Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets

Abstract.— Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free-living female decorated crickets, Gryllodes sigillatus , and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high-food-stress or low-food-stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mother's polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.     

Polyandry in dragon lizards: inbred paternal genotypes sire fewer offspring

Multiple mating in female animals is something of a paradox because it can either be risky (e.g., higher probability of disease transmission, social costs) or provide substantial fitness benefits (e.g., genetic bet hedging whereby the likelihood of reproductive failure is lowered). The genetic relatedness of parental units, particularly in lizards, has rarely been studied in the wild. Here, we examined levels of multiple paternity in Australia's largest agamid lizard, the eastern water dragon (Intellagama lesueurii), and determined whether male reproductive success is best explained by its heterozygosity coefficient or the extent to which it is related to the mother. Female polyandry was the norm: 2/22 clutches (9.2%) were sired by three or more fathers, 17/22 (77.2%) were sired by two fathers, and only 3/22 (13.6%) clutches were sired by one father. Moreover, we reconstructed the paternal genotypes for 18 known mother–offspring clutches and found no evidence that females were favoring less related males or that less related males had higher fitness. However, males with greater heterozygosity sired more offspring. While the postcopulatory mechanisms underlying this pattern are not understood, female water dragons likely represent another example of reproduction through cryptic means (sperm selection/sperm competition) in a lizard, and through which they may ameliorate the effects of male‐driven precopulatory sexual selection.     

Cryptic female choice predicated on wing dimorphism in decorated crickets

Male decorated crickets, Gryttodes sigllatus, normally lackbind wings and are incapable of flight (short-winged males),but occasionally exhibit fully developed hind wings that makerudimentary flight possible (long-winged males). Long-wingedmales bear a cost of flight in the form of decreased inseminationsuccess, which arises as a consequence of two interrelated factors:(1) long-winged males exhibit a lower reproductive investmentrelative to short-winged males, as measured by the mass of amale's spermatophore and reproductive organs and (2) the postcopulatorybehavior of females favors males that maximize their reproductiveinvestment. Of particular importance to male mating successis the spermatophylax, a large gelatinous mass forming partof the spermatophore and consumed by the female after mating.Consumption of the spermatophylax keeps the female preoccupiedwhile sperm are discharged from the remaining portion of thespermatophore (sperm ampulla) into her repro ductive tract.The spermatophylax of long-winged males is significantly smallerthan that of short-winged males and consequently requires lesstime to consume. As a result, the sperm ampulla of long-wingedmales is frequently removed before its complete evacuation andsignificantly sooner than that of short-winged males. Becausethe spermatophore-removal behavior of females mediates the relativeinsemination success of short-winged and long-winged males,it can be considered a form of cryptic female choice     

The complex interplay between macronutrient intake,cuticular hydrocarbon expression and mating success in male decorated crickets

The condition dependence of male sexual traits plays a central role in sexual selection theory. Relatively little, however, is known about the condition dependence of chemical signals used in mate choice and their subsequent effects on male mating success. Furthermore, few studies have isolated the specific nutrients responsible for condition‐dependent variation in male sexual traits. Here, we used nutritional geometry to determine the effect of protein (P) and carbohydrate (C) intake on male cuticular hydrocarbon (CHC) expression and mating success in male decorated crickets (Gryllodes sigillatus). We show that both traits are maximized at a moderate‐to‐high intake of nutrients in a P:C ratio of 1 : 1.5. We also show that female precopulatory mate choice exerts a complex pattern of linear and quadratic sexual selection on this condition‐dependent variation in male CHC expression. Structural equation modelling revealed that although the effect of nutrient intake on mating success is mediated through condition‐dependent CHC expression, it is not exclusively so, suggesting that other traits must also play an important role. Collectively, our results suggest that the complex interplay between nutrient intake, CHC expression and mating success plays an important role in the operation of sexual selection in G. sigillatus.     

Female remating and the intensity of female choice in black-horned tree crickets, Oecanthus nigricornis

Repeated mating by females of many species occurs at frequenciesin excess of those needed to acquire additional sperm for fertilizingova. I tested three alternative hypotheses for the rate of rematingby females of the courtship-feeding tree cricket, Oecanthusnigricornis Walker, by manipulating diet quality and courtshipfeeding and measuring the time to remating by the female inrelation to four aspects of male phenotype (age, condition,fluctuating asymmetry, and size). First, in courtship-feedingspecies, remating may be due to selection to increase the amountof nutritional resources provided by males, with nutrient-deprivedfemales remating more quickly. Second, remating may functionas a mechanism of postcopulatory mate choice, with females rematingquickly when the quality of a previous mate is low. Third, quicknessof remating may be the consequence of precopulatory mate choiceprior to future matings, with females remating more quicklywith high-quality males, regardless of the quality of priormates. Females on a low-quality diet remated quickly, did notvary remating speed with the phenotype of their first mate,and did not differentially reject prospective second mates withdifferent phenotypes. In contrast, both the degree of coyness(measured as the frequency of mate rejection) and the intensityof female choice (measured as the size differential betweenaccepted and rejected mates) increased with diet quality. Theseresults support both the material-benefits and the precopulatorymate-choice hypotheses for remating speed of female tree crickets.There was mixed support for the postcopulatory choice hypothesis:females on the high-quality diet remated more slowly after firstmating with relatively large males, in support of the postcopulatorychoice hypothesis; however, the remating interval of femaleson the high-quality diet decreased with the condition of thefirst mate, opposite to the prediction of the postcopulatorychoice hypothesis     

