The large-male advantage in brown antechinuses: female choice, male dominance, and delayed male death

Male-biased dimorphism in body size is usually attributed tosexual selection acting on males, through either male competitionor female choice. Brown antechinuses (Antechinus stuartii) aresexually dimorphic in size, and heavier males are known to siremore offspring in the wild. We investigated four possible mechanismsthat might explain this large-male reproductive advantage. Wetested if there is a female preference for large males, a femalepreference for dominant males, if larger males compete moreeffectively for mates, and if there is a survival advantagefor large males during the mating season. We established nestinggroups of males in captivity and conducted mate choice trialsin which males from nesting groups either could or could notinteract. We assessed male dominance rank and recorded survivaltimes after mating. Females did not prefer larger males directly.The results suggest that the other three mechanisms of sexualselection tested account for the large-male advantage: largemales competed more successfully for mates, so were sociallydominant; females rejected subordinates (males they saw losingtwice in contests to previous mates); and dominant males survivedfor longer after their first mating. Females judged male rankbased on direct observation of male competitive interactionsat the time of mating and apparently could not distinguish rankfrom male scent. Effects of size and dominance on male reproductivesuccess are not confounded by age because male antechinusesare semelparous.     

Comparative evidence supports a role for reproductive allocation in the evolution of female ornament diversity

1. Sexually selected ornaments are highly variable, even among closely related species, and the ultimate causes of variation in ornament evolution are unclear, including in rare cases of female ornament expression. One hypothesis is that differences across species in female reproductive allocation may help to explain patterns of female ornament expression among insects with nuptial gifts. 2. Dance flies (Diptera: Empididae: Empidinae) vary considerably among species in the presence and extravagance of female ornaments, which probably evolved through female contests for mates. In most dance flies, adult females appear to acquire all their dietary protein from nuptial gifts provided by males during mating. The importance of nuptial feeding on egg development is not yet known. 3. To test the prediction that the presence of female ornaments reflects differences in the degree to which females rely on nuptial feeding for egg development, egg development was examined in wild females of two species, one ornamented and the other unornamented. An ageing technique based on cuticular bands was validated, which permitted a regression of egg size on adult age. 4. We found that egg development depended on mating status in the ornamented species alone, meaning the eggs of unmated females of the ornamented species did not develop. This contrast across species is consistent with expectations that females of different species vary in their dependence on nuptial gifts for egg development. 5. These findings provide preliminary support for the hypothesis that differences in reproductive allocation mediate the intensity of female contests for nuptial gifts.     

Determinants of sperm transfer in the scorpionfly Panorpa cognate: male variation, female condition and copulation duration

Recent studies suggest that sperm production and transfer may have significant costs to males. Male sperm investment into a current copulation may therefore influence resources available for future matings, which selects for male strategic mating investment. In addition, females may also benefit from actively or passively altering the number of sperm transferred by males. In the scorpionfly Panorpa cognata, the number of sperm transferred during copulation depended on copulation duration and males in good condition (residual weight) copulated longer and also transferred more sperm. Moreover, sperm transferred and stored per unit time was higher in copulations with females in good condition than in copulations with females in poor condition. Males varied greatly and consistently in their sperm transfer rate, indicative of costs associated with this trait. The duration of the pairing prelude also varied between males and correlated negatively with the male's sperm transfer rate, but no other male character correlated significantly with male sperm transfer rate. The results are consistent with strategic mating effort but sperm transfer could also be facilitated by the physical size of females and/or females in good condition may be more cooperative during sperm transfer.     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.     

Precopulatory choice for cues of material benefits in tree crickets

The relative importance of direct and indirect benefits modelsof mate choice is a central question in sexual selection, butseparating the two models is very difficult because high qualitymales often provide both better direct benefits and better genes.In tree crickets, Oecanthus nigricornis, females have the opportunityto gain both directly and indirectly from mate choice. Femaletree crickets exercise premating choice for large males, butthe model underlying this choice is unknown. In this study weexamine the proximate cues used by female tree crickets to rejectmales, and show that the ability of males to provide food isa central cue. In contrast, we find no evidence that the relativesize of mates is important in mate rejection. The fact thatthe major phenotypic cues of male quality are related to foodprovisioning suggests that the role of genetic benefits in shapingfemale preferences is limited by the extent to which food provisioningsignals genetic quality.     

