Life history and sex allocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema: the role of sperm competition

Sex allocation theory predicts that, in hermaphroditic organisms,individuals allocate a fixed amount of resources divided amongmale and female functions to reproduction and that the proportiondevoted to each sex depends on the mating group size. As themating group size increases, hermaphrodites are predicted toallocate proportionally more resources to the male and lessresources to the female function (approaching equal allocationto both sexes) to face increased sperm competition. Up to nowlittle experimental evidence has been provided to support thetheory in hermaphroditic animals. Facultative shift betweenmale and female allocation in response to variation in localgroup size does occur in several taxa but not always in theexpected direction and not with similar patterns. In the protandricand then simultaneously hermaphroditic polychaete worm Ophryotrochadiadema reproductive resources are flexibly allocated in theprotandrous and the hermaphroditic phase. The cost of male reproductionduring adolescence is spread over the whole energy budget ofthe animal as shown by the shortening of lifespan and the loweringof growth rate in individuals with enhanced male expenditureduring the protandrous phase. Moreover, in this species, shortterm sex allocation adjustments differ from those describedin other taxa. Individuals regulate their reproductive outputso that where reproductive competitors are present, the numberof female gametes is strongly reduced but the number of malegametes (although it changes) is not significantly increased.Resources subtracted from the female function are not directlyallocated to sperm production, but to expensive male behaviorsthat are likely to enhance male reproductive success. Theseresults are discussed in the light of the relevance of sexualselection in large populations of hermaphrodites.     

INTRASPECIFIC VARIATION IN SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE: THE EFFECT OF INDIVIDUAL SIZE

Within a population of simultaneous hermaphrodites, individuals may vary in both their current reproductive investment (biomass invested in gonads) and in how they allocate that investment between male and female function. In the chalk bass, Serranus tortugarum, estimates of both reproductive allocation and reproductive success as a male and a female can be made for individuals of different sizes. As individuals increase in size, their investment in gamete production increases, and there is a shift in allocation to a stronger female bias. Spawning frequency as a female in pair spawnings and as a male in both pair spawning and streaking (an alternative mating tactic) does not vary with individual size. As a result, larger individuals should release more sperm or eggs per spawn. Size-assortative pair spawning in this species leads to larger individuals having higher potential returns in total male reproductive success than smaller individuals, which should lead to increases in absolute levels of sperm production in larger individuals when individuals compete for fertilizations through sperm competition. However, smaller individuals contribute a smaller proportion of the sperm released in spawns with multiple spawners and thus are under more intense sperm competition than larger individuals, which should select for increases in male allocation in smaller individuals, all else equal. A local-mate-competition (LMC) model predicts that these factors select for increasing absolute male and female investment with individual size but a relative shift to more female-biased allocation as individual size increases. These predictions are supported by gonadal data. The predictions of average male allocation from the quantitative LMC model were 21.6% and 25.7%, whereas the collections averaged 21.3%. This close agreement of both the mean male allocation and its relative shift with individual size between model and data support the hypothesis that size-specific shifts in sex allocation in this species represent an adaptive response to patterns of mating success and sperm competition.     

Juvenile socio-sexual experience determines lifetime sperm expenditure and adult survival in a polygamous moth,Ephestia kuehniella

Male animals often adjust their sperm investment in response to sperm competition environment. To date, only a few studies have investigated how juvenile sociosexual settings affect sperm production before adulthood and sperm allocation during the first mating. Yet, it is unclear whether juvenile sociosexual experience (1) determines lifetime sperm production and allocation in any animal species; (2) alters the eupyrene : apyrene sperm ratio in lifetime ejaculates of any lepidopteran insects, and (3) influences lifetime ejaculation patterns, number of matings and adult longevity. Here we used a polygamous moth, Ephestia kuehniella, to address these questions. Upon male adult emergence from juveniles reared at different density and sex ratio, we paired each male with a virgin female daily until his death. We dissected each mated female to count the sperm transferred and recorded male longevity and lifetime number of matings. We demonstrate for the first time that males ejaculated significantly more eupyrenes and apyrenes in their lifetime after their young were exposed to juvenile rivals. Adult moths continued to produce eupyrene sperm, contradicting the previous predictions for lepidopterans. The eupyrene : apyrene ratio in the lifetime ejaculates remained unchanged in all treatments, suggesting that the sperm ratio is critical for reproductive success. Male juvenile exposure to other juveniles regardless of sex ratio caused significantly shorter adult longevity and faster decline in sperm ejaculation over successive matings. However, males from all treatments achieved similar number of matings in their lifetime. This study provides insight into adaptive resource allocation by males in response to juvenile sociosexual environment.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Sexual conflict in action: An antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby,Notamacropus eugenii

