Lovesick: immunological costs of mating to male sagebrush crickets

A growing body of evidence suggests that resources invested in reproduction often come at the expense of the ability to mount an immune response. During mating, female sagebrush crickets, Cyphoderris strepitans, consume the ends of the male’s hind wings and ingest his haemolymph. Previous research has shown that this behaviour impairs the ability of males to secure additional matings. One hypothesis to account for this effect is that wing wounding triggers an energetically costly immune response, such that nonvirgin males are unable to sustain the costly acoustical signalling needed to attract additional females. To test this hypothesis, we injected virgin males with lipopolysaccharides (LPS) to provoke an immune response, and monitored their mating success in the field. LPS‐injected virgin males took significantly longer to mate than sham‐injected virgin males, and spent significantly less time calling. We also compared virgin, nonvirgin and experimentally wing‐wounded virgin males with respect to: (1) their ability to encapsulate a foreign invader via the accumulation of haemocytes and deposition of melanin and (2) baseline levels of phenoloxidase (PO), a key enzyme in the biochemical cascade leading to the production of melanin. Although encapsulation ability did not differ with reproductive experience, virgin males had significantly higher levels of PO than either nonvirgin or experimentally wing‐wounded virgin males. These results suggest that wing‐wounding alone is sufficient to impair male immunity, and that males trade‐off investment in reproduction and immunity.     

Genetic association between male attractiveness and female differential allocation

Differential allocation of reproductive effort towards offspring of attractive mates is a form of post-copulatory mate choice. Although differential allocation has been demonstrated in many taxa, its evolutionary implications have received little attention. Theory predicts that mate choice will lead to a positive genetic correlation between female preference and male attractiveness. This prediction has been upheld for pre-copulatory mate choice, but whether such a relationship between male attractiveness and female differential allocation exists has never been tested. Here, we show that both female pre-copulatory mate choice and post-copulatory differential allocation are genetically associated with male attractiveness in house crickets, Acheta domesticus. Daughters of attractive males mated sooner and laid more eggs when paired with larger males. These forms of mate choice are strongest in large females, suggesting that costs decrease with increasing female size. The genetic association between attractiveness and differential allocation suggests potential for differential allocation to become exaggerated by coevolutionary runaway processes in an analogous manner to pre-copulatory choice. Sexual selection is thus likely to be stronger than predicted by pre-copulatory choice alone.     

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.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

The role of cuticular hydrocarbons in male attraction and repulsion by female Dawson's burrowing bee, Amegilla dawsoni

Cuticular hydrocarbons (CHCs) are long-chain fatty acids and their derivatives that protect insects from desiccation. They can also be important semiochemicals in insect reproduction. We used behavioural and chemical assays to examine the potential role of CHCs in sexual communication in a solitary burrowing bee, Amegilla dawsoni. Washing CHC blends from the cuticle of emerging virgin females made them unattractive to mate-searching males. Returning the CHC blends restored their attractiveness. Nesting females were unattractive to mate-searching males, whether they were washed or not. Chemical analysis identified significant differences between male and female CHC blends and between virgin female and nesting female blends. Some of these differences were due to specific compounds. Loss of attractiveness is unlikely to be due to antiaphrodisiac compounds delivered by males, because male-specific compounds were not found on nesting females, and because recently mated females with intact CHC blends were attractive to searching males. Nesting females could not be made attractive to searching males by removing their CHC blends. Adding virgin female CHC blends tended to improve attractiveness but the effect was weak, suggesting that some form of volatile compound may also be involved in signalling unreceptivity.     

Changes in male sexual responses from silk cues of females at different reproductive states in the wolf spider Schizocosa malitiosa

Male wolf spiders are capable of recognising sexual signals associated with female silk threads. In the wolf spider Schizocosa malitiosa variations in female receptivity have been studied, but changes in female silk attractiveness remain unknown. We analysed the sexual responses of adult males (leg shaking, papal drumming and searching) exposed to silk cues from subadult, virgin and mated females of different ages, and females that were or were not carrying an egg-sac. Penultimate and recently moulted adult females elicited low levels of male sexual behaviour, while those of virgin females (21–40 days old) were the most attractive. Silk threads slowly became less attractive after mating. Cues from females carrying an egg-sac as well as females in the inter egg-sac period were fairly attractive. The low attractiveness of recently moulted females disagrees with their high sexual receptivity. In contrast, females continued to elicit strong male responses during a 10-day period after mating, despite the fact that they immediately become sexually reluctant, suggesting strong selection for male searching ability. Low attractiveness during the egg-carrying period could reflect the fact that females do not require any further sperm. Concordances and discordances between attractiveness and sexual receptivity suggest that they respond to different physiological mechanisms.     

