Sexual signaling and immune function in the black field cricket Teleogryllus commodus

The immunocompetence handicap hypothesis predicts that male sexual trait expression should be positively correlated with immunocompetence. Here we investigate if immune function in the cricket, Teleogryllus commodus, is related to specific individual components of male sexual signals, as well as to certain multivariate combinations of these components that females most strongly prefer. Male T. commodus produce both advertisement and courtship calls prior to mating. We measured fine-scale structural parameters of both call types and also recorded nightly advertisement calling effort. We then measured two standard indices of immune function: lysozyme-like activity of the haemolymph and haemocyte counts. We found a weak, positive relationship between advertisement calling effort and lysozyme-like activity. There was, however, little evidence that individual structural call components or the net multivariate attractiveness of either call type signalled immune function. The relationships between immunity and sexual signaling did not differ between inbred and outbred males. Our data suggest that it is unlikely that females assess overall male immune function using male calls.     

Sexual advertisement and immune function in an arachnid species (Lycosidae)

A simple version of the immunocompetence handicap hypothesizesthat through condition-dependence, the size of the sexual traitmay be positively related to immune function at the populationlevel. In the present study, we investigated the relationshipbetween sexual advertisement and immune function in a naturalpopulation of male wolf spiders, Hygrolycosa rubrofasciata (Araneae:Lycosidae). Males of H. rubrofasciata have a costly and condition-dependentacoustic signal, courtship drumming. In the mating season, malesdrum against dry leaves while wandering around the habitat searchingfor receptive females. Males increase their mating success byincreasing their drumming rate and mobility. We used drummingrate and mobility measured without female proximity as estimatesof sexual advertisement. As estimates of male immune function,we used encapsulation rate and lytic activity. Encapsulationrate is a common challenging technique, which measures immuneresponse against multicellular parasites. Lytic activity isa monitoring technique, which measures immune response againstpathogens. Our results show that males with higher drummingrate had higher encapsulation rate. This suggests that femalesmight use drumming rate as a signal for choosing males withgood immunocompetence. Moreover, our results show that maleswith higher mobility had higher lytic activity. As females aremore likely to encounter those males that have higher mobility,this might also select males with better immune function. Ourresults suggest that the immunocompetence handicap might workalso among spiders, although we could not assess the causalityof the relationship between sexual selection and immune functionin this correlational study.     

A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata

The field of ecological immunology is ultimately seeking to address the question ‘Why is there variation in immune function?’ Here, we provide experimental evidence that costs of ubiquitous sexual signals are a significant source of variation in immune function. In the mating season, males of the wolf spider Hygrolycosa rubrofasciata drum against dry leaves while wandering around the habitat searching for receptive females. According to a previous study, the male metabolic rate during the drumming increases 22‐fold compared to the resting metabolic rate. In the present study, we examined whether investment in costly courtship drumming decreases male immune function in a wild population of H. rubrofasciata. We induced males to increase their drumming rate by introducing females in proximity. As estimates of male immune function, we used lytic activity and encapsulation rate. Lytic activity estimates the concentration of antimicrobial peptides in haemolymph, which have been shown to play an important role in defence against bacteria, viruses and fungi. Encapsulation is an important defence mechanism against nematodes and insect parasitoids, but it also plays a role in defence against viruses. Our results show that males with nonarbitrarily increased investment in drumming rate had considerably lower lytic activities than control males. Also, there was a tendency for males with nonarbitrarily increased investment in drumming rate to have lower encapsulation rates than control males. This study provides experimental evidence for the first time, to our knowledge, that there are direct immunological costs of sexual signalling in natural populations. Therefore, immunological costs of sexual signals may provide significant phenotypic variation to parasite‐mediated sexual selection.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

Mating with large males decreases the immune defence of females in Drosophila melanogaster

