Sperm limitation affects sex allocation in a parasitoid wasp Nasonia vitripennis

Insect reproduction is influenced by various external factors including temperature, a well-studied constraint. We investigated to what extent different levels of sperm limitation of males exposed to different heat stresses (34 and 36℃) afFect fem ales' offspring production and sex allocation in Nasonia vitripennis. In this haplodiploid parasitoid wasp attacking different species of pest flies, we investigated the effect of the quantity of sperm females received and stored in their spermatheca on their sperm use decisions, hence sex allocation, over successive ovipositions. In particular, we compared the sex allocation of females presenting three levels of sperm limitation (i.e.,mated with control, 34 ℃ heat-stressed or 36℃heat-stressed males) on each host they parasitized. To disentangle the potential reduction of sperm quality after a heat stress exposure from that of sperm quantity, we also explored the clutch size and sex ratio produced by fem ales that were partially sperm limited after copulating with multiply mated males. Independently of their sperm numbers, all types of fem ales produced a similar total number of offspring, but the more limited ones had fewer daughters. Sperm limitation further affected the distribution of daughters' production across time.In addition to constraints acting on female physiology, male fertility should therefore be considered in studies measuring reproductive outputs of insects submitted to heat stresses.     

Male facial attractiveness and masculinity may provide sex‐ and culture‐independent cues to semen quality

Phenotype‐linked fertility hypothesis (PLFH) predicts that male secondary sexual traits reveal honest information about male fertilization ability. However, PLFH has rarely been studied in humans. The aim of the present study was to test PLFH in humans and to investigate whether potential ability to select fertile partners is independent of sex or cultural background. We found that on the contrary to the hypothesis, facial masculinity was negatively associated with semen quality. As increased levels of testosterone have been demonstrated to impair sperm production, this finding may indicate a trade‐off between investments in secondary sexual signalling (i.e. facial masculinity) and fertility or status‐dependent differences in investments in semen quality. In both sexes and nationalities (Spanish and Colombian), ranked male facial attractiveness predicted male semen quality. However, Spanish males and females estimated facial images generally more attractive (gave higher ranks) than Colombian raters, and in both nationalities, males gave higher ranks than females. This suggests that male facial cues may provide culture‐ and sex‐independent information about male fertility. However, our results also indicate that humans may be more sensitive to facial attractiveness cues within their own populations and also that males may generally overestimate the attractiveness of other men to females.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Colorful male guppies do not provide females with fecundity benefits

The phenotype-linked fertility hypothesis (PLFH) predicts thatmales with elaborated sexual ornaments signal their high fertilizingefficiency to females and that female preferences for ornamentedmales are driven by direct fecundity benefits. Although somestudies have demonstrated that attractive males produce moreor higher quality sperm, there is limited experimental evidencethat females derive fecundity benefits by mating with attractivemales. Some of the best indirect evidence for the PLFH comesfrom work on guppies (Poecilia reticulata), an internally fertilizingspecies of freshwater fish in which phenotypically attractivemales produce larger and relatively higher quality ejaculatesthan their less attractive counterparts. We used artificialinsemination to impregnate female guppies using known numbersof sperm from a range of males with different phenotypes andrelated female fecundity (brood success, time from inseminationto parturition, and brood size) to sperm numbers and male phenotype(body size and the relative area of color spots). We found noevidence that male phenotype or experimentally adjusted "ejaculate"size influenced any of our measures of female fecundity. Theseresults highlight the importance of experimentally investigatingpotential fecundity benefits associated with female mating preferencesbefore concluding that the maintenance of these preferencesis driven by the pursuit of such benefits.     

