater attention to the sequential choice problem in males may help illuminate similarities and differences between the sexes when it comes to mating decisions.Communicated by T. Czeschlik     

Indirect genetic benefits of polyandry in a spider with direct costs of mating

The search for the evolutionary explanation of polyandry is increasingly focused on direct and indirect selection on female resistance. In a polyandrous spider Stegodyphus lineatus, males do not provide material benefits and females are resistant to remating. Nevertheless, polyandrous females may obtain indirect genetic benefits that offset the costs associated with multiple mating. We manipulated the opportunity for females to select between different partners and examined the effect of female mating history (mated once, mated twice, or rejected the second male) on offspring body mass, size, condition, and survival under high- and low-food rearing regimens. We found that multiple mating, not female choice, results in increased female offspring body mass and condition. However, these effects were present only in low-food regimen. We did not find any effects of female mating history on male offspring variables. Thus, the benefits of polyandry depend not only on sex, but also on offspring environment. Furthermore, the observed patterns suggest that indirect genetic benefits cannot explain the evolution of female resistance in this system.     

Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice

Empirical and theoretical studies have only recently begun to examine how females use complex multi-component displays when selecting mates. Superb fairy-wrens are well suited to the study of female choice because females have control over extra-group paternity and cuckold their mates at high rates, while males possess a variety of sexually selected traits. Available evidence suggests that females base their extra-group mate choice on the timing of male moult into breeding plumage or the onset of display. However, males continue to perform elaborate displays throughout the season, and direct most displays to females during their fertile period. We therefore conducted focal observations on fertile females to quantify the frequency of male display and used microsatellite genotyping to compare the role of display rate during the breeding season and the timing of male moult on female mate choice. We show that the addition of data on male display rate does not improve our ability to predict which males obtain extra-group paternity. The timing of male moult into breeding plumage remains the only predictor of male extra-group reproductive success. Nevertheless, we found that males displayed more to females that were unable to select extra-group mates on the basis of the timing of moult or the onset of display. This raises the possibility that there are circumstances when females use display rate to discriminate between potential extra-group sires. Overall this study supports the theoretical prediction that females are more likely to base their mate choice on reliable indicators of male quality such as fixed morphological traits and displays of endurance, in this case an early moult into breeding plumage and the performance of an elaborate display during the winter, than a flexible behavioural trait such as display rate during the breeding season. Received: 26 January 2000 / Revised: 1 August 2000 / Accepted: 26 August 2000     

An estimate of female mate searching costs in the lekking butterfly Coenonympha pamphilus

We estimated the cost to females of the lekking butterfly Coenonympha pamphilus of visiting males on leks instead of taking off and soliciting courtship from males passing them outside leks, as occurs in the non-lekking congener C. tullia. We followed released virgin females of C. pamphilus in the field until they mated. We estimated the time they lost by remaining perched and not approaching males that passed them, and observed how often and at what distance virgin females were passed by males in the field. We then calculated how much faster these females would have been detected if they had taken off and approached these males, using probabilities of detection as a function of passing distance derived from field observations on C. tullia females. C. pamphilus females on average lost 201 min by not approaching males on their way to leks. To estimate what this time loss meant in terms of fitness, we measured how the age at mating affected fecundity. Using field measures of fecundity and mortality, the time loss translated into an average 2.8% reduction in fecundity as a best estimate, and an average 1.3% reduction in fecundity as a lower estimate. This fitness cost is larger than has been reported earlier for a lekking bird, but is probably too small to eliminate the possibility of indirect benefits of mating with males on leks. Received: 15 August 1996 / Accepted after revision: 24 January 1997     

Imperfect female choice and male mating skew on leks of different sizes

We present a model of error-prone female choice on leks, and investigate the effects of different degrees of error on the distribution of mating success among males present at leks of different sizes. At higher levels of error, the best male is predicted to gain a smaller share of matings, while low-ranking males gain a larger share. Males who are of high rank but not the most desirable on the lek do best at intermediate levels of error, since the top-ranked male does not then claim all the matings, but assessment is still sufficiently accurate for females to discriminate between high-ranking and low-ranking competitors. The effects of error are shown to be more pronounced on larger leks, due to smaller expected differences in mating value between males of adjacent ranks. This interaction between lek size and error suggests that observed negative relationships between lek size and mating skew need not be attributed solely to intrasexual competition, as previously suggested, but could also be a result of imperfect choice. Received: 20 February 1998 / Accepted after revision: 25 October 1998