注射胸腺依赖和非胸腺依赖抗原雄性黑线毛足鼠的内分泌状态和气味吸引力

作者研究了胸腺依赖抗原 (SRBC) (羊红血细胞 ,sheepredbloodcells ,SRBC)和非胸腺依赖抗原 (细菌脂多糖 ,lipopolysaccharide ,LPS)的免疫活化对黑线毛足鼠气味信号和内分泌状态的影响。成年雄鼠注射SRBS5天后 ,其气味的性吸引力下降 ,这种结果伴随着粪便中睾酮含量的下降。SRBC处理后 ,雄性气味吸引力降低 ,这在体液免疫反应低的雄性个体中最明显。与SRBC的作用相反 ,注射LPS的雄性个体的气味吸引力增加 ,成熟雌性个体用于嗅闻嗅觉刺激上的时间差异与经LPS和盐处理过的雄鼠的粪便中睾酮浓度的差异呈正相关。作者讨论了这两种相反的嗅觉效应的适应性意义     

The Effects of Age and Previous Mating Experience on Pre- and Post-copulatory Mate Choice in Female House Crickets (<Emphasis Type="Italic">Acheta domesticus</Emphasis> L.)

Although females’ mating preferences are influenced by male characteristics, there are a number of factors intrinsic to females and unrelated to male phenotype that can modulate female choice. We assessed the effects of age and mating experience on mechanisms of pre- and post-copulatory mate choice in female house crickets, Acheta domesticus L., by randomly assigning males to females, but independently varying the age and number of previous matings of females at the time of experimental matings. Latency to mating, a measure of a female’s pre-copulatory preference, was influenced by female age at the time of mating, with older females mating sooner than younger females. The reduced selectivity of older females appears consistent with life-history theory, which predicts that the reproductive value of females should decline with age. The length of time that females retained the spermatophore after mating, a measure of a female’s post-copulatory mating preference, was not influenced by female age at the time of mating, the number of previous matings, or any interaction between the two main effects. Contrary to previous reports, male mass had no effect on either the latency to mating or female retention of the spermatophore in A. domesticus. We conclude that female age and mating experience can moderate female selectivity, but that their impact varies according to the mechanism by which females favor particular sires.     

Female choice and the relatedness of mates in the guppy (<Emphasis Type="Italic">Poecilia reticulata</Emphasis>)

Several studies suggest that females may offset the costs of genetic incompatibility by exercising pre-copulatory or post-copulatory mate choice to bias paternity toward more compatible males. One source of genetic incompatibility is the degree of relatedness among mates; unrelated males are expected to be genetically more compatible with a female than her relatives. To address this idea, we investigated the potential for inbreeding depression and paternity biasing mechanisms (pre- and post-copulatory) of inbreeding avoidance in the guppy, Poecilia reticulata. Inbreeding resulted in a reduction in offspring number and quality. Females mated to siblings gave birth to significantly fewer offspring compared to females mated to non-siblings and inbred male offspring took longer to reach sexual maturity. There was no evidence of inbreeding avoidance in pre-copulatory behaviors of females or males. Sexual responsiveness of females to courting males and the number of sexual behaviors males directed at females did not decrease as a function of the relatedness of the two individuals. We also tested whether female guppies can use post-copulatory mechanisms to bias sperm usage toward unrelated males by comparing the number of offspring produced by females mated to two of their siblings (SS), two males unrelated to the female (NN), or to one unrelated male and a sibling male (NS). We found that NS females produced a number of offspring not significantly different than what would be expected if fertilization success were halfway between completely outbreeding (NN) and completely inbreeding (SS) females. This suggests that there is no significant improvement in the number of offspring produced by females mating to both related and unrelated males, relative to that which would be expected if sperm from both males were used equally. Our results suggest that female guppies do not discriminate against closely related males or their sperm.     