A Combined Approach to Heat Stress Effect on Male Fertility in Nasonia vitripennis: From the Physiological Consequences on Spermatogenesis to the Reproductive Adjustment of Females Mated with Stressed Males

In recent years, several studies have shown a decline in reproductive success in males in both humans and wildlife. Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capacities due to environmental stresses can have strong negative ecological impacts, and also dramatic consequences on world food production if it affects the reproductive success of biological control agents, such as parasitic wasps used to control crop pests. Here Nasonia vitripennis, a parasitic wasp of various fly species, was studied to test the effects of 24h-heat stress applied during the first pupal stage on male fertility. Results showed that only primary spermatocytes were present at the first pupal stage in all cysts of the testes. Heat stress caused a delay in spermatogenesis during development and a significant decrease in sperm stock at emergence. Females mated with these heat-stressed males showed a reduce sperm count stored in their spermatheca. Females did not appear to distinguish heat-stressed from control males and did not remate more frequently to compensate for the lack of sperm transferred. As a result, females mated with heat-stressed males produced a suboptimal lifetime offspring sex ratio compared to those mated with control males. This could further impact the population dynamics of this species. N. vitripennis appears to be an interesting biological model to study the mechanisms of subfertility and its consequence on female reproductive strategies and provides new research perspectives in both invertebrates and vertebrates.     

Reproductive strategies of the larval parasitoid Microplitis croceipes

Mate choice may have important consequences for offspring sex ratio and fitness of haplodiploid insects. Mate preference of females of the solitary larval parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) for virgin and mated males, and vice versa, and the reproductive consequences (i.e., the sex ratio expressed as the proportion of male offspring) were examined in choice and non‐choice experiments. In addition, the effect of repeated rapid and daily copulation of an individual male on the sex ratio of offspring of the female mates was assessed. Males preferred virgins over mated females, whereas females copulated with a male irrespective of his mating status. In both the rapid and daily copulation assay, females copulating with a male that had copulated five times or more produced a higher sex ratio than females that had copulated with a virgin male. Females that copulated with virgin males once or twice produced a significantly and considerably lower sex ratio than females that first copulated with a sperm‐depleted male followed by a virgin male. This indicates that copulating with a sperm‐depleted male has costs and limits acquisition by the female of sperm from virgin males.     

A sex allocation cost to polyandry in a parasitoid wasp

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.     

Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae)

1. Multiple male copulations can have detrimental effects on female fitness due to sperm limitation. 2. Monandrous Naryciinae females are immobile while the males are short‐lived and do not feed. Multiple male mating is therefore expected to lead to sperm limitation in females. Sperm limitation and male limitation are hypothesised as causes of the repeated evolution of parthenogenetic reproduction in the Psychidae. 3. In this study, the effects of multiple male mating on female reproduction are investigated in several species of Naryciinae by allowing males multiple copulations. The results for two species, Siederia listerella and Dahlica lichenella, are compared. The sex ratios of 53 natural populations are examined for indications of male limitation. 4. Previous copulations by the male increased the female's risk of remaining unfertilised. However, contrary to expectations, those unfertilised females were capable of successful re‐mating. 5. In S. listerella, the number of previous copulations of males negatively influenced female fitness. Females produced 30% fewer offspring if they mated with a previously mated male. In D. lichenella, the older the male and the lower its number of total lifetime copulations, the higher the female's reproductive success. 6. Only a fraction of the investigated populations had a female‐skewed sex ratio, but differences in development time between males and females could lead to reproductive asynchrony. 7. In conclusion, male mating history did not lead to strong sperm limitation in Naryciinae as had been suggested by their life history.     

Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera)

Parasitoid Nasonia wasps adjust their progeny sex ratio to the presence of conspecifics to optimize their fitness. Another trait under female control is the induction of offspring diapause. We analysed progeny sex ratios and the proportion of diapausing offspring of individual Nasonia females in host patches parasitized by two species, Nasonia vitripennis and Nasonia giraulti, in North American field populations using microsatellite fingerprinting. Both Nasonia species produced similar sex ratios on hosts that were co‐parasitized by their own species as by the other species, indicating that females do not distinguish between con‐ and heterospecific clutches. The sex ratios of the diapause and adult fractions of mixed broods from single females were not correlated. We found further indications that N. vitripennis females take the emergence time of the offspring into account in their sex allocation. The reproductive strategies of Nasonia under multiparasitism are largely adaptive, but also partially constrained by information.     

