Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences

The sexes often differ in the reproductive trait limiting their fitness, an observation known as Bateman's principle. In many species, females are limited by their ability to produce eggs while males are limited by their ability to compete for and successfully fertilize those eggs. As well as promoting the evolution of sex-specific reproductive strategies, this difference may promote sex differences in other life-history traits due to their correlated effects. Sex differences in disease susceptibility and immune function are common. Two hypotheses based on Bateman's principle have been proposed to explain this pattern: that selection to prolong the period of egg production favors improved immune function in females, or that the expression of secondary sexual characteristics reduces immune function in males. Both hypotheses predict a relatively fixed pattern of reduced male immune function, at least in sexually mature individuals. An alternative hypothesis is that Bateman's principle does not dictate fixed patterns of reproductive investment, but favors phenotypically plastic reproductive strategies with males and females adaptively responding to variation in fitness-limiting resource availability. Under this hypothesis, neither sex is expected to possess intrinsically superior immune function, and immunological sex differences may vary in different environments. We demonstrate that sex-specific responses to experimental manipulation of fitness-limiting resources affects both the magnitude and direction of sex differences in immune function in Drosophila melanogaster. In the absence of sexual interactions and given abundant food, the immune function of adults was maximized in both sexes and there was no sex difference. Manipulation of food availability and sexual activity resulted in female-biased immune suppression when food was limited, and male-biased immune suppression when sexual activity was high and food was abundant. The immunological cost to males of increased sexual activity was found to be due in part to reduced time spent feeding. We suggest that for species similarly limited in their reproduction, phenotypic plasticity will be an important determinant of sex differences in immune function and other life-history traits.     

On sexual dimorphism in immune function

Sexual dimorphism in immune function is a common pattern in vertebrates and also in a number of invertebrates. Most often, females are more 'immunocompetent' than males. The underlying causes are explained by either the role of immunosuppressive substances, such as testosterone, or by fundamental differences in male and female life histories. Here, we investigate some of the main predictions of the immunocompetence handicap hypothesis (ICHH) in a comparative framework using mammals. We focus specifically on the prediction that measures of sexual competition across species explain the observed patterns of variation in sex-specific immunocompetence within species. Our results are not consistent with the ICHH, but we do find that female mammals tend to have higher white blood cell counts (WBC), with some further associations between cell counts and longevity in females. We also document positive covariance between sexual dimorphism in immunity, as measured by a subset of WBC, and dimorphism in the duration of effective breeding. This is consistent with the application of 'Bateman's principle' to immunity, with females maximizing fitness by lengthening lifespan through greater investment in immune defences. Moreover, we present a meta-analysis of insect immunity, as the lack of testosterone in insects provides a means to investigate Bateman's principle for immunity independently of the ICHH. Here, we also find a systematic female bias in the expression of one of the two components of insect immune function that we investigated (phenoloxidase). From these analyses, we conclude that the mechanistic explanations of the ICHH lack empirical support. Instead, fitness-related differences between the sexes are potentially sufficient to explain many natural patterns in immunocompetence.     

Female‐biased size dimorphism in a diapausing caddisfly,Mesophylax aspersus: effect of fecundity and natural and sexual selection

1. The effect of mating success, female fecundity and survival probability associated with intra‐sex variation in body size was studied in Mesophylax aspersus, a caddisfly species with female‐biased sexual size dimorphism, which inhabits temporary streams and aestivates in caves. Adults of this species do not feed and females have to mature eggs during aestivation. 2. Thus, females of larger size should have a fitness advantage because they can harbour more energy reserves that could influence fecundity and probability of survival until reproduction. In contrast, males of smaller size might have competitive advantages over others in mating success. 3. These hypotheses were tested by comparing the sex ratio and body size of individuals captured before and after the aestivation period. The associations between body size and female fecundity, and between mating success and body size of males, were explored under laboratory conditions. 4. During the aestivation period, the sex ratio changed from 1 : 1 to male biased (4 : 1), and a directional selection on body size was detected for females but not for males. Moreover, larger clutches were laid by females of larger size. Finally, differences in mating success between small and large males were not detected. These results suggest that natural selection (i.e. the differential mortality of females associated with body size) together with possible fecundity advantages, are important factors responsible of the sexual size dimorphism of M. aspersus. 5. These results highlight the importance of taking into account mechanisms other than those traditionally used to explain sexual dimorphism. Natural selection acting on sources of variation, such as survival, may be as important as fecundity and sexual selection in driving the evolution of sexual size dimorphism.     

