Attractive males do not sire superior daughters

Much of the recent work on the evolution of female choice has focused on the relative influence of direct and indirect benefits, and particularly whether direct costs can be offset by indirect benefits. Studies investigating whether attractive males benefit females by increasing the viability of their offspring often report mating advantages to sons consistent with the Fisher process, while detecting no or weak viability benefits. One potential reason for this is that sons may trade-off viability benefits with investment in costly traits that enhance mating success, leading to the suggestion that viability benefits may be better detected by examining daughters’ fitness. Here we investigate the relationship between male attractiveness and daughters’ fitness in Drosophila simulans. We measured daughter (and dam) lifetime reproductive success and longevity. We found no evidence that attractive males sire high fitness daughters. Additionally, neither daughters nor dams gained direct benefits from mating with attractive males. However, aspects of daughters’ fitness were related to dam characters.     

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters

Female mate choice and male–male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male–male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male–male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male–male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.     

Fisherian flies: benefits of female choice in a lekking sandfly

We experimentally investigated the fitness consequences of female mate choice in order to test the relative importance of three competing but non-exclusive hypotheses for the maintenance of pronounced female mating preferences on leks: that females benefit directly; that they gain indirect Fisherian benefits by producing more attractive sons; or that they benefit indirectly because preferred males possess ''good genes'' that confer increased viability on their sons and daughters. We allowed lekking female sandflies, Lutzomyia longipalpis, to choose between males of varying attractiveness to females, and monitored the consequences for their own survival and reproductive success as well as for their offspring. In contrast to the predictions of the direct-benefits model, we found no clear sire effect on the fecundity or survival of the females themselves; females mating with more attractive males did survive longer after oviposition, but never long enough to undertake a second batch of egg laying. We also found no evidence that females gained good-genes benefits in terms of enhanced offspring survival. However, we did find that generally attractive males fathered sons who were then chosen when they in turn formed leks. Although not completely precluding other benefits, our results indicate that Fisherian benefits are at least partly responsible for maintaining female choice at L. longipalpis leks. These findings indicate the importance of testing all putative benefits concurrently in exploring the maintenance of female mate choice.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.     

Male‐induced costs of mating for females compensated by offspring viability benefits in an insect

Sexual conflict facilitates the evolution of traits that increase the reproductive success of males at the expense of components of female fitness. Theory suggests that indirect benefits are unlikely to offset the direct costs to females from antagonistic male adaptations, but empirical studies examining the net fitness pay‐offs of the interaction between the sexes are scarce. Here, we investigate whether matings with males that invest intrinsically more into accessory gland tissue undermine female lifetime reproductive success (LRS) in the cricket Teleogryllus oceanicus. We found that females incur a longevity cost of mating that is proportional to the partner’s absolute investment into the production of accessory gland products. However, male accessory gland weight positively influences embryo survival, and harmful ejaculate‐induced effects are cancelled out when these are put in the context of female LRS. The direct costs of mating with males that sire offspring with higher viability are thus compensated by direct and possibly indirect genetic benefits in this species.     

Direct and indirect fitness consequences of female choice in a crustacean

Understanding the evolution and maintenance of female mate choice requires information on both the benefits (the sum of direct and indirect benefits) and costs of selective mating. In this study, I assessed the fitness consequences of female mate choice in a freshwater crustacean. In Hyalella amphipods, males attempt to form precopulatory pairs with females. Large males, bearing large posterior gnathopods, tend to be over-represented in precopulatory pairs. I show that females receive both direct (reduced risk of predation while paired) and indirect (sexy sons) benefits from mating with these males. Furthermore, the behavioral mechanisms used to filter male phenotypes carry no detectable energetic cost for females. Thus, females that choose males with successful phenotypes are expected to have higher Darwinian fitness than females that mate at random. This study shows that direct and indirect selection act together to favor large male size, which explains the sexual size dimorphism and size-based mating biases observed in this species.     