A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod

A number of parasites are vertically transmitted to new host generations via female eggs. In such cases, host reproduction is an intimate component of parasite fitness and no cost of the infection on host reproduction is expected to evolve. A number of these parasites distort host sex ratios towards females, thereby increasing either parasite fitness or the proportion of the host that transmit the parasite. In terrestrial isopods (woodlice), Wolbachia bacteria are responsible for sex reversion and female-biased sex ratios, changing genetic males into functional neo-females. Although sex ratio distortion is a powerful means for parasites to increase in frequency in host populations, it also has potential consequences on host biology, which may, in turn, have consequences for parasite prevalence. We used the woodlouse Armadillidium vulgare to test whether the interaction between Wolbachia infection and the resulting excess of females would limit female fertility through the reduction in sperm number that they receive from males. We showed that multiple male mating induces sperm depletion, and that this sperm depletion affects fertility only in infected females. This decrease in fertility, associated with male mate choice, may limit the spread of Wolbachia infections in host populations.     

Consequences of sperm displacement for female dung flies,Scatophaga stercoraria

Displacement of stored sperm during copulation occurs in many insects. This process provides direct benefits for males via increased fertilization success, but the fitness consequences of sperm displacement for females are less clear. Here we investigate potential benefits of sperm displacement for female yellow dung flies, Scatophaga stercoraria. We find no evidence that female dung flies gain direct benefits from displacement of previously stored sperm in terms of increased fertility or fecundity. There was no difference in the relative survival rate, development time, size or fluctuating asymmetry of offspring produced by females that had previously stored sperm displaced before oviposition and those that did not. Females using previously stored sperm to fertilize their eggs produced significantly higher ratios of male to female offspring. These novel findings have important implications for understanding the evolutionary dynamics of male–female interactions in sperm competition.     

Brothers smell similar: variation in the sex pheromone of male European Beewolves Philanthus triangulum F. (Hymenoptera: Crabronidae) and its implications for inbreeding avoidance

Female choice is thought to increase the fitness returns of females. The complementary choice model states that the best mate depends on the particular genotype of a female. Aculeate Hymenoptera represent a special case of complementary female choice because males should be chosen on the basis of their allele at the sex determination locus. The prevalent sex determination mechanism in bees and wasps (single-locus complementary sex determination) requires that, to produce a daughter, diploid offspring are heterozygous at the sex determination locus. Otherwise, infertile diploid males result. Inevitably, the proportion of diploid males increases with the rate of inbreeding. In the European Beewolf, males scent mark territories to attract mates and the composition of the pheromone might provide a basis for female choice. One crucial prerequisite for females to be able to discriminate against brothers and avoid inbreeding is that the male sex pheromone varies with familial affiliation. This hypothesis was tested by analysing the pheromone of male progeny of eight mothers using gas chromatography and mass spectrometry. A significantly higher similarity was found among brothers than among unrelated individuals. Such a genetic component of a male sex pheromone has not yet been described from aculeate Hymenoptera.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 433–442.     

Host acceptance and sex allocation of Nasonia wasps in response to conspecifics and heterospecifics

Species recognition is an important aspect of an organism''s biology. Here, we consider how parasitoid wasps vary their reproductive decisions when their offspring face intra- and interspecific competition for resources and mates. We use host acceptance and sex ratio behaviour to test whether female Nasonia vitripennis and Nasonia longicornis discriminate between conspecifics and heterospecifics when ovipositing. We tested pairs of conspecific or heterospecific females ovipositing either simultaneously or sequentially on a single host, using strains varying in their recent history of sympatry. Both N. vitripennis and N. longicornis rejected parasitized hosts more often than unparasitized hosts, although females were more likely to superparasitize their own species in the sequential treatment. However, sex ratio behaviour did not vary, suggesting similar responses towards conspecifics and heterospecifics. This contrasts with theory predicting that heterospecifics should not influence sex ratios as their offspring do not influence local mate competition, where conspecifics would. These non-adaptive sex ratios reinforce the lack of adaptive kin discrimination in N. vitripennis and suggest a behavioural constraint. Discrimination between closely related species is therefore context dependent in Nasonia. We suggest that isolating mechanisms associated with the speciation process have influenced behaviour to a greater extent than selection on sex ratios.     

