Ejaculate expenditures of male crickets in response to varying risk and intensity of sperm competition: not all species play games

Costs incurred in the manufacture of ejaculates may constrainthe number of sperm that males can produce, so males shouldshow some economy in their allocation of sperm across multiplematings. In species in which females mate with multiple malesand are capable of storing sperm for extended periods, spermallocation of males should be tailored to the risk of spermcompetition. Recent game theory predicts that males shouldtransfer the least sperm when there are no other rivals, andthe most sperm when only one other rival is likely to inseminatethe female. However, as the numbers of competitors increasesbeyond two, the models predict a corresponding decrease in ejaculate expenditure. We tested these predictions in three cricket species, Gryllodes sigillatus, Gryllus veletis, and Gryllus texensis, assessing the sperm allocation of males held under three levelsof apparent interrival competition: no rivals, one rival andsix rivals. Sperm allocation of G. veletis varied accordingto theory: males increased their sperm allocation with an increasedrisk of sperm competition (no rivals vs. one), but decreasedtheir allocation with an increased intensity of sperm competition(one rival vs. six). Sperm allocation of male G. texensis showedno significant response to the density of rivals, and spermallocation in G. sigillatus was influenced by an unexpectedinteraction between treatment density and the order in whichmales experienced the three treatments. The observed interspecificvariation in facultative sperm allocation may be due to interspecificdifferences in population density, rearing environment, orfemale mating behavior.     

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.     

FEMALE CONTROL OF SPERM TRANSFER AND INTRASPECIFIC VARIATION IN SPERM PRECEDENCE: ANTECEDENTS TO THE EVOLUTION OF A COURTSHIP FOOD GIFT

Manipulation of ejaculates is believed to be an important avenue of female choice throughout the animal kingdom, but evidence of its importance to sexual selection remains scarce. In crickets, such manipulation is manifest in the premature removal of the externally attached spermatophore, which may afford females an important means of postcopulatory mate choice. We tested the hypothesis that premature spermatophore removal contributes significantly to intraspecific variation in sperm precedence by (1) experimentally manipulating spermatophore attachment durations of competing male Gryllodes sigillatus and (2) employing protein electrophoresis to determine the paternity of doubly mated females. The relative spermatophore attachment durations of competing males had a significant influence on male paternity, but the pattern of sperm precedence deviated significantly from the predictions of an ideal lottery. Instead, paternity data and morphological evidence accorded best with a model of partial sperm displacement derived here. Our model is similar to a displacement model of Parker et al. in that sperm of the second male mixes instantaneously with that of the first throughout the displacement process, but the novel feature of our model is that the number of sperm displaced is only a fraction of the number of sperm transferred by the second male. Regardless of the underlying mechanism, female G. sigillatus can clearly alter the paternity of their offspring through their spermatophore-removal behavior, and employ such cryptic choice in favoring larger males and those providing larger courtship food gifts. We discuss how female control of sperm transfer and intraspecific variation in sperm precedence may be important precursors to the evolution of gift giving in insects.     

Food fight: sexual conflict over free amino acids in the nuptial gifts of male decorated crickets

In decorated crickets, Gryllodes sigillatus, the spermatophore that a male transfers at mating includes a gelatinous spermatophylax that the female consumes, delaying her removal of the sperm‐filled ampulla. Male fertilization success increases with the length of time females spend feeding on the spermatophylax, while females may benefit by prematurely discarding the spermatophylaxes of undesirable males. This sexual conflict should favour males that produce increasingly appealing spermatophylaxes, and females that resist this manipulation. To determine the genetic basis of female spermatophylax feeding behaviour, we fed spermatophylaxes to females of nine inbred lines and found that female genotype had a major influence on spermatophylax feeding duration. The amino acid composition of the spermatophylax was also significantly heritable. There was a positive genetic correlation between spermatophylax feeding duration and the gustatory appeal of the spermatophylax. This correlation suggests that genes expressed in males that produce more manipulative spermatophylaxes are positively linked to genes expressed in females that make them more vulnerable to manipulation. Outbred females spent less time feeding on spermatophylaxes than inbred females, and thus showed greater resistance to male manipulation. Further, in a nonspermatophylax producing cricket (Acheta domesticus), females were significantly more prone to feeding on spermatophylaxes than outbred female Gryllodes. Collectively, these results suggest a history of sexually antagonistic coevolution over the consumption of nuptial food gifts.     