Geographical variation and sexual dimorphism of phenoloxidase levels in Japanese beetles (Popillia japonica)

Phenoloxidase (PO) production can be used as an indicator of pathogen defence in insects. The geographical mosaic of coevolution implies that traits associated with pathogen defence will vary across a geographical range. Bateman's principle implies that the benefit of increased defence levels is greater for females than males. To test both of these hypotheses, we sampled four populations of Japanese beetles, Popillia japonica, across Vermont: two were from locations using biological pest control, and two locations did not use biocontrol. We quantified defence levels (PO) and parasite resistance in males and females from each population. Populations from areas with biocontrol exhibited greater PO production, females produced more PO, populations with higher levels of PO suffered less mortality from pathogen exposure, and PO levels positively correlate with increased mortality in the absence of parasitism. Results support the geographical mosaic of coevolution and the implications of Bateman's principle.     

Bateman's principle and immunity

The immunocompetence handicap hypothesis (ICHH) of Folstad and Karter has inspired a large number of studies that have tried to understand the causal basis of parasite-mediated sexual selection. Even though this hypothesis is based on the double function of testosterone, a hormone restricted to vertebrates, studies of invertebrates have tended to provide central support for specific predictions of the ICHH. I propose an alternative hypothesis that explains many of the findings without relying on testosterone or other biochemical feedback loops. This alternative is based on Bateman's principle, that males gain fitness by increasing their mating success whilst females increase fitness through longevity because their reproductive effort is much higher. Consequently, I predict that females should invest more in immunity than males. The extent of this dimorphism is determined by the mating system and the genetic correlation between males and females in immune traits. In support of my arguments, I mainly use studies on insects that share innate immunity with vertebrates and have the advantage that they are easier to study.     

Bateman's Principle and Simultaneous Hermaphrodites: A Paradox

Bateman's principle states that reproductive success is limiteda) in females by the resources available for egg production;and b) in males, only by access to females and/or eggs. Theprinciple has been used to generate predictions for two aspectsof hermaphroditism; a) the advantage of hermaphroditism andb) sexual conflict. Comparing these predictions to the empiricaldata offers tests of Bateman's principle. Charnov's predictionthat hermaphroditism would occur under circumstances where Bateman'sprinciple does not apply is found to be largely correct. However,the prediction as to the association of hermaphroditism andlow fixed costs is inconsistent with the data. Alternative explanationsthat predict that hermaphroditism is a strategy for reducingvariance in reproductive success may better explain the data.Probability theory demonstrates that where two strategies haveequal mean fitness, which must be the case for male and femalefunction, the strategy with the lower variance in reproductivesuccess must have higher fitness (Gillespie's principle). Bateman'sprinciple predicts that this will be the female role in hermaphrodites.However, Charnov, assuming Bateman's principle, predicted thatsexual conflict stemming from a preference for the male rolewould be important in hermaphrodite mating systems, creatinga paradox. Many hermaphrodite mating systems are based on conditionalreciprocity with a preferred sexual role indicating sexual conflict.The data demonstrate that the preferred role varies among taxa,contrary to the predictions of Bateman's principle. It has beensuggested that Bateman's principle can explain cases in whichthe female role is preferred (sperm-trading) as involving energyrather than gamete trading. However, energetic considerationssuggest that energy trading would only be adaptive if Bateman'sprinciple does not apply, paradoxically. The gamete tradingmodel, based on the prediction that the role that offers controlof fertilization will be preferred, is more consistent withthe data. Application of Bateman's principle to hermaphroditesleads to contradictory predictions and does not offer the basisfor a coherent theory of sexual selection, as Bateman proposed.     