Courtship rate signals fertility in an externally fertilizing fish

Sperm limitation is widespread across many animal species. Several mechanisms of sperm allocation have been proposed, including optimal allocation according to clutch size and equal allocation across females. However, considerably less effort has been directed at investigating the behavioural signals associated with sperm limitation in males, which may include mating rate and the intensity of courtship. We investigated whether multiple successive spawnings affect individual male fertilization success, mating rates and courtship rates in Japanese medaka (Oryzias latipes). Across an average of 17 spawning events per male, fertilization success decreased from 83.7 per cent for the first spawning to 40 per cent for the last spawning while courtship rate decreased from 3.4 to 1.5 min⁻¹. Females appeared to respond to male sperm depletion by reducing clutch size. Our results suggest that male Japanese medaka are sperm-limited, and that courtship rate may be an honest indication of fertilization ability.     

Male red coloration,female mate preference,and sperm longevity in the cyprinid fish Puntius titteya

In recent decades, the link between the exaggeration of male sexual ornaments and ejaculate quality has received much attention. When males with conspicuous sexual ornaments have high-quality ejaculate, females are believed to obtain benefits, such as high fertilization success and offspring with good genes, by choosing mates on the basis of male ornamentation. In this study, we examined the relationships among male body coloration, female mate preference, and sperm longevity in the sexually dichromatic fish Puntius titteya. Males of this species assume a bright red coloration over the entire body, and neither sex invests in the parental care of eggs. In the female preference test, females preferred males with redder body coloration over their counterpart males with duller coloration. In addition, the sperm longevity test indicated that redder males had sperm with greater longevity. These results suggest that the red coloration of males in this species may signal sperm longevity and that females can mate with males with higher quality sperm by choosing redder males.     

Females avoid manipulative males and live longer

Abstract Female mate choice has been demonstrated in a wide variety of species and is now accepted as an important factor in sexual selection. One of the remaining questions, however, is why females prefer specific males. Do females or their offspring benefit from their choice? Or do females choose mates to minimize costs of mating? Here we show that, in the ovoviviparous cockroach Nauphoeta cinerea, where sexual selection has been well documented, females chose mates to avoid costly male manipulation. Females were partnered with preferred or nonpreferred mates, and fitness of the females measured. We found that females lived longer when they mated with preferred males. Female lifespan depended on the rate at which offspring developed from egg to parturition: slower development led to longer life. We manipulated the male pheromone and showed that the component of the pheromone blend that makes males attractive to females also delayed parturition. Thus, like other aspects of sexual conflict in this species, offspring development and thereby the mother's lifespan depended on exposure of females to specific components of the male pheromone. Males benefit from manipulating offspring development because females with accelerated parturition remained unreceptive whereas females with slower developing offspring readily remated after giving birth to their offspring. Our results suggest a hormone‐like role for the male pheromone in N. cinerea and provide the first direct evidence of mate choice to avoid male manipulation. This study shows that dominant males may not be preferred males if they are manipulating females, why multiple components with contrasting effects can exist in a sexual signal, and emphasizes the complex fitness relationships that can arise in species with sexual conflict.     