Mating has been widely reported to be a costly event for females. Studies indicate that female cost of mating in terms of fecundity and survivorship can be affected by their mates, leading to antagonistic coevolution between the sexes. However, as of now, there is no evidence that the female cost of mating in terms of immune defence is affected by their mates. We assess the effect of different sized males on antibacterial immune defence and reproductive fitness of their mates. We used a large outbred population of Drososphila melanogaster as the host and Serratia marcescens as the pathogen. We generated three different male phenotypes: small, medium and large, by manipulating larval densities. Compared to females mating with small males, those mating with large males had higher bacterial loads and lower fecundity. There was no significant effect of male phenotype on the fraction of females mated or copulation duration (an indicator of ejaculate investment). Thus, our study is the first clear demonstration that male phenotype can affect the cost of mating to females in terms of their antibacterial immune defence. Mating with large males imposes an additional cost of mating to females in terms of reduced immune defence. The observed results are very likely due to qualitative/quantitative differences in the ejaculates of the three different types of males. If the phenotypic variation that we observed in males in our study is mirrored by genetic variation, then, it can potentially lead to antagonistic coevolution of the sexes over immune defence.     

Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius

One of the most common life history trade-offs in animals is the reduction in survivorship with increasing reproductive effort. Despite the prevalence of this pattern, its underlying physiological mechanisms are not well understood. Here we test the hypothesis that immune suppression mediates this phenotypic trade-off by manipulating reproductive effort and measuring immune function and mortality rates in the striped ground cricket, Allonemobius socius. Because A. socius males provide females with a hemolymph-based nuptial gift during copulation, and many structural components of immunity reside in the hemolymph, we also predicted that sexual selection may differentially affect how disease resistance evolves in males and females. We found that an increased mating effort resulted in a reduced immune ability, coupled with an increased rate in age-specific mortality for both sexes. Thus, immune suppression appears to be a link between reproductive effort and cost in this system. In addition, males and females appeared to differentially invest in several aspects of immunity prior to mating, with males exhibiting a higher concentration of circulating hemocytes and a superior bacterial defense capability. This pattern may be the result of previously established positive selection on gift size due to its affect on female fecundity. In short, female choice for larger gifts may lead to a sexually dimorphic immune ability.     

Different Reproductive Tactics in House Sparrows Signalled by Badge Size: Is There a Benefit to Being Average?

Sexual selection models usually predict directional selection for ornamental traits because of intra‐ as well as inter‐sexual selection. Animals frequently face reproductive trade‐offs, such as between mating and parental effort. Provided that both are essential and have opposite effects on ornament expression, we may however not necessarily expect directional selection for ornament size. The house sparrow is an ideal species to study such a trade‐off, as the size of the male ornament, the black throat badge, seems to be inversely related to mating and parental effort. It has been suggested that large‐badged males invest more in female attraction and territory defence, while small‐badged males may invest more in parental care. In a nest‐box study, we show that females started to breed earliest and produced the largest clutches when mated to males with average‐sized badges that invested in paternal care more than other males. These results are discussed in view of inter‐ as well intra‐sexual selection. Overall, average‐badged males experienced the highest hatching failures, their chicks were in the poorest physical condition and they did not fledge more chicks than other males. It is therefore unlikely that the mating advantages that we observed could by themselves lead to stabilizing selection for badge size. Our results rather suggest that badge size in male house sparrows signals different reproductive tactics, which are adapted flexibly according to their physical condition and socio‐ecological situations.     

Enhanced male coloration after immune challenge increases reproductive potential

In many animal species, females select a mate on the basis of the expression of secondary sexual traits. A prevalent theory suggests that male ornaments are reliable indicators of immunocompetence, because the cost of immune function prevents cheating. However, sexual signalling is a component of male reproductive effort, and an immune challenge may also alter his perceived future prospects and hence signalling effort. In this study, blue‐footed booby males (Sula nebouxii) were inoculated with a diphtheria–tetanus vaccine during courtship to investigate the consequences of mounting an immune response on signalling effort. We found that, after this immune challenge, on average, males increased their signalling effort but lost more body mass compared with control males. Importantly, vaccination affected the partner's reproductive decisions: compared with control females, females paired with vaccinated males laid eggs earlier and increased clutch volume in pairs that laid early. Overall, our results suggest that blue‐footed booby males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Increased signalling effort by infected individuals may contrast the idea of sexual ornaments as signals of infection status.     