Antagonistic pre- and post-copulatory sexual selection on male body size in a water strider (Gerris lacustris)

A crucial question in sexual selection theory is whether post-copulatory sexual selection reinforces or counteracts conventional pre-copulatory sexual selection. Male body size is one of the traits most generally favoured by pre-copulatory sexual selection; and recent studies of sperm competition often suggest that large male size is also favoured by post-copulatory sexual selection. In contrast to this general pattern, this study shows that pre- and post-copulatory sexual selection act antagonistically on male body size in Gerris lacustris. One large and one small male were kept together with two females in this experiment. Large males had a significant mating advantage, but small males copulated longer and gained higher fertilization success from each mating. Large and small males, however, gained similar reproductive success, and there was no overall correlation between mating success and reproductive success. These results suggest that estimates of male fitness based solely on mating success should be viewed with caution, because of potentially counteracting post-copulatory selection.     

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.     

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice‐mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S₂) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.     

Mating Status Effects on Sexual Response of Males and Females in the Parasitoid Wasp <Emphasis Type="Italic">Urolepis rufipes</Emphasis>

Although mate preferences are most commonly examined in females, they are often found in both sexes. In the parasitoid wasp Urolepis rufipes, both female and male mating status affected certain aspects of sexual interactions. Female mating status mattered only in the later stages of mating. Males did not discriminate between virgin and mated females in terms of which they contacted or mounted first. However, once mounted, most virgin females were receptive to copulation, whereas very few mated females were. Whether a male’s mating status affected his own sexual response depended on the female’s ability to respond and the stage of mating. Examining male behavior toward dead females allowed elimination of the role of female behavior in how males responded. Virgin and mated males are both attracted to dead females as evidenced by their fanning their wings at such females. However, mated males were quicker than virgin males to contact and to mount in an experiment with dead females, whereas there was no such differential response in an experiment with live females. This difference is consistent with greater female sexual responsiveness to virgin males. Male mating status also affected female receptivity to copulate. Once mounted, live virgin females were less likely to become receptive to copulation by mated males than to virgin males, but only in a choice experiment, not in a no-choice experiment.     

Female social preference for males that have evolved via monogamy: evidence of a trade-off between pre- and post-copulatory sexually selected traits?

When females mate with multiple males both pre- and post-copulatory sexual selections occur. It has been suggested that females benefit from polyandry when better-quality males are successful in sperm competition and sire high-quality offspring. Indeed, studies of experimental evolution have confirmed that sperm competition selects for both increased ejaculate quality and elevated offspring viability. Fewer investigations have explored whether these fitness benefits are evident beyond early life-history stages. Here, I used house mice (Mus domesticus) from selection lines that had been evolving for 25 generations under either polygamy or monogamy to test whether females preferred males from lines that had evolved with sperm competition. Males from the polygamous lines had previously been shown to achieve a fitness advantage under semi-natural conditions, deeming them to be of high genetic quality and leading to the a priori expectation that females would prefer males that had evolved with sperm competition compared with males that had not. Contrary to expectation, the data showed that sexually receptive females spent more time associating with males from the monogamous lines. This unexpected but interesting result is discussed in relation to sperm competition theory that predicts a trade-off between male investment in pre- and post-copulatory sexually selected traits.     

Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies

Polyandry, where females mate with multiple males, means that a male''s reproductive success will depend both on his ability to acquire mates and the ability of his sperm to compete effectively for fertilizations. But, how do males partition their reproductive investment between these two episodes of selection? Theory predicts that increases in ejaculate investment will come at a cost to investment in other reproductive traits. Although evidence revealing such trade-offs is accumulating, we know little about their genetic basis. Here, I report patterns of genetic (co)variation for a range of traits subject to pre- and post-copulatory sexual selection in the guppy Poecilia reticulata, a promiscuous livebearing fish in which males alternate between courtship and sneak matings to obtain copulations. The analyses of genetic variation and covariation for these behaviours revealed a strong genetic predisposition for one tactic over the other. Both mating tactics were also strongly genetically integrated with the level of sexual ornamentation and ejaculate quality. Males that predominantly performed sneak matings were less ornamented but had faster swimming sperm than those that predominantly used courtship. These patterns of genetic variation and covariation reveal potential evolutionary constraints on the direction of selection of pre- and post-copulatory traits, and support sperm competition theory by revealing a trade-off between sexual attractiveness and investment in ejaculates.     

