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.     

Sexually dimorphic effect of mating on the melanotic encapsulation response in the harem‐defending Wellington tree weta,Hemideina crassidens (Orthoptera: Tettigonioidea: Anostostomatidae)

Reproductive activities are generally costly to immune responsiveness because limited resources required by reproduction are diverted away from immunity (and vice versa). Reproduction, however, is not expected to affect the immune response in males and females similarly as mating is expected to negatively affect male immunity more so than female immunity. Here, I test the phenotypic plasticity hypothesis in the Wellington tree weta (Hemideina crassidens), a sexually dimorphic orthopteran insect that is endemic to New Zealand. My laboratory experiment showed that although males had higher rates of melanotic encapsulation than females, contrary to prediction, females were the only sex significantly affected by mating and the effect was positive. In addition to immunity differing between the sexes, immune function can differ intrasexually, particularly when males are polymorphic and different investment strategies are used to maximize fitness. Male H. crassidens exhibit alternative mating strategies that are represented by three different morphotypes. I therefore explored whether the morphs differed in their melanotic encapsulation response and whether mating affected the morphs differently. I found no difference among morphs or an effect of mating on male immune response.     

An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks

The immunocompetence handicap hypothesis (ICHH) provides a functional explanation for how sexual ornaments can provide honest signals of male quality. A key aspect of this hypothesis is that testosterone (T) has a bimodal effect: a higher T level enhances the expression of ornaments (increasing mating success and, ultimately, fitness); however, at the same time, it suppresses immune function. Tests of the latter assumption, which have focused mainly on aspects of adaptive immunity in birds, led to equivocal results. We performed a hormone-implant experiment in male three-spined sticklebacks (Gasterosteus aculeatus) to test the key assumptions of the ICHH in a fish, where the dominant circulating androgen is 11-ketotestosterone (11kT) rather than T. Males were implanted with 11-ketoandrostenedione, which is a natural precursor of 11kT. Each individual's circulating 11kT level, ornamentation, and immunocompetence were measured 2 weeks later. In addition, we quantified oxidative tissue damage because the ICHH has been hypothesized to work via oxidative stress. We found that the males' 11kT levels correlated positively with ornamentation but negatively with immunocompetence, in particular, measures of innate immunity. Moreover, there was a trend for fish with high 11kT levels to suffer more from oxidative stress. Thus, our data provide support for the ICHH.     

Maintenance of a female-limited polymorphism in Ischnura ramburi (Zygoptera: Coenagrionidae)

Colour polymorphisms can be maintained in a population if all morphs have equal fitness on average, if fitness is frequency dependent or if fitness functions cross for some environmental or social variable. We studied female-limited colour polymorphism in the Rambur's forktail damselfly, Ischnura ramburi, in which one female morph looks like the male. The most commonly cited hypotheses to explain this polymorphism involve an advantage to andromorphs of avoiding costly matings through male mimicry. An alternative hypothesis argues that males learn the most common morph and that the polymorphism is maintained by a rare-morph advantage of mating avoidance, irrespective of male mimicry. We tested predictions of the male mimicry hypothesis, learned mate recognition hypothesis (LMR) and two new hypotheses. We used censuses and a mark-resight study to estimate density, sex ratio, morph frequency and mating frequencies. We observed interactions to test for male mimicry and female competition and to evaluate the frequency of mating attempts. Andromorphs were less likely than gynomorphs to receive mating attempts in encounters with males, but did not mate less frequently, or attack males or interrupt oviposition by other females more frequently. Contrary to the LMR hypothesis, the rarer morph was more likely to receive mating attempts. Andromorph frequency was greater in older females than in younger females, suggesting higher mortality or dispersal of gynomorphs. Our results support a modification of the male mimicry hypothesis, the signal detection hypothesis. Together with past studies, our results suggest that the female morphs may be alternative mating avoidance strategies.     

An experimental investigation into status-dependent male dimorphism in the European earwig, Forficula auricularia

Discrete alternative reproductive phenotypes are probably often due to individuals adopting alternative tactics with unequal fitnesses in conditional strategies with status-dependent selection. One tactic is believed to be favoured below a status switch point and another tactic above it, owing to different fitness functions of the tactics. Males of the European earwig are dimorphic. Macrolabic males are large (high status) and have long forceps, and brachylabic males are small (low status) with short forceps. I tested whether fitness functions, measured as mating success, of the two morphs differed with regard to forceps length and body weight. Macrolabic males with longer forceps than a competing male had higher mating success but brachylabic males benefited by being heavier than their competitor. Thus, different selection regimes were acting on the two morphs, suggesting that their fitness functions differed in relation to status. These observations and those of previous studies, showing that morph expression is environmentally determined and is associated with body size and that the morphs have unequal fitness, provide support for the hypothesis that male dimorphism in this species is a conditional strategy that has evolved under status-dependent selection. The differential investment in forceps growth that characterizes the morphs was manifested in a steeper allometric relation between forceps length and body size in macrolabic than brachylabic males. Behavioural observations showed that males of both morphs engaged in direct contests for females. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

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.     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.     