Mate preference for multiple cues: interplay between male and nest size in the sand goby, Pomatoschistus minutus

Female mating preferences are often based on more than one cue.In empirical studies, however, different mate choice cues aretypically treated separately ignoring their possible interactions.In the current work, we studied how male body size and sizeof the male's nest jointly affect mate preferences of femalesand gobies, Pomatoschistus minutus. The females were givena binary choice between males that differed either in body sizeor size of their nest or both. We found that neither body sizenor size of the nest alone affected male attractiveness, buttogether these 2 cues had a significant effect. Specifically,large males were more popular among females when they had alarge nest than when they occupied a small nest. The resultssuggest that if interaction effects between multiple mate choicecues are not considered, there is a danger of ignoring or underestimatingthe importance of these cues in sexual selection by female choice.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Reliable acoustic cues for female mate preference in a katydid (Scudderia curvicauda, Orthoptera: Tettigoniidae)

The call of male Scudderia curvicauda (Orthoptera: Tettigoniidae)consists of a series of phrases, and each phrase contains syllables.Females respond to the male signal with ticks that follow malephrases after a specific period of time. Pair formation takesplace after males locate the female using her response sounds.Repeated recordings of males revealed that the average numberof syllables produced per phrase was a table, within-male parameterand that this parameter was a reliable predictor of male size(pronotum length). Thus, phrase length could be a reliable cueby which females evaluate males. We presented virgin femaleswith a sequential choice of two tape-recorded male calls thatdiffered only in the mean number of syllables produced per phrase.Two different playback tapes were used, and each female wastested on each of 5 consecutive days with the same playbacktape. Females responded more often and with a greater numberof ticks to calls containing more syllables per phrase, andthis preference was maintained throughout the testing period.Male size was a poor predictor of the size of the spermatophorefood-gift produced by the male; therefore, females are probablynot selecting males for this attribute. For one of the playbacktapes, there was a significant increase in female responsivenessover several playback trials, suggesting that females may employa falling-threshold tactic with respect to mate preference.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

Direct detection of male quality can facilitate the evolution of female choosiness and indicators of good genes: Evolution across a continuum of indicator mechanisms

The evolution of mating displays as indicators of male quality has been the subject of extensive theoretical and empirical research for over four decades. Research has also addressed the evolution of female mate choice favoring such indicators. Yet, much debate still exists about whether displays can evolve through the indirect benefits of female mate choice. Here, we use a population genetic model to investigate how the extent to which females can directly detect male quality influences the evolution of female choosiness and male displays. We use a continuum framework that incorporates indicator mechanisms that are traditionally modeled separately. Counter to intuition, we find that intermediate levels of direct detection of male quality can facilitate, rather than impede, the evolution of female choosiness and male displays in broad regions of this continuum. We examine how this evolution is driven by selective forces on genetic quality and on the display, and find that direct detection of male quality results in stronger indirect selection favoring female choosiness. Our results imply that displays maybe more likely to evolve when female choosiness has already evolved to discriminate perceptible forms of male quality. They also highlight the importance of considering general female choosiness, as well as preference, in studies of “good genes.”     

Geographic variation in male ornamentation and female mate preference in the house finch: a comparative test of models of sexual selection

I compared the mate preferences of female house finches (Carpodacusmexicanus) from populations in which males differ in both plumagecoloration and the extent of ventral pigmentation (patch size).Phylogenetic analysis indicated that the small patch of ventralcoloration displayed by males in some populations is derivedfrom a larger-patched ancestral state. Regardless of the appearanceof males in their own populations, however, females from allpopulations showed a preference for the most brightly coloredmales and males with the largest patches. A reduction in patchsize independent of a change in female mate preference is notconsistent with sensory-bias or reproductive isolation modelsof sexual selection or with general predictions of runaway modelsof sexual selection. In contrast, a lack of congruence betweenfemale mate preference and male trait expression is predictedby the honest advertisement model, with house finches respondingto variation in regional and local access to carotenoid plumagepigments.     

Conflict between direct and indirect benefits of female choice in desert Drosophila

Identifying the factors that contribute to the adaptive significance of mating preferences is one major goal of evolutionary research and is largely unresolved. Both direct and indirect benefits can contribute to mate choice evolution. Failure to consider the interaction between individual consequences of mate choice may obscure the opposing effects of individual costs and benefits. We investigate direct and indirect fitness effects of female choice in a desert fly (Drosophila mojavensis), a species where mating confers resistance to desiccation stress. Females prefer males that provide a direct benefit: greater resistance to desiccation stress. Mating preferences also appear to have indirect consequences: daughters of preferred males have lower reproductive success than daughters of unpreferred males, although additional experimentation will be needed to determine if the indirect consequences of female preferences actually arise from 'sexually antagonistic' variation. Nevertheless, the results are intriguing and are consistent with the hypothesis that an interaction between direct and indirect benefits maintains sexually antagonistic variation in these desert flies: increased desiccation resistance conferred by mating might offset the cost of producing low-fecundity daughters.     