Promiscuous mating produces offspring with higher lifetime fitness

In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco (Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extra-pair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.     

Female choice for male cuticular hydrocarbon profile in decorated crickets is not based on similarity to their own profile

Indirect genetic benefits derived from female mate choice comprise additive (good genes) and nonadditive genetic benefits (genetic compatibility). Although good genes can be revealed by condition‐dependent display traits, the mechanism by which compatibility alleles are detected is unclear because evaluation of the genetic similarity of a prospective mate requires the female to assess the genotype of the male and compare it to her own. Cuticular hydrocarbons (CHCs), lipids coating the exoskeleton of most insects, influence female mate choice in a number of species and offer a way for females to assess genetic similarity of prospective mates. Here, we determine whether female mate choice in decorated crickets is based on male CHCs and whether it is influenced by females' own CHC profiles. We used multivariate selection analysis to estimate the strength and form of selection acting on male CHCs through female mate choice, and employed different measures of multivariate dissimilarity to determine whether a female's preference for male CHCs is based on similarity to her own CHC profile. Female mating preferences were significantly influenced by CHC profiles of males. Male CHC attractiveness was not, however, contingent on the CHC profile of the choosing female, as certain male CHC phenotypes were equally attractive to most females, evidenced by significant linear and stabilizing selection gradients. These results suggest that additive genetic benefits, rather than nonadditive genetic benefits, accrue to female mate choice, in support of earlier work showing that CHC expression of males, but not females, is condition dependent.     

Sire coloration influences offspring survival under predation risk in the moorfrog

When breeding, male moor frogs Rana arvalis develop a bright blue dorsal coloration which varies in intensity between males. We tested whether this colour acts as a potential signal of a male's genetic quality to female moor frogs by artificially crossing pairs of males differing in the extent of the blue coloration to the same female. Maternal half-sibships provide a powerful means to detect paternal genetic effects on offspring as they control for other potentially confounding variables. We assayed the ability of offspring to survive an ecologically realistic test of fitness by exposing them to predation by the larvae of the predatory water beetle Dytiscus marginalis. Although sire's coloration did not influence tadpole body size, it did affect their ability to survive the predation trial. Offspring of bright blue males had higher survival than those of dull males when exposed to large predators, which were more voracious predators than smaller ones. Our results indicate that paternal secondary sexual traits provide information about genetic effects on offspring fitness in this species, but suggest that these effects may be context-dependent. Variable selection caused by contextual dependence may have important consequences for the evolution of female choice rules, and for the maintenance of genetic variation for both male trait and female preference.     

Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males in Drosophila melanogaster

A prominent hypothesis for polyandry says that male–male competitive drivers induce males to coerce already‐mated females to copulate, suggesting that females are more likely to be harassed in the presence of multiple males. This early sociobiological idea of male competitive drive seemed to explain why sperm‐storing females mate multiply. Here, we describe an experiment eliminating all opportunities for male–male behavioral competition, while varying females’ opportunities to mate or not with the same male many times, or with many other males only one time each. We limited each female subject's exposure to no more than one male per day over her entire lifespan starting at the age at which copulations usually commence. We tested a priori predictions about relative lifespan and daily components of RS of female Drosophila melanogaster in experimental social situations producing lifelong virgins, once‐mated females, lifelong monogamous, and lifelong polyandrous females, using a matched‐treatments design. Results included that (1) a single copulation enhanced female survival compared to survival of lifelong virgins, (2) multiple copulations enhanced the number of offspring for both monogamous and polyandrous females, (3) compared to females in lifelong monogamy, polyandrous females paired daily with a novel, age‐matched experienced male produced offspring of enhanced viability, and (4) female survival was unchallenged when monogamous and polyandrous females could re‐mate with age‐ and experienced‐matched males. (5) Polyandrous females daily paired with novel virgin males had significantly reduced lifespans compared to polyandrous females with novel, age‐matched, and experienced males. (6) Polyandrous mating enhanced offspring viability and thereby weakened support for the random mating hypothesis for female multiple mating. Analyzes of nonequivalence of variances revealed opportunities for within‐sex selection among females. Results support the idea that females able to avoid constraints on their behavior from simultaneous exposure to multiple males can affect both RS and survival of females and offspring.     