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.     

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.     

Hemolymph loss during nuptial feeding constrains male mating success in sagebrush crickets

Although costs of mating have been widely documented in females,intrinsic costs of copulation have been poorly documented inmales, and there is little evidence that such costs constrainmale mating success under natural conditions. Male sagebrushcrickets, Cyphoderris strepitans, offer females an unusual somaticfood gift at copulation that may constitute a significant costof copulation: females chew on the ends of the males' fleshyhind wings and ingest hemolymph seeping from the wounds theyinflict. Previous studies have shown that once a male has mated,his probability of obtaining an additional copulation is reducedrelative to that of a virgin male seeking to secure his firstmating. If the future mating prospects of nonvirgin males arediminished because of the costs of copulation, this could stemeither from the resources required to manufacture a new spermatophoreor through the energy needed to replenish hemolymph lost throughfemale wing-feeding. To distinguish between these two alternatives,we experimentally depleted virgin males of varying amounts hemolymphin a way that mimicked hemolymph loss of nonvirgin males, withoutthe attendant costs of spermatophore production. After theyhad been treated, males were released in the field and recapturedover the course of the breeding season to monitor their matingsuccess. Control males mated significantly sooner than did malesdepleted of hemolymph. We conclude, therefore, that the depletionof hemolymph that occurs through female wing feeding is sufficientby itself to diminish a nonvirgin male's ability to secure anothermating.     

Mate choice by male water striders (Gerris lacustris): expression of a wing morph preference depends on a size difference between females

Natural selection maintains wing polymorphism in populationsof water striders. Long-winged females benefit from being ableto migrate because they avoid the risk of pool evaporation,but early in the season their fecundity is lower than that ofshort-winged females. We tested preferences of 18 long-wingedmales and 29 short-winged males in spring. Males preferred long-wingedfemales, and there was no difference between the two male morphs.The preference was only observed when the long-winged femalewas heavier; when the short-winged female was larger, the malesshowed no preference. There was a positive relationship betweenlong-winged female weight and number of eggs laid per day, andthe males behaved as if they were taking into account that large,long-winged females are more fecund. We suggest that males preferredlong-winged females because this preference increases the proportionof long-winged individuals in the autumn F2 generation.     

Biting off more than you can chew: sexual selection on the free amino acid composition of the spermatophylax in decorated crickets

Nuptial food gifts function to enhance male fertilization success, but their consumption is not always beneficial to females. In decorated crickets, the spermatophore transferred at mating includes a gelatinous mass, the spermatophylax, which is consumed by females after mating. However, females often discard spermatophylaxes shortly after mating, whereupon they terminate sperm transfer. We hypothesized that females discard gifts based on their assessment of the gift itself, and specifically the composition of free amino acids. We tested this hypothesis by comparing spermatophylaxes discarded by females after mating with those that were destined to be fully consumed, and employed multivariate selection analysis to quantify the strength and form of multivariate sexual selection operating on the free amino acid composition of gifts. The analysis yielded a saddle-shaped fitness surface with two local peaks. Different amino acid profiles appear to elicit continued feeding on the spermatophylax either because they offer the same level of gustatory appeal, or because they differentially affect both the gustatory appeal and texture of the spermatophylax. We conclude that the gustatory response of females to males' nuptial food gifts represents an important avenue of post-copulatory mate choice, imposing significant sexual selection on the free amino acid composition of the spermatophylax.     

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.     

Female remating propensity contingent on sexual cannibalism in sagebrush crickets, Cyphoderris strepitans: a mechanism of cryptic female choice

Male sagebrush crickets (Cyphoderris strepitans) permit femalesto engage in an unusual form of sexual cannibalism during copulation:females feed on males' fleshy hind wings and ingest hemolymphoozing from the wounds they inflict. These wounds are not fatal,and normally only a portion of the hind wings are eaten at anyone mating, so that mated males are not precluded from matingagain. As a result, nonvirgin males have fewer material resources tooffer females than do virgin males, such that females shouldbe selected to preferentially mate with high-investment virginmales. We tested the hypothesis that female mating preferencesfavor males capable of supplying females with the highest materialinvestment. Our results indicate that both female diet and opportunitiesfor sexual cannibalism influence female mating behavior. Femalesmaintained on a low-nutrient diet mounted males significantlysooner than females maintained on a high-nutrient diet, indicatingthat a female's overall nutrient intake may determine her propensityto mate. In addition, females were significantly more reluctantto mount and mate with males whose hind wings had been surgicallyremoved and thus were incapable of providing females with awing meal. Finally, females initially mated to dewinged malesremated with winged males significantly sooner than femalesallowed to feed freely during their initial mating, resultingin cryptic female choice of investing males.     