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

Empirical studies in vertebrates support the hypothesis that inbreeding reduces resistance against parasites and pathogens. However, studies in insects have not found any evidence that inbreeding compromises immune defence. Here we tested whether one generation of brother-sister mating or extreme outbreeding (mating between two populations) have an effect on innate immunity and life history traits in the autumnal moth, Epirrita autumnata. We show that the effect of inbreeding on immune response differed between the sexes: whereas in females, inbreeding significantly reduced encapsulation response against nylon monofilament ability, it did not have a significant effect on male immune response. There were also differences in the correlation of the immune response with other traits: in females increased immune response was positively correlated with large size, whereas in males immune response increased with a reduction in development time. Immune response differed significantly among families in males but not in females, both for the inbreeding and extreme outbreeding experiments. In conjunction with the observed immune responses to inbreeding, these data suggest that in males genetic variation for immune response is largely additive or non-directional with respect to dominance, whereas in females variation is much reduced and consists of directional dominance variance. Further, we show that encapsulation response against nylon monofilament is associated with the resistance against real pathogens suggesting that this widely used method to measure the strength of immune defence in insects is also a biologically relevant method.     

Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.     

An empirical test of the bet‐hedging polyandry hypothesis: Female red flour beetles avoid extinction via multiple mating

Bet‐hedging via polyandry (spreading the extinction risk of the female''s lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when “unsuitable” males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet‐hedging strategy, empirical tests are scarce. In the present study, we tested the bet‐hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet‐hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet‐hedging polyandry hypothesis.     

No genetic correlation between the sexes in mating frequency in the bean beetle, Callosobruchus chinensis

Female multiple mating, which is common in animals, may have evolved not in response to fitness advantages to females but as a genetic corollary to selection on males to mate frequently. This nonadaptive hypothesis assumes a genetic correlation between females and males in mating frequency, which has received a few empirical investigations. We tested this hypothesis by observing the correlated response in male mating frequency in the adzuki bean beetle, Callosobruchus chinensis to artificial selection on female propensity to remate. Compared to control females, females from lines selected for increased or decreased female propensity to remate had, respectively, higher or lower mating frequency measured by the number of mating within a given period. This indicates that female receptivity to remating is genetically correlated with female mating frequency, and thus the artificial selection for female propensity to remate influenced female mating frequency. In contrast, males from the selected lines that diverged in female mating frequency did not vary significantly in their mating frequency. These results indicate that there is no genetic correlation between the sexes in mating frequency in C. chinensis. This study shows that the reason why females in C. chinensis remate despite suffering fitness costs cannot be explained by indirect selection resulting from selection on males to mate multiple times.     

Age-specific mating strategies and reproductive senescence

While males gain obvious direct advantages from multiple mating, the reproductive capacity of females is more constrained. The reason why polyandry evolved in females is therefore open to many conjectures. One hypothesis postulates that females gain indirect benefits by increasing the probability of siring young from high quality males. To explore this hypothesis, we used the natural variation of the reproductive value that males and females undergo through age. The age-related variation of phenotypic performance might then induce variations in mating strategies in males and females. Using the common lizard (Lacerta vivipara) as our model system, we showed that reproductive immaturity and senescence created variability in both male and female reproductive success (including survival of offspring). Consistent with theory, males at their best-performing phenotype adopted a polygynous strategy. These males were of an intermediate age and they produced offspring of higher viability than younger and older males. In contrast, females at their best performing phenotype, also of an intermediate age, were less polyandrous than other less-performing females. Middle-aged females tended to mate with males of an intermediate age and produced litters with higher viability independently from their reproductive strategy. Males of an intermediate age enhanced their fitness by additional matings with young or old females. Young and old females increased their fitness by being more polyandrous. Polyandry therefore appears as means to seek for good males. A positive correlation between males and their partners' fitness disagree with the idea that polyandry is the result of a sexual conflict in this species.     