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male-male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (I males). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7-44%, n=6 years) of the total I males was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44-58% of the total I males was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

Nongenetic inheritance and the evolution of costly female preference

In species where males provide neither direct benefits nor paternal care, it is typically assumed that female preferences are maintained by indirect selection reflecting genetic benefits to offspring of preferred males. However, it remains unclear whether populations harbour sufficient genetic variation in fitness to support costly female preferences – a problem called the ‘lek paradox’. Here, we ask whether indirect selection on female preferences can be maintained by nongenetic inheritance. We construct a general model that can be used to represent either genetic or nongenetic inheritance, depending on the choice of parameter values. Interestingly, we find that costly preference is most likely to evolve and persist when fitness depends on an environmentally induced factor that can be transmitted over a single generation only, such as an environment‐dependent paternal effect. Costly preference can also be supported when fitness depends on a highly mutable factor that can persist over multiple generations, such as an epigenetic mark, but the necessary conditions are more restrictive. Our findings show that nongenetic inheritance provides a plausible hypothesis for the maintenance of costly female preferences in species where males provide no direct benefits to females. Nongenetic paternal inheritance of fitness can occur in species lacking conventional forms of paternal care. Indeed, transmission of paternal condition via sperm‐borne nongenetic factors may be more likely to evolve than conventional forms of paternal investment because sperm‐borne effects are protected from cuckoldry. Our results furnish a novel example of an interaction between genetic and nongenetic inheritance that can lead to otherwise unexpected evolutionary outcomes.     

Determinants of male ejaculate investment in the cotton bollworm Helicoverpa armigera: mating history,female body size and male age

Many studies demonstrate that ejaculate size may be influenced by male condition, female quality and the risk or intensity of sperm competition. In the present study, the effect of male and female conditions, male mating history and female mating status on ejaculate sperm numbers in the polyandrous moth Helicoverpa armigera is examined. A large variation in ejaculate size is found and, although female body size and male age influence ejaculate size, female age and copula duration do not. Both male and female mating histories have significant effects on ejaculate sperm numbers. Males reduce ejaculate expenditure in successive matings but deliver significantly more apyrene and eupyrene sperm to nonvirgin than to virgin females.     

Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle

Several hypotheses have been proposed to explain the evolutionof polyandry in species that provide nuptial gifts. When nuptialgifts are in the form of nutritional elements in the ejaculateand ejaculate size is correlated with male body size, femalescan accrue both direct (nutritional) and indirect (genetic)benefits from multiple mating. We examined remating decisionsin females of the seed beetle Stator limbatus and, using pathanalysis, examined the effects of male body size on the sizeof his ejaculate, the amount of ejaculate that was successfullytransferred to females, and the overall effect of these variableson female fecundity. Larger males produced larger ejaculatesand consequently transferred a larger ejaculate to females,but the effects on female fecundity differed between the females'first and second mates. Both larger first and second males wereable to transfer more of their ejaculate to females than weresmaller males. Both the total amount of ejaculate transferredby these males and polyandry (number of matings) were positivelycorrelated to female fecundity independently of each other.However, larger second males were more successful at stimulatingfemale fecundity independently of how much ejaculate they transferred.We also provide evidence that females are choosy during theirsecond mating opportunity. Both female choosiness and higherfemale investment after mating with larger second males suggestthat females may benefit from both direct and indirect effectsfrom multiple mating. We also conclude that male body size isunder both directional fecundity selection and directional sexualselection.     

Diel variation in a dynamic sexual display and its association with female mate-searching behaviour

Dynamic sexual signals often show a diel rhythm and may vary substantially with time of day. Diel and short-term fluctuations in such sexual signals pose a puzzle for condition capture models of mate choice, which assume a female preference for male traits that reliably reflect a male's quality. Here we experimentally manipulated the food supply of individual male field crickets Gryllus campestris in their natural habitat in two consecutive seasons to determine (i) the effect of male nutritional condition on the fine-scaled variation of diel investment in acoustic signalling and (ii) the temporal association between the diel variation in male signalling and female mate-searching behaviour. Overall food-supplemented males signalled more often, but the effect was only visible during the daytime. In the evening and the night, signal output was still high but the time spent signalling was unrelated to a male's nutritional condition. Females' mate-searching behaviour also showed a diel rhythm with peak activity during the afternoon, when differences among calling males were highest, and where signal output reliably reflects male quality. These findings suggest that males differing in nutritional condition may optimize their investment in signalling in relation to time of day as to maximize mating success.