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.     

INBREEDING AND ADVERTISEMENT CALLING IN THE CRICKET TELEOGRYLLUS COMMODUS: LABORATORY AND FIELD EXPERIMENTS

If sexually selected traits reveal a male's heterozygosity or condition to females, then such traits should exhibit declines with inbreeding. We tested this by examining the effect of inbreeding on advertisement calling in male crickets Teleogryllus commodus. We investigated the effect of one generation of full‐sibling mating on calling effort and fine‐scale call structure. Inbreeding reduced calling effort but had no effect on call structure. We then compared the attractiveness of inbred and outbred calls in the field by monitoring how many wild females were attracted to each call type. From the field data, we conducted a selection analysis to identify the major axes of linear and nonlinear multivariate sexual selection on call structure. A comparison of multivariate attractiveness of inbred and outbred calls along each major axis of selection revealed no difference in attractiveness. Our results suggest that inbred male calls have a fine‐scale structure that is no less attractive to females than that of outbred calls. However, because inbred males call less often, and female T. commodus prefer males with a higher calling effort, inbred males will suffer reductions in mating success. Females who base mate choice on call rate are therefore using a signal correlated with male heterozygosity and/or condition.     

Male Head Secretion Triggers Copulation in the Dwarf Spider Diplocephalus permixtus

The term nuptial feeding is applied for any possible form of transfer of substances during the course of mating. However, the underlying functions can range from increased coupling efficiency or increased male survival to various levels of sexual selection. Males of many dwarf spider species (Erigoninae: Linyphiidae; Araneae) produce secretions from conspicuous grooves or elevations on their prosoma that seem to play a role during the mating episode. We asked if these structures represent a survival strategy, a mating effort in that they function as a mate attractant or as a mechanism to secure matings or if they simply facilitate successful genital coupling. In Diplocephalus permixtus males possess a deep groove in the ocular area into which females sink their chelicerae before mating commences. Secretory glands in the area of the groove produce a substance, which is taken up by the female in the process of mating. We experimentally prevented females from taking up secretion by covering the head structures of one group of males and compared the behaviour with controls. We investigated effects in a single male setting as well as in a competitive two‐males setting. Under both experimental conditions the probability that copulation occurred was significantly reduced in head covered males: females bit into male head structures irrespective of male treatment but covered males did not commence pedipalp insertion despite optimal mating position. Our data suggest that in contrast to other gustatorial arthropod species investigated so far the head–mouth contact between the sexes primarily triggers the mating behaviour of the male and not that of the female. Clearly, the secretion does not function as a mate attractant as mating position was achieved with similar probability in covered and control males. A function as a survival strategy can be excluded as well, because sexual cannibalism never occurred. Potential stimulating or manipulative effects of the secretion during copulatory and post‐copulatory phases remain to be investigated.     

Forceps size and immune function in the earwig Forficula auricularia L.

Females of many species select their mates on the basis of the size or intensity of sexual ornaments, and it has been suggested that these provide reliable signals of a male's ability to resist parasites and pathogens. European earwigs, Forficula auricularia , are sexually dimorphic in forceps shape and length. Male forceps are used as weapons in male contests for access to females, but recent findings suggest that females also choose males on the basis of their forceps length. In the present study, we tested the hypotheses that in the European earwig, F. auricularia , the size of forceps is correlated with immune function and that immune function differs between the sexes. We found that encapsulation rate was not correlated with the length of forceps in either sex, but was negatively correlated with body size. By contrast, lytic activity of the haemolymph increased with overall body size in both sexes but, in females, lytic activity increased with relative forceps length whereas, in males, it decreased with relative forceps length. After accounting for effects of body size, there was no remaining significant correlation in females but the negative correlation in males remained. Furthermore, we found that males had higher encapsulation rate and higher lytic activity than females, suggesting that males have stronger immune defence. The results of the study indicate that the size of forceps in male earwigs does not reliably reflect male immune defence.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 509–516.     