Sex ratio biases are often inconsistent, both among and within species and populations. While some of these inconsistencies may be due to experimental design, much of the variation remains inexplicable. Recent research suggests that an exclusive focus on mothers may account for some of the inconsistency, with an increasing number of studies showing variation in sperm sex ratios and seminal fluids. Using fluorescent in‐situ hybridization, we show a significant population‐level Y‐chromosome bias in the spermatozoa of wild tammar wallabies, but with significant intraindividual variation between males. We also show a population‐level birth sex ratio trend in the same direction toward male offspring, but a weaning sex ratio that is significantly female‐biased, indicating that males are disproportionately lost during lactation. We hypothesize that sexual conflict between parents may cause mothers to adjust offspring sex ratios after birth, through abandonment of male pouch young and reactivation of diapaused embryos. Further research is required in a captive, controlled setting to understand what is driving and mechanistically controlling sperm sex ratio and offspring sex ratio biases and to understand the sexually antagonistic relationship between mothers and fathers over offspring sex. These results extend beyond sex allocation, as they question studies of population processes that assume equal input of sex chromosomes from fathers, and will also assist with future reproduction studies for management and conservation of marsupials.     

Biases in sperm use in the mallard: no evidence for selection by females based on sperm genotype

If we are to understand fully the factors influencing fertilization success, it is essential to untangle male and female effects on sperm use. In many species, differences in fertilizing ability have been found between males or male genotypes, but the impact of female effects is less clear and may vary between taxa. Here, we examine sperm use in the mallard (Anas platyrhynchos), a species of bird in which forced copulation forms a major component of the mating system, to investigate whether there is any evidence for post-insemination female choice or rejection of particular sperm genotypes. Current models of sperm use in birds suggest observed patterns of paternity are a result of passive sperm loss from the reproductive tract and the relative timing of inseminations. Although this type of model successfully predicted average values of last male precedence observed in this species, there was considerable variation between females in their pattern of sperm use, with a tendency for females to use sperm of a single genotype. However, females did not consistently prefer one genotype over another in repeated inseminations with identical sperm mixtures, suggesting that post-insemination female preference based on sperm genotype did not account for this variation.     

Sex Allocation Ratio in a Wind-Pollinated Self-Incompatible Monoecious Tree, Alnus firma Sieb. et Zucc. (Betulaceae)

Abstract Biomass sex allocation of Alnus firma , a wind-pollinated self-incompatible monoecious tree species, was directly measured at the inflorescence (prezygotic) stage. Sex allocation ratio at the fruit stage was estimated from the number of female inflorescences, percent fruit production, and the mean dry weight of a female inflorescence and a fruit catkin. Investment in male function far exceeds that in female function at the prezygotic stage. When the costs of fruit catkins and seeds were included in the estimation of female function, then the sex allocation bias was reversed towards female. Intrapopulational variation of the sex allocation ratio with respect to tree height and size was also investigated. A strong negative correlation was observed in both cases, although a positive relationship has been predicted by theorists and some previous empirical data have supported this prediction.     

Temporal variation in sex allocation in the mealybug Planococcus citri: adaptation, constraint, or both?

Sex ratio theory has been very successful in predicting under which circumstances parents should bias their investment towards a particular offspring sex. However, most examples of adaptive sex ratio bias come from species with well-defined mating systems and sex determining mechanisms, while in many other groups there is still an on-going debate about the adaptive nature of sex allocation. Here we study the sex allocation in the mealybug Planococcus citri, a species in which it is currently unclear how females adjust their sex ratio, even though experiments have shown support for facultative sex ratio adjustment. Previous work has shown that the sex ratio females produce changes over the oviposition period, with males being overproduced early and late in the laying sequence. Here we investigate this complex pattern further, examining both the robustness of the pattern and possible explanations for it. We first show that this sex allocation behaviour is indeed consistent across lines from three geographical regions. Second, we test whether females produce sons first in order to synchronize reproductive maturation of her offspring, although our data provide little evidence for this adaptive explanation. Finally we test the age at which females are able to mate successfully and show that females are able to mate and store sperm before adult eclosion. Whilst early-male production may still function in promoting protandry in mealybugs, we discuss whether mechanistic constraints limit how female allocate sex across their lifetime.     

Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

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.     

FACULTATIVE SEX ALLOCATION BIASING BY WORKERS IN SOCIAL HYMENOPTERA

A single-locus two-allele model is analyzed to determine the invasion conditions for facultative biasing of colony sex allocation by hymenopteran workers in response to queen mating frequency, for a situation in which colonies have a single queen mated to one or two males. Facultative biasing of sex allocation towards increased male production in double mated colonies and increased female production in single mated colonies can both invade when the population sex allocation ratio is at the worker optimum. However, when the population sex allocation ratio is more male biased than the worker optimum, plausibly due to mixed queen and worker control, it is likely that only increased female allocation in colonies perceived by the workers to have single mated queens can invade. In this case, the frequency of mistakes made by workers in assessing queen mating frequency is an important constraint on the invasion of facultative male biasing in colonies perceived to have a double mated queen. When the population sex allocation ratio is not between the optima for workers in single and double mated colonies, plausibly due to strong queen control, then facultative biasing cannot invade. In this situation, workers in all colonies should attempt to bias allocation towards increased females. Worker male production in queenright colonies (provided not all males are worker-derived), unequal sperm use by double mated queens, and the amount of facultative biasing, do not alter these results.     

Sons are made from old stores: sperm storage effects on sex ratio in a lizard

Sperm storage is a widespread phenomenon across taxa and mating systems but its consequences for central fitness parameters, such as sex ratios, has rarely been investigated. In Australian painted dragon lizards (Ctenophorus pictus), we describe elsewhere that male reproductive success via sperm competition is largely an effect of sperm storage. That is, sperm being stored in the female reproductive tract out-compete more recently inseminated sperm in subsequent ovarian cycles. Here we look at the consequences of such sperm storage for sex allocation in the same species, which has genetic sex determination. We show that stored sperm have a 23% higher probability of producing sons than daughters. Thus, shifts in sex ratio, for example over the reproductive season, can partly be explained by different survival of son-producing sperm or some unidentified female mechanism taking effect during prolonged storage.     

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.     

Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade‐offs in mating systems that have been overlooked in the past.     

Temporal Variation in the Sex Ratio of a Natural Population of a Multivoltine Gall-Inducing Braconid Wasp

Temporal variation in the sex ratio of populations with continuous generations is poorly understood. We report changes in the sex ratio of a tropical gall-inducing braconid wasp throughout the fruiting season of its host plant. At the beginning of the season, fruits produce male biased sex ratios; at the end, female biased sex ratios. This change results from differential sex allocation rather than just earlier male emergence. A male bias followed by female bias is predicted following an increase in recruitment as occurs during the start of the main fruiting season, because males are likely to have the more consistent reproductive value over time. An initial male bias might also result from selection for protandry, or from constrained sex allocation during the low-density non-fruiting season.     

Coevolution of non-fertile sperm and female receptivity in a butterfly

Sexual conflict can promote rapid evolution of male and female reproductive traits. Males of many polyandrous butterflies transfer nutrients at mating that enhances female fecundity, but generates sexual conflict over female remating due to sperm competition. Butterflies produce both normal fertilizing sperm and large numbers of non-fertile sperm. In the green-veined white butterfly, Pieris napi, non-fertile sperm fill the females'' sperm storage organ, switching off receptivity and thereby reducing female remating. There is genetic variation in the number of non-fertile sperm stored, which directly relates to the female''s refractory period. There is also genetic variation in males'' sperm production. Here, we show that females'' refractory period and males'' sperm production are genetically correlated using quantitative genetic and selection experiments. Thus selection on male manipulation may increase the frequency of susceptible females to such manipulations as a correlated response and vice versa.     