Direct benefits and costs for hybridizing Ficedula flycatchers

It is well understood that females may gain direct benefits from breeding with attractive males. However, the direct fitness effects of mate-choice are rarely considered with respect to mating between different species (hybridization), a field dominated by discussion of indirect costs of producing unfit hybrid offspring. Hybridizing females may also gain by the types of direct benefits that are important for intraspecific mate choice, and in addition may have access to certain benefits that are restricted to mating with males of an ecologically diverged sister-taxon. We investigate possible direct benefits and costs female Ficedula flycatchers gain from breeding with a heterospecific male, and demonstrate that hybridizing female collared flycatchers (F. albicollis) breed in territories that do not suffer the seasonal decline in habitat quality experienced by females breeding with conspecifics. We exclude the hypotheses that heterospecific males provide alternative food-types or assume a greater amount of the parental workload. In fact, the diets of the two species (F. albicollis and F. hypoleuca) were highly similar, suggesting possible interspecific competition over food resources in sympatry. We discuss the implications of direct fitness effects of hybridization, and why there has been such a disparity in the attention paid to such benefits and costs with regard to intraspecific and interspecific mate-choice.     

The sexual selection continuum

The evolution of mate choice for genetic benefits has become the tale of two hypotheses: Fisher's 'run-away' and 'good genes', or viability indicators. These hypotheses are often pitted against each other as alternatives, with evidence that attractive males sire more viable offspring interpreted as support for good genes and with a negative or null relationship between mating success of sons and other components of fitness interpreted as favouring the Fisher process. Here, we build a general model of female choice for indirect benefits that captures the essence of both the 'Fisherian' and 'good-genes' models. All versions of our model point to a single process that favours female preference for males siring offspring of high reproductive value. Enhanced mating success and survival are therefore equally valid genetic benefits of mate choice, but their relative importance varies depending on female choice costs. The relationship between male attractiveness and survival may be positive or negative, depending on life-history trade-offs and mating skew. This relationship can change sign in response to increased costliness of choice or environmental change. Any form of female preference is subject to self-reinforcing evolution, and any relationship (or lack thereof) between male display and offspring survival is inevitably an indicator of offspring reproductive values. Costly female choice can be maintained with or without higher offspring survival.     

Indirect benefits for choosy female grasshoppers (Chorthippus biguttulus)?

Since direct benefits are likely to be absent in the grasshopper Chorthippus biguttulus, indirect genetic benefits are a potential explanation for costly female preference. Choosy females may improve their fitness in terms of enhanced attractiveness of sons alone or additionally by improved viability of offspring. We tested the predictions of these two hypotheses by comparing attractiveness-related song traits and viability in offspring of attractive and unattractive grasshopper males. The experiment was conducted with larvae reared under semi natural lab conditions in one year and under natural conditions in the field in the following year. If reared under natural conditions no significant differences in viability and song traits between offspring of attractive and unattractive males could be found. Offspring reared in the lab produced calling songs with a significantly more exact song rhythm when sired by attractive males than offspring of unattractive males. Offspring of attractive males should thus have a theoretical advantage in mate choice, which, however, did not translate into higher attractiveness values in acoustic female choice experiments. Therefore our experiments could not resolve whether female choice in C. biguttulus evolved according to the sexy son hypothesis. Since viability in offspring of attractive males did not differ from offspring of unattractive males, “good genes” seems unlikely to be the underlying mechanism of female choice.     

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by-product of sexual conflict over the mating rate.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.     

Male Courtship Behavior and Weapon Trait as Indicators of Indirect Benefit in the Bean Bug,Riptortus pedestris

Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male–male competition also drives evolution of male traits that represent competitive ability. Because female choice and male–male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male–male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.     

Females lay fewer eggs for males with greater courtship success in a lekking Drosophila

The evolutionary basis for female mate choice in lek mating systems has been a common subject of research in animal behaviour. Because males apparently provide only gametes to females in lekking species, most research has focused on possible indirect (genetic) benefits that females might gain by discriminating among males. Despite the emphasis on indirect benefits, it has been recognized that females in non-resource-based systems such as leks could potentially gain direct benefits via mate choice if males varied in fertilization abilities, for example. Previous evidence has shown that females of a lekking Hawaiian Drosophila, D. grimshawi, vary in fecundity when mated to certain males, and that females possess preferences for vigorously courting males. This study tests the hypothesis that D. grimshawi females gain direct benefits by preferentially mating with more sexually vigorous males. Male courtship vigour (performance of wing and head-under-wing displays) and the consequences of female choice on offspring production were evaluated separately using different females. Unexpectedly, matings involving more vigorously courting males resulted in fewer offspring being produced. Reduced offspring number resulted because females laid fewer eggs when mating with males having greater courtship success. These results are discussed in light of sexual conflict and possible multiple mating by females. Females also demonstrated considerable variation in mating behaviour and behavioural variation was correlated with mating benefits. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

What is driving male mate preference evolution in Jamaican field crickets?