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.     

Macronutrient intake regulates sexual conflict in decorated crickets

Sexual conflict results in a diversity of sex‐specific adaptations, including chemical additions to ejaculates. Male decorated crickets (Gryllodes sigillatus) produce a gelatinous nuptial gift (the spermatophylax) that varies in size and free amino acid composition, which influences a female's willingness to fully consume this gift. Complete consumption of this gift maximizes sperm transfer through increased retention of the sperm‐containing ampulla, but hinders post‐copulatory mate choice. Here, we examine the effects of protein (P) and carbohydrate (C) intake on the weight and amino acid composition of the spermatophylax that describes its gustatory appeal to the female, as well as the ability of this gift to regulate sexual conflict via ampulla attachment time. Nutrient intake had similar effects on the expression of these traits with each maximized at a high intake of nutrients with a P : C ratio of 1 : 1.3. Under dietary choice, males actively regulated their nutrient intake but this regulation did not coincide with the peak of the nutritional landscape for any trait. Our results therefore demonstrate that a balanced intake of nutrients is central to regulating sexual conflict in G. sigillatus, but males are constrained from reaching the optima needed to bias the outcome of this conflict in their favour.     

Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides

Male reproductive success generally increases with number of mates but this need not be true for females. If females are the limiting sex, as few as one mate can be optimal. Despite the theoretical differences driving multiple mating in the sexes, multiple mating is the norm rather than the exception. Empirical investigations are therefore required to determine why females mate with multiple males. Both nonadaptive (correlated responses to selection on males, given the mean mating rates have to be the same) and adaptive (direct or indirect fitness benefits) can drive the evolution of multiple mating in females. Females of the burying beetle Nicorphorus vespilloides often mate repeatedly with the same male, but this appears to be a correlated response to selection on males rather than reflecting direct benefits to females for multiple mating. However, an unexamined alternative to this nonadaptive explanation is that females benefit by mating with multiple different males and therefore are selected for general promiscuity. Here we examine if mating polyandrously provides fitness benefits by examing the effects of number of mates (1, 2 or 3), mating system (monogamous, polyandrous) and their interaction. The only significant influence was mating more than once. This did not depend on type of mating. We suggest that unlike most other species examined, in N. vespilloides mating with the same male repeatedly or with several different males reflects an indiscriminate willingness to mate as a result of correlated selection on males for high rates of mating.     

Pre- and post-copulatory sexual selection increase offspring quality but impose survival costs to female field crickets

Whether sexual selection increases or decreases fitness is under ongoing debate. Sexual selection operates before and after mating. Yet, the effects of each episode of selection on individual reproductive success remain largely unexplored. We ask how disentangled pre- and post-copulatory sexual selection contribute to fitness of field crickets Gryllus bimaculatus. Treatments allowed exclusively for (i) pre-copulatory selection, with males fighting and courting one female, and the resulting pair breeding monogamously, (ii) post-copulatory selection, with females mating consecutively to multiple males and (iii) relaxed selection, with enforced pair monogamy. While standardizing the number of matings, we estimated a number of fitness traits across treatments and show that females experiencing sexual selection were more likely to reproduce, their offspring hatched sooner, developed faster and had higher body mass at adulthood, but females suffered survival costs. Interestingly, we found no differences in fitness of females or their offspring from pre- and post-copulatory sexual selection treatments. Our findings highlight the potential for sexual selection in enhancing indirect female fitness while concurrently imposing direct survival costs. By potentially outweighing these costs, increased offspring quality could lead to beneficial population-level consequences of sexual selection.     

Polyandry facilitates postcopulatory inbreeding avoidance in house mice

The avoidance of genetic incompatibilities between parental genotypes has been proposed to account for the evolution of polyandry. An extension of this hypothesis suggests polyandry may provide an opportunity for females to avoid the cost of inbreeding by exploiting postcopulatory mechanisms that bias paternity toward unrelated male genotypes. Here we test the inbreeding avoidance hypothesis in house mice by experimentally manipulating genetic compatibility via matings between siblings and nonsiblings. We observed little difference in reproductive success between females mated to two siblings or females mated to two nonsiblings. Females mated to both a sibling and a nonsibling tended to have a lower litter survival, but only when the first male to mate was a sibling. Microsatellite data revealed that paternity was biased toward nonsiblings when a female mated with both a sibling and a nonsibling. Unlike previous studies of invertebrates, paternity bias toward the sibling male was independent of mating sequence. We provide one of the first empirical demonstrations that polyandry facilitates postcopulatory sexual selection in a vertebrate. We discuss this result in relation to the possibility of selective fertilization of ova based on major histocompatibility complex (MHC) haploid expression of sperm.     