SEX ALLOCATION IN THE MONOECIOUS HERB BEGONIA SEMIOVATA

Sex-allocation models predict that the evolution of self-fertilization should result in a reduced allocation to male function and pollinator attraction in plants. The evolution of sex allocation may be constrained by both functional and genetic factors, however. We studied sex allocation and genetic variation for floral sex ratio and other reproductive traits in a Costa Rica population of the monoecious, highly selfing annual Begonia semiovata. Data on biomass of floral structures, flower sex ratios, and fruit set in the source population were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and genetic correlations for floral sex ratio and for floral traits related to male and female function were estimated from the greenhouse-grown progeny of field-collected maternal families. The proportion of reproductive biomass invested in male function was low (0.34 at flowering, and 0.07 for total reproductive allocation). Significant among-family variation was detected in the size (mass) of individual male and female flowers, in the proportion of male flowers produced, and in the proportion of total flower mass invested in male flowers. Significant among-family variation was also found in flower number per inflorescence, petal length of male and female flowers, and petal number of female flowers. Except for female petal length, we found no difference in the mean value of these characters between selfed and outcrossed progeny, indicating that, with the possible exception of female petal length, the among-family variation detected was not the result of variation among families in the level of inbreeding. Significant positive phenotypic and broad-sense genetic correlations were detected between the mass of individual male and female flowers, between male and female petal length, and between number of male and number of female flowers per inflorescence. The ratio of stamen-to-pistil mass (0.33) was low compared to published data for autogamous species with hermaphroditic flowers, suggesting that highly efficient selfing mechanisms may evolve in monoecious species. Our results indicate that the study population harbors substantial genetic variation for reproductive characters. The positive genetic correlation between investment in male and female flowers may reflect selection for maximum pollination efficiency, because in this self-pollinating species, each female flower requires a neighboring male flower to provide pollen.     

Snail sperm production characteristics vary with sperm competition risk

Sperm competition is widespread and influences both male investment in spermatogenic tissue and ejaculate characteristics. Sperm competition models assume trade-offs between sperm size and number, although such trade-offs may be difficult to detect. This study examines the effects of sperm competition risk on the sperm production characteristics of the freshwater snail Viviparus ater. In this prosobranch, females mate frequently and store sperm, generating sperm competition. Males produce two sperm morphs, fertile eupyrene sperm and non-fertilizing oligopyrene sperm. Non-fertilizing sperm may play a role in sperm competition and therefore, like fertilizing sperm, the number produced could vary relative to sperm competition risk. In addition, trade-offs between sperm number and sperm size may be expected. We manipulated the sex ratio of sexually mature snails and found the presence of rivals affected the ratio of oligopyrene/eupyrene sperm males produced. In experimental and natural populations, the number of oligopyrene sperm produced, but not the number of eupyrene sperm, was significantly higher when the sex ratio was male biased. Testis mass did not vary between experimental treatments. We also found a negative relationship between the number and size of oligopyrene sperm produced, which is consistent with evolutionary models of sperm competition, and is, to our knowledge, the first intraspecific demonstration of a trade-off between these traits.     

Influence of body size on fecundity and sperm management in the parasitoid wasp Anisopteromalus calandrae

A large body size is considered to be advantageous to the reproductive success of females as a result of several factors, such as the allocation of more resources to reproduction and the efficient management of sperm transferred by males. In the present study, the effects of female body size, female mating status and additional food availability on fecundity and the offspring sex ratio are investigated in the parasitoid wasp Anisopteromalus calandrae Howard (Hymenoptera: Pteromalidae). Because of haplodiploid sex determination, females must fertilize eggs to produce female offspring but not to produce male offspring. As predicted, female fecundity and the number of female offspring are positively correlated with body size. However, although the volume of the spermatheca increases with female body size, the amount of sperm stored in the spermatheca is relatively constant, irrespective of body size. Consequently, larger females produce a greater proportion of male offspring, especially at the end of the oviposition sequence, suggesting that larger females that possess more resources for reproduction and produce a larger number of offspring are more likely to suffer sperm depletion. The results of the present study also show that mated females have an increased fecundity compared with virgin females, although the opportunity to feed on honey along with host feeding has no impact upon fecundity or the sex ratio.     

Precision in sex allocation is influenced by mate choice in Drosophila melanogaster

Theory predicts that a 1 : 1 sex ratio is favoured in the absence of countervailing selection pressures. In an experiment with Drosophila melanogaster, we found significantly greater variation in the offspring sex ratios of freely mated flies than would be expected by the binomial distribution. In a surprise result, control flies given no mate choice exhibited significant under-dispersal in their sex ratio variation, possibly from sperm limitation. Both treatments, however, produced populations with a 1 : 1 sex ratio. This supports the hypothesis that sexually antagonistic selection for reproductive success in sons, and fecundity in daughters, may overcome selection for an equal sex ratio. Such precision in sex allocation may allow for the maintenance of genetic variation underlying trade-offs between male and female reproductive success.