Male mating preferences are often a neglected aspect of studies on sexual selection. Male mating preferences may evolve if they provide males with direct‐fitness benefits such as increased opportunity to fertilize more eggs or indirect‐fitness benefits such as enhanced offspring survival. We tested these ideas using Jamaican field crickets, Gryllus assimilis, previously shown to exhibit male mating preferences. We randomly mated males to either their preferred or non‐preferred potential mates and then asked whether mating treatment influenced egg oviposition or offspring viability. Preferred females were not significantly more fecund and did not produce more viable eggs or offspring than non‐preferred females. Male mate preferences were therefore inconsistent with both the direct‐ and indirect‐fitness benefits hypotheses under the conditions of our experiment. Our null results leave us with an open question about what is driving the evolution of mating preferences in male crickets. Future research should explore the whether the offspring of preferred females are more attractive, have stronger immune systems, and/or experience higher adult longevity.     

The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides

Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.     

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.     

Males from populations with higher competitive mating success produce sons with lower fitness

Female mate choice can result in direct benefits to the female or indirect benefits through her offspring. Females can increase their fitness by mating with males whose genes encode increased survivorship and reproductive output. Alternatively, male investment in enhanced mating success may come at the cost of reduced investment in offspring fitness. Here, we measure male mating success in a mating arena that allows for male–male, male–female and female–female interactions in Drosophila melanogaster. We then use isofemale line population measurements to correlate male mating success with sperm competitive ability, the number of offspring produced and the indirect benefits of the number of offspring produced by daughters and sons. We find that males from populations that gain more copulations do not increase female fitness through increased offspring production, nor do these males fare better in sperm competition. Instead, we find that these populations have a reduced reproductive output of sons, indicating a potential reproductive trade‐off between male mating success and offspring quality.     

Costly sexual harassment in a beetle

Abstract The optimal number of mating partners for females rarely coincides with that for males, leading to sexual conflict over mating frequency. In the bruchid beetle Callosobruchus maculatus, the fitness consequences to females of engaging in multiple copulations are complex, with studies demonstrating both costs and benefits to multiple mating. However, females kept continuously with males have a lower lifetime egg production compared with females mated only once and then isolated from males. This reduction in fitness may be a result of damage caused by male genitalia, which bear spines that puncture the female’s reproductive tract, and/or toxic elements in the ejaculate. However, male harassment rather than costs of matings themselves could also explain the results. In the present study, the fitness costs of male harassment for female C. maculatus are estimated. The natural refractory period of females immediately after their first mating is used to separate the cost of harassment from the cost of mating. Male harassment results in females laying fewer eggs and this results in a tendency to produce fewer offspring. The results are discussed in the context of mate choice and sexual selection.     

Costs and benefits of polyandry in a sexually cannibalistic mantis

Mating with more than one male often provides direct or indirect benefits to female fitness but can also increase the chance of injury and death. Costs of mating are expected to increase linearly with increasing mating number. But how such costs interact with benefits to determine the net payoff of mating multiply is not well understood. Using the highly cannibalistic Springbok mantis, Miomantis caffra, a species where females are stabbed in the abdomen by males during violent premating struggles that males initiate to avoid being cannibalized, we took an experimental approach to assess the economics of polyandry under the risk of external, male-inflicted injury. We predicted that females that mate multiply would be more likely to show abdominal injuries, have higher prereproductive mortality, produce fewer offspring and be more likely to engage in pre-mating cannibalism to avoid unwanted matings. In line with our predictions, we found that the likelihood of abdominal injury was highest among females that mated at least once, and prereproductive death was highest among females that mated twice or three times. Virgin females completely avoided these costs and produced some offspring parthenogenetically but not enough to provide a net benefit. Although mating was better than not mating, there was no singularly optimal mating number: females that mated once and three times produced similarly high numbers of offspring from the first ootheca, which resulted in an intermediate trough in offspring production at two matings. We also found little evidence that cannibalism was deployed as a mate-avoidance strategy: females consistently attacked and consumed males regardless of how many times they mated or how long they were housed with males. Our results suggest the possibility of two distinct mating strategies in M. caffra, where females either mate at a lower frequency to minimize costs or at a higher frequency to maximize benefits. We discuss possible explanations for this bimodal pattern in offspring production.