Sex allocation and nestling survival in a dimorphic raptor: does size matter?

Fisher's theory predicts equal sex ratios at the end of parentalcare if the costs and benefits associated with raising eachsex of offspring are equal. In raptors, which display variousdegrees of reversed sexual size dimorphism (RSD; females thelarger sex), sex ratios biased in favor of smaller males areonly infrequently reported. This suggests that offspring ofeach sex may confer different fitness advantages to parents.We examined the relative returns associated with raising eachsex of offspring of the brown falcon Falco berigora, a medium-sizedfalcon exhibiting RSD (males approximately 75% of female bodymass) and subsequent sex ratios. Female nestlings hatched eitherfirst or second did not receive more food nor did they hatchfrom larger eggs or remain dependent on parents for longer periodsthan male offspring from these hatch orders. Together with previousstudies this result indicates that even in markedly dimorphicspecies, the required investment to raise the larger sex islikely to be less than that predicted by body size differencesalone. Moreover, among last-hatched nestlings, both sexes faceda reduced food allocation and suffered a slower growth rateand thus final body size, with a concurrent increased probabilityof mortality. For last-hatched females the reduction in foodallocation was more marked, with complete mortality of all last-hatchedfemale nestlings monitored in this study. Once independent,males of any size but only larger females are likely to be recruitedinto the breeding population. The sex-biased food allocationamong last-hatched offspring favoring males thus reflects therelative returns to parents in raising a small member of eachsex.     

Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination

An adaptive explanation for environmental sex determination is that it promotes sexual size dimorphism when larger size benefits one sex more than the other. That is, if growth rates are determined by environment during development, then it is beneficial to match developmental environment to the sex that benefits more from larger size. However, larger size may also be a consequence of larger size at hatching or growing for a longer time, i.e., delayed age at first reproduction. Therefore, the adaptive significance of sexual size dimorphism and environmental sex determination can only be interpreted within the context of both growth and maturation. In addition, in those animals that continue to grow after maturation, sexual size dimorphism at age of first reproduction could differ from sexual size dimorphism at later ages as growth competes for energy with reproduction and maintenance. I compared growth using annuli on carapace scales in two species of box turtles (Terrapene carolina and T. ornata) that have similar patterns of environmental sex determination but, reportedly, have different patterns of sexual size dimorphism. In the populations I studied, sexual size dimorphism was in the same direction in both species; adult females were, on average, larger than adult males. This was due in part to males maturing earlier and therefore at smaller sizes than females. In spite of similar patterns of environmental sex determination, patterns of growth differed between the species. In T. carolina, males grew faster than females as juveniles but females had the larger asymptotic size. In T. ornata, males and females grew at similar rates and had similar asymptotic sizes. Sexual size dimorphism was greatest at maturation because, although males matured younger and smaller, they grew more as adults. There was, therefore, no consistent pattern of faster growth for females that may be ascribed to developmental temperature. Received: 20 March 1996 / Accepted: 10 March 1998     

Explaining sex differences in lifespan in terms of optimal energy allocation in the baboon

We provide a quantitative test of the hypothesis that sex role specialization may account for sex differences in lifespan in baboons if such specialization causes the dependency of fitness upon longevity, and consequently the optimal resolution to an energetic trade‐off between somatic maintenance and other physiological functions, to differ between males and females. We present a model in which females provide all offspring care and males compete for access to reproductive females and in which the partitioning of available energy between the competing fitness‐enhancing functions of growth, maintenance, and reproduction is modeled as a dynamic behavioral game, with the optimal decision for each individual depending upon his/her state and the behavior of other members of the population. Our model replicates the sexual dimorphism in body size and sex differences in longevity and reproductive scheduling seen in natural populations of baboons. We show that this outcome is generally robust to perturbations in model parameters, an important finding given that the same behavior is seen across multiple populations and species in the wild. This supports the idea that sex differences in longevity result from differences in the value of somatic maintenance relative to other fitness‐enhancing functions in keeping with the disposable soma theory.     