Male–male interactions and male mating success in the leafhopper Aphrodes makarovi

In mating systems based on substrate‐borne vibrations, sexual communication often involves a reciprocal exchange of species‐ and sex‐specific vibrational signals and male is searching for a stationary female. In the leafhopper Aphrodes makarovi, female reply is essential for successful location of the female and its variable duration directly affects male's costs associated with signalling and searching. We studied male and female behaviour in a trio situation (two males and one female), and our results show that male–male competition had important effects on male mating success. Females replied equally to advertisement calls emitted by the winning and losing males and mated with the first male that located them, regardless of his investment in calling effort. Males eavesdropped to male–female duet maintained by the rival, and the winners were better at exploiting female replies to the rival's advertisement calls by silently approaching the female. To interfere with the ongoing male–female duet, males also emitted masking signals overlapping the latter part of the female reply. More overlapped female replies were registered in response to the losers and masking signals most likely delay the rival in reaching the female. Our study shows that a comprehensive understanding of male mating success and female preferences in vibrational duetting systems requires also investigations in more complex settings that more realistically represent the situation in nature.     

Effects of Egg and Circulating Testosterone on Ring‐Necked Pheasant (Phasianus colchicus) Male Traits and Combat Outcome

Studies of avian species have shown that maternal effects mediated by the transfer of egg hormones can profoundly affect offspring phenotype and fitness. We previously demonstrated that the injection of a physiological amount of testosterone (T) in the eggs of ring‐necked pheasants (Phasianus colchicus) disrupted the covariation among male morphological traits at sexual maturity and positively affected male mating success. Here, we investigate whether egg T exposure affected adult male circulating T levels at the onset of the breeding season (reflecting gonadal maturation), and the relationship between circulating T and male traits. Egg T exposure did not affect pre‐mating plasma T. T levels were not associated with the expression of secondary sexual and non‐sexual traits or socio‐sexual behaviour (social rank, overall fighting ability and mating success). However, wattle brightness decreased with increasing circulating T in males hatched from T‐eggs (T‐males) but not among control males. In dyadic encounters during the peak mating period, control males with higher pre‐mating T levels had higher chances of being dominant over other control males. However, higher pre‐mating T levels did not predict success in male‐male competition in encounters involving T‐males. We suggest that the long‐term effects of egg T on male phenotype do not originate from differential gonadal maturation according to egg T treatment. Rather, prenatal androgens may have priming effects on functioning of target tissues, translating into differential phenotypic effects according to androgen exposure during embryonic development.     

Do Antlers Honestly Advertise the Phenotypic Quality of Fallow Buck (Dama dama) in a Lekking Population?

Size and symmetry of secondary sexual traits are supposed to be honest signals of male phenotypic quality in vertebrates. Antler size and symmetry, male quality and mating success have not been fully demonstrated to be correlated in cervids. Such correlations can be particularly intriguing in the case of species adopting costly mating strategies, which imply territorial defence without feeding. In these cases, body condition appears to be crucial at the onset of the rut, and large and symmetrical antlers may be borne by successful males. For these reasons, during four consecutive years, we analysed growth rate, size and symmetry of 26 fallow bucks’ antlers in relation to individual mating strategy and success in a lekking population. Territorial (T) males, which gained higher mating success in the lek, showed a faster antler growth (about 10 g/d per antler) than non‐territorial (NT) males (3.6–5.2 g/d per antler) during the velvet period, and this was likely because of optimized foraging strategies. At the onset of the rut, when antler growth was completed, T males had larger antlers than NT males. Possibly because of worsened body conditions, NT males showed a pronounced antler directional asymmetry, while T males did not. However, no direct link between antler symmetry and mating success was found, thus confirming the ambiguous role of antler asymmetry as an indicator of fitness. The faster the antler growth, the larger its final size and the higher its beholder’s mating success. Our results confirmed that, like groaning and scent marking, antler size reflects social status and dominance in male fallow deer, and therefore represents an honest advertisement of phenotypic quality.     