Life‐history traits of the Whiting polyploid line of the parasitoid Nasonia vitripennis

In hymenopterans, males are normally haploid (1n) and females diploid (2n), but individuals with divergent ploidy levels are frequently found. In species with ‘complementary sex determination’ (CSD), increasing numbers of diploid males that are often infertile or unviable arise from inbreeding, presenting a major impediment to biocontrol breeding. Non‐CSD species, which are common in some parasitoid wasp taxa, do not produce polyploids through inbreeding. Nevertheless, polyploidy also occurs in non‐CSD Hymenoptera. As a first survey on the impacts of inbreeding and polyploidy of non‐CSD species, we investigate life‐history traits of a long‐term laboratory line of the parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) (‘Whiting polyploid line’) in which polyploids of both sexes (diploid males, triploid females) are viable and fertile. Diploid males produce diploid sperm and virgin triploid females produce haploid and diploid eggs. We found that diploid males did not differ from haploid males with respect to body size, progeny size, mate competition, or lifespan. When diploid males were mated to many females (without accounting for mating order), the females produced a relatively high proportion of male offspring, possibly indicating that these males produce less sperm and/or have reduced sperm functionality. In triploid females, parasitization rate and fecundity were reduced and body size was slightly increased, but there was no effect on lifespan. After one generation of outbreeding, lifespan as well as parasitization rate were increased, and a body size difference was no longer apparent. This suggests that outbreeding has an effect on traits observed in an inbred polyploidy background. Overall, these results indicate some phenotypic detriments of non‐CSD polyploids that must be taken into account in breeding.     

How parasitoid females produce sexy sons: a causal link between oviposition preference, dietary lipids and mate choice in Nasonia

Sexual selection theory predicts that phenotypic traits used to choose a mate should reflect honestly the quality of the sender and thus, are often costly. Physiological costs arise if a signal depends on limited nutritional resources. Hence, the nutritional condition of an organism should determine both its quality as a potential mate and its ability to advertise this quality to the choosing sex. In insects, the quality of the offspring's nutrition is often determined by the ovipositing female. A causal connection, however, between the oviposition decisions of the mother and the mating chances of her offspring has never been shown. Here, we demonstrate that females of the parasitic wasp Nasonia vitripennis prefer those hosts for oviposition that have been experimentally enriched in linoleic acid (LA). We show by (13)C-labelling that LA from the host diet is a precursor of the male sex pheromone. Consequently, males from LA-rich hosts produce and release higher amounts of the pheromone and attract more virgin females than males from LA-poor hosts. Finally, males from LA-rich hosts possess three times as many spermatozoa as those from LA-poor hosts. Hence, females making the right oviposition decisions may increase both the fertility and the sexual attractiveness of their sons.     

Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata

Abstract. 1. Adult males of the two-spot ladybird beetle, Adalia bipunctata , did not show a functional response to increase in aphid abundance and consumed markedly fewer aphids than do the females.
2. At high densities of prey, females spent more time in area-restricted search than when prey was scarce. Males were always less active than females and they did not respond to an increase in prey abundance by a change in searching behaviour.
3. After a brief encounter with a female, a male showed area-restricted searching behaviour. This behaviour occurred in response to encountering a female's elytra and in particular to a chloroform-soluble component (sex pheromone) present on or in the elytra.
4. Males needed to encounter a female in order to respond to her presence, which indicated the pheromone is a contact pheromone.
5. The searching behaviour of males appeared to be mainly directed towards locating females; that of females towards locating aphids. This difference between the sexes should be taken into account when quantifying the predatory response of ladybirds to aphid abundance in the field.     

The effect of sperm storage and timing of mating on offspring sex ratios in the yellow dung fly Scatophaga stercoraria

1. Offspring sex ratios in the yellow dung fly Scatophaga stercoraria were examined in the laboratory. 2. Previous work indicated that females using previously stored sperm to fertilise their eggs produced male‐biased sex ratios. This result may have been due to female influences or the effects of sperm storage per se. 3. This pattern was not reproduced in the study presented here. Females that were allowed to mate just prior to oviposition produced similarly male‐biased sex ratios to those females that used previously stored sperm to fertilise their clutch. 4. Captive‐reared females may have perceived a lack of males in the population and thus produced a male‐biased offspring sex ratio. Alternatively, gamete ageing or extra‐chromosomal sex ratio distorters may have produced the male bias.