Adaptiveness of sex ratio control by the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size

Adaptiveness of sex ratio control by the solitary parasitoid wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size was studied, by examining whether differential effects of host size on the fitness of resulting wasps are to be found between males and females. The offspring sex ratio (male ratio) decreased with increasing host size. Larger hosts yielded larger wasps. Male larvae were less efficient in consuming larger hosts than female larvae. No significant interaction in development time was found between parasitoid sex and host size. Larger female wasps lived longer than smaller females, while longevity of male wasps did not increase with increasing wasp size. Smaller males were able to mate either with small or with large females, while larger males failed to mate with small females. Larger female wasps had a greater number of ovarioles and mature eggs at any one time than smaller females, although the number of eggs produced per host-feeding was not influenced by female wasps. Thus, the differential effect of host size on the fitness of males and females exists in I. naranyae. The basic assumption of the host-size model was therefore satisfied, demonstrating that sex ratio control by I. naranyae in response to host size is adaptive.     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Diet, sex, and death in field crickets

Senescence is shaped by age-dependent trade-offs between fitness components. Because males and females invest different resources in reproduction, the trade-offs behind age-dependent reproductive effort should be resolved differently in the sexes. In this study, we assess the effects of diet (high carbohydrate and low protein vs. equal carbohydrate and protein) and mating (once mated vs. virgin) on lifespan and age-dependent mortality in male and female field crickets (Teleogryllus commodus), and on male calling effort. Females always had higher actuarial ageing rates than males, and we found a clear lifespan cost of mating in females. Mated males, however, lived longer than virgin males, possibly because virgins call more than mated males. The fastest age-dependent increases in mortality were among mated males on the high-carbohydrate diet. Males on a high-carbohydrate diet showed a faster increase in calling effort earlier in life, and a more pronounced pattern of senescence once they reached this peak than did males on a diet with equal amounts of protein and carbohydrates. Our results provide evidence that the cost of mating in this cricket species is both diet and sex-dependent, and that the underlying causes of sex differences in life-history traits such as lifespan and senescence can be complex.     

POLYGYNANDRY IN THE DUSKY PIPEFISH SYNGNATHUS FLORIDAE REVEALED BY MICROSATELLITE DNA MARKERS

In the dusky pipefish Syngnathus floridae, like other species in the family Syngnathidae, ‘pregnant’ males provide all post-zygotic care. Male pregnancy has interesting implications for sexual selection theory and the evolution of mating systems. Here, we employ microsatellite markers to describe the genetic mating system of S. floridae, compare the outcome with a previous report of genetic polyandry for the Gulf pipefish S. scovelli, and consider possible associations between the mating system and degree of sexual dimorphism in these species. Twenty-two pregnant male dusky pipefish from one locale in the northern Gulf of Mexico were analyzed genetically, together with subsamples of 42 embryos from each male's brood pouch. Adult females also were assayed. The genotypes observed in these samples document that cuckoldry by males did not occur; males often receive eggs from multiple females during the course of a pregnancy (six males had one mate each, 13 had two mates, and three had three mates); embryos from different females are segregated spatially within a male's brood pouch; and a female's clutch of eggs often is divided among more than one male. Thus, the genetic mating system of the dusky pipefish is best described as polygynandrous. The genetic results for S. floridae and S. scovelli are consistent with a simple model of sexual selection which predicts that for sex role-reversed organisms, species with greater degrees of sexual dimorphism are more highly polyandrous.     