The Opportunity for Post-Copulatory Sexual Selection in the Ectoparasitic Pea Crab,Dissodactylus primitivus (Brachyura: Pinnotheridae)

Pea crabs, Dissodactylus primitivus, inhabit multiple echinoid (heart urchin) hosts. Male and female crabs move among hosts in search for mates, and both sexes mate multiple times, creating opportunities for post-copulatory sexual selection. For such selection to occur, only a fraction of the males who succeed in mating can also succeed in siring progeny. Jossart et al. 2014 used 4 microsatellite loci to document parentage and mating frequencies of both sexes in D. primitivus. From these data we identified the mean and variance in female offspring numbers, as well as the proportions of the female population that were gravid and not bearing offspring. We next identified the proportions of the male population who had (1) mated and sired offspring, (2) mated but failed to sire offspring, and (3) failed to mate altogether. We used these results to estimate the opportunity for selection on males and females in terms of mate numbers and offspring numbers, and estimated the sex difference in the opportunity for selection (i.e., the opportunity for sexual selection) using both forms of data. We then partitioned the total variance in male fitness into pre- and post-copulatory components and identified the fraction of the total opportunity for selection occurring in each context. Our results show that the opportunity for selection on each sex was of similar magnitude (0.69–0.98), consistent with this polyandrogynous mating system. We also found that 37% of the total opportunity for sexual selection on males occurred within the context of post-copulatory sexual selection. However, the fraction of the total opportunity for selection that was due to sexual selection, estimated using both mate numbers and offspring numbers, was 9% and 23% respectively. Thus, we further reduced our estimate of the opportunity for post-copulatory sexual selection in D. primitivus to less than 10% of the total opportunity for selection (0.37 of 0.09 and 0.23 = 0.03 and 0.09). Our results provide the first estimate of the maximum possible strength of post-copulatory sexual selection in crustaceans using this approach.     

Sexually dimorphic immune response in the harem polygynous Wellington tree weta Hemideina crassidens

Abstract Adult males are often less immunocompetent than females. One explanation for this is that intense sexual selection causes males to trade‐off investment in immunity with traits that increase mating success. This hypothesis is tested in the Wellington tree weta (Hemideina crassidens), a large, sexually dimorphic orthopteran insect in which males possess enormous mandibular weaponry used during fights for access to female mates. Field‐collected males have a significantly greater immune response (greater melanotic encapsulation) than females, suggesting that body condition, longevity or an allied trait is important to male fitness, or that females require materials for egg production that would otherwise be used to boost immunity. Although immunity is expected to trade‐off against reproductive traits in both sexes, there is no significant relationship between immune response and weapon or testes size in males, nor fecundity in females.     

Female-limited X-chromosome evolution effects on male pre- and post-copulatory success

Intralocus sexual conflict arises when the expression of shared alleles at a single locus generates opposite fitness effects in each sex (i.e. sexually antagonistic alleles), preventing each sex from reaching its sex-specific optimum. Despite its importance to reproductive success, the relative contribution of intralocus sexual conflict to male pre- and post-copulatory success is not well-understood. Here, we used a female-limited X-chromosome (FLX) evolution experiment in Drosophila melanogaster to limit the inheritance of the X-chromosome to the matriline, eliminating possible counter-selection in males and allowing the X-chromosome to accumulate female-benefit alleles. After more than 100 generations of FLX evolution, we studied the effect of the evolved X-chromosome on male attractiveness and sperm competitiveness. We found a non-significant increase in attractiveness and decrease in sperm offence ability in males expressing the evolved X-chromosomes, but a significant increase in their ability to avoid displacement by other males'' sperm. This is consistent with a trade-off between these traits, perhaps mediated by differences in body size, causing a small net reduction in overall male fitness in the FLX lines. These results indicate that the X-chromosome in D. melanogaster is subject to selection via intralocus sexual conflict in males.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.