Male mating success and risk of predation in a wolf spider: a balance between sexual and natural selection?

1. Traits that benefit males through sexual selection are simultaneously expected to impair males by provoking costs through natural selection. If we consider the two male fitness components, mating success and viability, then we may expect that the increase in male mating success resulting from a larger trait size will be counterbalanced by an increase in viability costs.
2. We studied the benefits and costs of male mate searching and sexual signalling activity in the wolf spider Hygrolycosa rubrofasciata . In the field, males search females actively and court them by drumming dry leaves with their abdomen. Females have been shown to prefer males with high drumming rate. Male moving and especially drumming is energetically highly demanding and drumming results in significant mortality costs.
3. Our objective in this study was to determine whether male mate-searching activity or drumming activity affect male mating success and the risk of males being predated.
4. It was evident that both higher mate-searching activity and higher drumming activity benefited males by increasing their mating success. Higher mate-searching activity clearly impaired males by causing direct increase in predation risk. There was also a slight tendency that more actively drumming males had higher risk of predation and from all of the predated males 13.3% were caught directly after they had drummed. Furthermore, male drumming activity decreased drastically in the presence of the predator.
5. We conclude that in H. rubrofasciata both increased mate-searching activity and drumming activity benefit males through sexual selection, but at the same time natural selection provokes direct balancing costs on the same traits.     

Males mate indiscriminately in the tropical jumping spider Hasarius adansoni (Audouin, 1826)

Traditionally, sexual selection has been seen as a process in which choosy females select non‐choosy males. Recent studies, however, have challenged this view by showing that males can also be choosy in many species. We assessed the sexual preferences in males of the tropical jumping spider Hasarius adansoni (Audouin, 1826). We measured mating effort in males and determined how female quality influences offspring quality, quantity, and survival. We also estimated total sperm load and how much sperm was invested in a mating with a particular female. We found no evidence of male mating effort in terms of mating frequency nor sperm investment. Similarly, there was no relationship between female quality (i.e., size and condition) and offspring quality (i.e., survival and feeding performance) or quantity. We found strong evidence that the sperm invested in a particular female is a function of the amount of sperm the male had available for usage at that particular mating. The fact that males probably find females sequentially, along with the lack of relationship between female quality and offspring quality/quantity, likely explains the lack of differences in mating effort by males.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Differences in size and energy content affect the territorial status and mating success of a neotropical dragonfly

In male odonates, both size and fat content are related to territory defence and mating success. Males that are larger and have higher energy reserves win relatively more disputes for territory and attract more females. Wing colour has also been regarded as a mechanism that influences agonistic behaviour between males, as wing pigmentation might be regarded as a sign of male quality. In this study, we analysed whether a set of male physical (body size and wing colour), physiological (body fat content) and behavioural (disputes between males) characteristics were involved in the territory defence and mating behaviour of the neotropical dragonfly Zenithoptera lanei Santos, 1941 (Anisoptera: Libellulidae). Males were characterised as territorial whenever they warded‐off other males and remained in the same place within the pond for two consecutive days. In general, these territorial males were larger and had more abdominal and thoracic fat, engaged in pursuits more frequently, spent more time on sexual behaviour and female guarding, and mated more in comparison to subordinate males. By evaluating whether the percentage of wing area covered by black ink influenced male behaviour, we found that territorial males tended to act aggressively towards other males whose wings were partially painted, and sexually towards females irrespective of wing area painted. In Z. lanei, both body size and fat content play a role in defining territoriality. By subduing competitors and dominating preferred locations within high‐quality sites, these males are likely to be visited by females and engage in mating.