Precopulation Sexual Selection in Nysius huttoni White (Heteroptera: Lygaeidae) in Relation to Morphometric Traits

Nysius huttoni White is a polygamous bug, endemic to New Zealand, and an important pest of wheat and brassicas. This bug has a female-biased sexual size dimorphism but relative to body length, males have longer antennae, suggesting that the allometric scales of antennal–body relationships may be highly selective in sexual selection. Body weight and most morphometric traits measured have no effect on mating success of either sex. Males significantly preferred mating with females having thicker abdomens, more mature eggs, and longer ovipositors. This result suggests that males may select their mates on the basis of immediate reproductive benefit: fertilizing more eggs and ensuring better survival of these eggs. Males with large genital structures have mating advantages over those with small ones, suggesting that precopulation sexual selection in this species act on male genital traits rather than body weight and nonsexual traits. Finally, females significantly preferred males with greater slopes for the antennal-body relationship for mating. The allometry in the male antennal length may be an indicator of male reproductive fitness.     

INEXPLICABLY FEMALE‐BIASED SEX RATIOS IN MELITTOBIA WASPS

The sex ratio behavior of parasitoid wasps in the genus Melittobia is scandalous. In contrast to the prediction of Hamilton's local mate competition theory, and the behavior of numerous other species, their extremely female‐biased sex ratios (1–5% males) change little in response to the number of females that lay eggs on a patch. We examined the mating structure and fitness consequences of adjusting the sex ratio in M. australica and found that (1) the rate of inbreeding did not differ from that expected with random mating within each patch; (2) the fitness of females that produced less female‐biased sex ratios (10 or 20% males) was greater than that of females who produced the sex ratio normally observed in M. australica. These results suggest that neither assortative mating nor asymmetrical competition between males can explain the extreme sex ratios. More generally, the finding that the sex ratios produced by females led to a decrease in their fitness suggests that the existing theory fails to capture a key aspect of the natural history of Melittobia, and emphasizes the importance of examining the fitness consequences of different sex ratio strategies, not only whether observed sex ratios correlate with theoretical predictions.     

Sex differences in telomeres and lifespan in Soay sheep: From the beginning to the end

There is tremendous diversity in ageing rates and lifespan not only among taxa but within species, and particularly between the sexes. Women often live longer than men, and considerable research on this topic has revealed some of the potential biological, psychological and cultural causes of sex differences in human ageing and lifespan. However, sex differences in lifespan are widespread in nonhuman animals suggesting biology plays a prominent role in variation in ageing and lifespan. Recently, evolutionary biologists have borrowed techniques from biomedicine to identify whether similar mechanisms causing or contributing to variation in ageing and lifespan in humans and laboratory animals also operate in wild animals. Telomeres are repetitive noncoding DNA sequences capping the ends of chromosomes that are important for chromosomal stability but that can shorten during normal cell division and exposure to stress. Telomere shortening is hypothesized to directly contribute to the ageing process as once telomeres shorten to some length, the cells stop dividing and die. Men tend to have shorter telomeres and faster rates of telomere attrition with age than women, suggesting one possible biological cause of sex differences in lifespan. In this issue of Molecular Ecology, Watson et al. ( 2017 ) show that telomere lengths in wild Soay sheep are similar between females and males near the beginning of life but quickly diverge with age because males but not females showed reduced telomere lengths at older ages. The authors further show that some of the observed sex difference in telomere lengths in old age may be due to male investment in horn growth earlier in life, suggesting that sexually dimorphic allocation to traits involved in sexual selection might underlie sex differences in telomere attrition. This study provides a rare example of how biological mechanisms potentially contributing to sex differences in lifespan in humans may also operate in free‐living animals. However, future studies using a longitudinal approach are necessary to confirm these observations and identify the ultimate and proximate causes of any sex differences in telomere lengths. Collaborations between evolutionary biologists and gerontologists are especially needed to identify whether telomere lengths have a causal role in ageing, particularly in natural conditions, and whether this directly contributes to sex differences in lifespan.     