No direct or indirect benefits to cryptic female choice in house crickets (Acheta domesticus)

Cryptic female choice in crickets occurs through the prematureremoval of a male's spermatophore after copulation, which terminatessperm transfer. Although it is known that this behavior candirectly influence the paternity of offspring, its effects onfemale fitness have not been directly assessed. We tested thehypothesis that spermatophore removal by female house crickets(Acheta domesticus) confers fitness benefits on females, byrandomly assigning mates to females but permitting some femalesto freely remove spermatophores after mating (cryptic-choicetreatment) while forcing others to accept complete ejaculates(no-choice treatment). Although there was about a two-fold differencein the volume of ejaculate received by females of the two treatments,there were no significant differences in female longevity, reproductiveoutput, or offspring quality, as measured by offspring massand developmental time. Although differential spermatophoreremoval by females imposes strong sexual selection on males,the absence of a clear treatment effect suggests that femalesobtain no direct or indirect genetic benefits through theirpostcopulatory mating preferences.     

Maternal sexual interactions affect offspring survival and ageing

In many species, females exposed to increased sexual activity experience reductions in longevity. Here, in Drosophila melanogaster, we report an additional effect on females brought about by sexual interactions, an effect that spans generations. We subjected females to a sexual treatment consisting of different levels of sexual activity and then investigated patterns of mortality in their offspring. We found reduced probabilities of survival, increases in the rate of senescence and a pattern of reduced mean longevities, for offspring produced by mothers that experienced higher levels of sexual interaction. We contend that these effects constitute trans‐generational costs of sexual conflict – the existence or implications of which have rarely been considered previously. Our results indicate that ongoing exposure by mothers to male precopulatory interactions is itself sufficient to drive trans‐generational effects on offspring mortality. Thus, we show that increases in maternal sexual activity can produce trans‐generational effects that permeate through to latter life stages in the offspring. This helps to elucidate the complex interplay between sex and ageing and provides new insights into the dynamics of adaptation under sexual selection.     

Female mating decisions: maximizing fitness?

Sexual selection theory assumes that maximizing fitness is the ultimate goal in every mating decision. Fitness can be maximized directly by increasing the number of offspring (direct benefits) or indirectly by maximizing offspring's lifetime reproductive success (indirect benefits). Whereas there is considerable evidence in the literature for the influence of mating decisions on direct benefits, indirect benefits have been more elusive. Here, we review the variables that influence mating decisions made by females of freshwater fish and how these affect their fitness directly, as well as indirectly. Females enhance their fitness by matching their mating decisions to current environmental conditions, using a wide range of pre- and post-copulation mechanisms that enable them to maximize benefits from mating. Male sexual traits and courtship displays are signals used by females as a way of assessing male quality in terms of both direct and indirect benefits. Polyandry is very common among freshwater fish species, and indirect benefits have been hypothesized as drivers of its predominance. Despite intensive theoretical work, and multiple suggestions of the effects of indirect benefits, to date no study has been able to demonstrate experimentally the existence of indirect benefits in freshwater fish species. Additionally, most studies of direct benefits measure short-term benefits of mating decisions. In both cases, lifetime reproductive success is not assessed. Therefore, we are led to conclude that evidence as to whether female mating decisions result in direct and/or indirect benefits in freshwater fish species is still lacking. These results should be considered in light of the ongoing debate about the significance of indirect benefits in female mating decisions.     

Evolutionary causes and consequences of sequential polyandry in anuran amphibians

Among anuran amphibians (frogs and toads), there are two types of polyandry: simultaneous polyandry, where sperm from multiple males compete to fertilize eggs, and sequential polyandry, where eggs from a single female are fertilized by multiple males in a series of temporally separate mating events, and sperm competition is absent. Here we review the occurrence of sequential polyandry in anuran amphibians, outline theoretical explanations for the evolution of this mating system and discuss potential evolutionary implications. Sequential polyandry has been reported in a limited number of anurans, but its widespread taxonomic and geographic distribution suggests it may be common. There have been no empirical studies that have explicitly investigated the evolutionary consequences of sequential polyandry in anurans, but species with this mating pattern share an array of behavioural, morphological and physiological characteristics, suggesting that there has been common sexual selection on their reproductive system. Sequential polyandry may have a number of adaptive benefits, including spreading the risk of brood failure in unpredictable environments, insuring against male infertility, or providing genetic benefits, either through good genes, intrinsic compatibility or genetic diversity effects. Anurans with sequential polyandry provide untapped opportunities for innovative research approaches that will contribute significantly to understanding anuran evolution and also, more broadly, to the development of sexual‐selection and life‐history theory.