Chance, time allocation, and the evolution of adaptively flexible sex role behavior

An alternative to classic sexual selection hypotheses for sex differentiated pre-mating behavior is that time available for mating-as individuals experience it-along with fitness differences among alternative potential mates, induces choosy versus indiscriminate mating behavior. This alternative hypothesis says that selection has acted so that all individuals flexibly express fitness-enhancing choosy, indiscriminate, and competitive mating behavior, induced by time-varying life histories, environmental and social cues. Key predictions of DYNAMATE, the formal model of adaptively flexible sex role behavior of individuals of both sexes within dynamically changing populations, include: (1) All individuals regardless of sex assess likely fitness outcomes from mating with alternative potential mates before expressing choosy or indiscriminate behavior. (2) Males and females express adaptively flexible, choosy and indiscriminate behavior so that individuals may change their behavior-from moment to moment-to fit dynamically changing circumstances. (3) Indiscriminate behavior of males and (4) choosy behavior of females would often be maladaptive even in species with greater female than male parental investment, when females have longer latencies to receptivity to re-mating than males, and when the relative reproductive rate of males is greater than in females. (5) Whether or not females show choosy behavior will not affect whether or not males exhibit choosy or indiscriminate behavior, and vice versa. (6) When other model parameters are equal, the proportion of individuals of a given sex expressing choosy or indiscriminate mating behavior is a function of the distribution of fitness ratios (a distribution of all fitness differences that would be conferred on an individual by mating with any two sequentially or simultaneously encountered alternative potential mates). (7) Whether same-sex individuals behaviorally compete is a function of the fitness that would be conferred if the strategist won access to a potential mate, but not a function of relative reproductive rate or its proxy, the operational sex ratio. We call for re-evaluation of sex differences in choosy, indiscriminate, and competitive behavior under strong experimental controls that level the ecological playing fields of males and females, i.e., under experimental conditions informing the mechanisms of phenotypic expression. We end with comments on the classic question of questions: why are the sexes as they are?     

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.     

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.     

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

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

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

The Harmonic Convergence of Fathers Predicts the Mating Success of Sons in Aedes aegypti

During courtship males often communicate information about their fitness to females. The matching of harmonic components of flight tone in male-female pairs of flying mosquitoes, or harmonic convergence, was recently described. This behaviour occurs prior to mating and has been suggested to function in mate selection. We investigated the hypothesis that harmonic convergence is a component of mosquito courtship. A key prediction of this hypothesis is that harmonic convergence should provide information to potential mates about fitness benefits. We measured the effect of harmonic convergence behaviour on the direct and indirect benefits obtained by females. We found that the sons of pairs that converged at harmonic frequencies prior to mating had increased mating success and that these offspring were themselves more likely to converge prior to mating. These results suggest that males may be able to signal information about their genetic quality to females prior to mating and that this signal may be heritable. These findings are important for our understanding of mosquito behaviour and have applications in the control of mosquito-borne disease. This study also contributes to the study of male-female interactions and signal coevolution.     

Sexual selection and immune function in Drosophila melanogaster

The evolution of immune function depends not only on variation in genes contributing directly to the immune response, but also on genetic variation in other traits indirectly affecting immunocompetence. In particular, sexual selection is predicted to trade-off with immunocompetence because the extra investment of resources needed to increase sexual competitiveness reduces investment in immune function. Additional possible immunological consequences of intensifying sexual selection include an exaggeration of immunological sexual dimorphism, and the reduction of condition-dependent immunological costs due to selection of 'good genes' (the immunocompetence handicap hypothesis, ICHH). We tested for these evolutionary possibilities by increasing sexual selection in laboratory populations of Drosophila melanogaster for 58 generations by reestablishing a male-biased sex ratio at the start of each generation. Sexually selected flies were larger, took longer to develop, and the males were more sexually competitive than males from control (equal sex ratio) lines. We found support for the trade-off hypothesis: sexually selected males were found to have reduced immune function compared to control males. However, we found no evidence that sexual selection promoted immunological sexual dimorphism because females showed a similar reduction in immune function. We found no evidence of evolutionary changes in the condition-dependent expression of immunocompetence contrary to the expectations of the ICHH. Lastly, we compared males from the unselected base population that were either successful (IS) or unsuccessful (IU) in a competitive mating experiment. IS males showed reduced immune function relative to IU males, suggesting that patterns of phenotypic correlation largely mirror patterns of genetic correlation revealed by the selection experiment. Our results suggest increased disease susceptibility could be an important cost limiting increases in sexual competitiveness in populations experiencing intense sexual selection. Such costs may be particularly important given the high intersex correlation, because this represents an apparent genetic conflict, preventing males from reaching their sexually selected optimum.     

Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster

New theoretical work on kin selection and inclusive fitness benefits predicts that individuals will sometimes choose close or intermediate relatives as mates to maximize their fitness. However, empirical examples supporting such predictions are rare. In this study, we look for such evidence in a natural population of Drosophila melanogaster. We compared mating and nonmating individuals to test whether mating was nonrandom with respect to relatedness. Consistent with optimal inbreeding, males were more closely related to their mate than to randomly sampled females. However, all individuals collected mating showed higher relatedness and males were not significantly more related to their mate than to other mating females. We also found a negative relationship between relatedness and fecundity. Our results are consistent with the hypothesis that inclusive fitness benefits may drive inbreeding tolerance despite direct costs to fitness; however, an experimental approach is needed to investigate the link between mate preference and relatedness.