The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence

1. In species such as quasi-gregarious egg parasitoids, which exploit defendable patches, the fitness pay-off from superparasitism is an important factor in considering the evolution of patch defence and optimal patch defence strategies.
2. When oviposition in a previously parasitized host has a non-zero fitness pay-off, competing parasitoids are not only able to diminish the future value of a patch to other females by depleting unparasitized hosts, but also devalue the previous investment of other females in the patch by superparasitizing.
3. In Trissolcus basalis , an egg parasitoid of pentatomid bugs, the fitness pay-off from superparasitism is higher than 0.5 when the time interval between ovipositions is less than 3 h, suggesting that defending a previous investment will be an important component of patch defence behaviour.
4. The data suggest a mechanism for the high early pay-off, which involves the superparasitizing female adjusting the sex ratio of its offspring in favour of males. Males develop more quickly than females and thus may have a competitive advantage.     

Sex-Specific Territorial Behaviour in the Banggai Cardinalfish, Pterapogon kaunderni

In a field experiment, we studied how levels of aggression in males and females in established pairs of the Banggai cardinalfish were influenced by the sex of an experimentally introduced individual larger and more attractive than its resident counterpart. Contrary to previous studies on other cardinalfish species, and contrary to expectations in a sex role reversed species, the male was the main aggressor towards an intruder. Moreover, residents were more aggressive towards an intruder of the same sex as themselves. Furthermore, even though females often courted introduced, larger males, no intruder managed to take over the partnership of any resident. We suggest that our findings imply relatively equal sex roles in the Banggai cardinalfish and we discuss the evolution of sex specific territory defence and its significance in the Banggai cardinalfish as well as the implications of such behaviour in the interpretations of sex roles in general.     

Adaptive significance of environmental sex determination in an amphipod

Environmental sex determination (ESD) permits adaptive sex choice under patchy environmental conditions, where the environment affects sex-specific fitness and where offspring can predict their likely adult status by monitoring an appropriate environmental cue. For Gammarus duebeni, an amphipod with ESD, it has been proposed that this flexible sex determination system is adaptive because males gain more from large size. Under ESD, young which are born earlier in the season become mostly males and, experiencing longer to grow, are therefore larger at breeding than females which are born later in the season. In order to test the hypothesis that ESD is adaptive for this species we investigated the relationship between size and fitness for both males and females, in a population of G. duebeni known to have ESD. We measured size related pairing success and fecundity, and used these two measures to calculate the relative fitness gains achieved through an increase in size for either sex. The fitness of both males and females increased with size, but males gained more from an increase in size than did females, throughout the breeding season. The data support the adaptive explanation for the evolution and maintenance of ESD in this species.     

Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect

1.?When parasitized, both vertebrates and invertebrates can enhance the immune defence of their offspring, although this transfer of immunity is achieved by different mechanisms. In some insects, immune-challenged males can also initiate trans-generational immune priming (TGIP), but its expressions appear qualitatively different from the one induced by females similarly challenged. 2.?The existence of male TGIP challenges the traditional view of the parental investment theory, which predicts that females should invest more into their progeny than males. However, sexual dimorphism in life-history strategies and the potential costs associated with TGIP may nevertheless lead to dissymmetric investment between males and females into the immune protection of the offspring. 3.?Using the yellow mealworm beetle, Tenebrio molitor, we show that after parental exposure to a bacterial-like infection, maternal and paternal TGIP are associated with the enhancement of different immune effectors and different fitness costs in the offspring. While all the offspring produced by challenged mothers had enhanced immune defence, only those from early reproductive episodes were immune primed by challenged fathers. 4.?Despite the fact that males and females may share a common interest in providing their offspring with an immune protection from the current pathogenic threat, they seem to have evolved different strategies concerning this investment.