Give ‘til it hurts: trade‐offs between immunity and male reproductive effort in the decorated cricket,Gryllodes sigillatus

Trade‐offs between life‐history variables can be manifested at either the phenotypic or genetic level, with vastly different evolutionary consequences. Here, we examined whether male decorated crickets (Gryllodes sigillatus) from eight inbred lines and the outbred founder population from which they were derived, trade‐off immune effort [lytic activity, phenoloxidase (PO) activity or encapsulation] to produce spermatophylaxes: costly nuptial food gifts essential for successful sperm transfer. Canonical correlation analysis of the outbred population revealed a trade‐off between spermatophylax mass and lytic activity. Analysis of our inbred lines, however, revealed that although PO activity, encapsulation, body mass, spermatophylax mass and ampulla (sperm capsule) mass were all highly heritable, lytic activity was not, and there was, therefore, no negative genetic correlation between lytic activity and spermatophylax mass. Thus, males showed a phenotypic but not a genetic trade‐off between spermatophylax mass and lytic activity, suggesting that this trade‐off is mediated largely by environmental factors.     

Heritable variation in the timing of spermatophore removal, a mechanism of post-copulatory female choice in crickets

Female crickets can exert post-copulatory mating preferences by prematurely removing a male's spermatophore after copulation, which terminates sperm transfer. Although most models of sexual selection assume that female mating preferences are heritable, there has been little work addressing genetic variation underlying post-copulatory mate choice. We used a paternal half-sib design, in which different males were randomly assigned as mates to several females to create half-sib families, to determine the heritability of spermatophore retention time in female house crickets, Acheta domesticus. There was significant additive genetic variance in the timing of spermatophore removal by females [h(2) = 0.50 +/- 0.19 (+/- SE)], suggesting that the timing of spermatophore removal is determined, in part, by the female's own genotype independent of the quality of her mate. The relatively high heritability of spermatophore retention time may be reflective of the absence of strong selection on this trait, consistent with previous work showing no difference in the fitness of females permitted to freely remove the spermatophore of their mates and those forced to accept complete ejaculates.     

Repeatability of mate choice in female red jungle fowl

We staged female mate choice trials between pairs of males andrepeated the process for each female to determine the repeatabilityof female preference for males in red jungle fowl (Gallus gallus)in the first and second half of the breeding season. We measuredmale morphological traits (the size and color of the comb andthe brightness of the hackle feathers) that females are knownto use in choosing a mate. In the first half of the breedingseason, females showed repeatability in their choices of matewith respect to the male's comb characters. Females did notshow a repeatable preference with respect to male hackle feathers,and we found no repeatability of mate choice in the second halfof the season. Females seem to primarily look at the male'scomb when choosing a mate, and other ornaments seem only ofsecondary importance.[Behav Ecol 7: 243-246 (1996)]     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

Variability in wing form of crickets

Population Ecology - Loss of functional hindwings is observed in most subfamilies of Japanese crickets. Habitat, behaviour, body size and phylogenetic factors might be involved, but interactions...     

Cryptic male choice: sperm allocation strategies when female quality varies

We examined evolutionary stable sperm allocation and included stochastic variation in male mating frequency, not included in previous models examining sperm allocation strategies. We assumed sperm mixing and variation in female quality and used a genetic algorithm to analyse the evolution of male sperm allocation. Our results show that males should invest more sperm in initial copulations than in subsequent copulations as a male might fail to mate again. The inclusion of variation in female fecundity had no influence on the evolutionary stable sperm allocation strategy if males were unable to recognize female quality. If males were assumed to allocate sperm in response to female quality, the proportion of sperm allocated was positively correlated with female quality. Moreover, with increasing variance in female quality, males conserved more sperm for later copulations. Literature data on sperm allocation from diverse taxa show a good fit with the predictions given by our model.