Seasonal trade-offs in cell-mediated immunosenescence in ruffs (Philomachus pugnax)

The immune system is an energetically expensive self-maintenance complex that, given the risks of parasitism, cannot be carelessly compromised. Life-history theory posits that trade-offs between fitness components, such as self-maintenance and reproduction, vary between genders and age classes depending on their expected residual lifetime reproductive success, and seasonally as energetic requirements change. Using ruff (Philomachus pugnax), a bird with two genetically distinct male morphs, we demonstrate here a decrease in male immunocompetence during the breeding season, greater variance in immune response among males than females, immunosenescence in both sexes and male morphs, and a seasonal shift in the age range required to detect senescence. Using a phytohaemagglutinin delayed hypersensitivity assay, we assessed cell-mediated immunity (CMI) of males of typical breeding age during the breeding and nonbreeding seasons, and of a larger sample that included females and birds of a greater age range during the non-breeding period. CMI was higher for breeding-aged males in May than in November, but the increase was not related to age or male morph. In November, mean CMI did not differ between the sexes, but the variance was higher for males than for females, and there were no differences in mean or variance between the two male morphs. For both sexes and male morphs, CMI was lower for young birds than for birds of typical breeding ages, and it declined again for older birds. In males, senescence was detected in the non-breeding season only when very old birds were included. These results, generally consistent with expectations from life-history theory, indicate that the immune system can be involved in multifarious trade-offs within a yearly cycle and along an individual's lifetime, and that specific predictions about means and variances in immune response should be considered in future immunoecological research.     

Bill colour and immunocompetence in the European blackbird

The level of expression of secondary sexual characters has been suggested to signal male ability to resist parasitic infestations. To test this idea, several studies have examined the link between sexual signals and immunocompetence in birds. However, most of them have used only a single aspect of immune response to evaluate immunocompetence. We investigated the relation between bill colour and immunocompetence in captive male European blackbirds, Turdus merula, during the breeding season by assessing both cell-mediated and humoral components of the immune system. The blackbird is a sexually dimorphic species with bill colour varying from yellow to orange in males. Humoral immunity was assessed by measuring both primary and secondary responses to sheep red blood cell inoculation. Cell-mediated immunity was estimated with a delayed cutaneous hypersensitivity response to an injection of a mitogen (phytohaemagglutinin). No relation was found between male bill colour and the primary humoral response. However, males with orange bills showed a lower secondary humoral response but a higher cell-mediated immune response than males with yellow bills. Thus, the relation between immunocompetence and a secondary sexual trait may differ markedly depending on which component of the immune system is under consideration. We discuss our results in relation to mechanisms involved in sexual selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Spawning colouration,parasites and habitat selection in Salvelinus alpinus: initiating speciation by sexual selection?

The relationship between parasite infection and breeding ornamentation in an Arctic charr Salvelinus alpinus population was examined. Interrelationships between the intensities of parasites with different dietary transmission routes suggested that hosts were segregated by habitat and diet preferences. That is, intensities of parasites transmitted through intermediate hosts that share habitat were, in both sexes, positively interrelated. Negative interrelationships in the intensities of parasites transmitted through different hosts were found only in females. The intensity of breeding colouration was positively correlated with intensities of amphipod‐transmitted parasites in both sexes. Intensities of parasites transmitted through copepods showed no relationship to morphological or ornamental characters. Seen in the context of morphology and ornaments of previously described sympatric populations of Arctic charr, these relationships suggested that individual variation in niche background may provide a source for the initial variation in morphology and secondary sexual traits leading to sympatric speciation through sexual selection.     

Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow

We analysed the morphology of nestling barn swallows (Hirundo rustica) in relation to their sex, and laying and hatching order. In addition, we studied sex-allocation in relation to parentage, parental age and expression of a secondary sexual character of fathers. Molecular sexing was conducted using the sex chromosome-linked avian CHD1 gene. Sex of the offspring was not associated with laying or hatching order. None of nine morphological, serological and immunological variables varied in relation to offspring sex. Sexual dimorphism did not vary in relation to parental age and expression of a paternal secondary sexual character. The proportion of sons declined with brood size. Individual males and females had a similar proportion of sons during consecutive breeding years. The proportion of sons of individual females declined with age, but increased with the expression of a secondary sexual character of their current mate. The generalized lack of variation in sexual dimorphism among nestlings may suggest that barn swallows do not differentially invest in sons vs. daughters. Alternatively, male offspring may require different parental effort compared to their female siblings in order to attain the same morphological state. The lack of variation in offspring sexual dimorphism with paternal ornamentation suggests no adjustment of overall parental effort in relation to reproductive value of the two sexes. However, male-biased sex ratio among offspring of highly ornamented males may represent an adaptive sex-allocation strategy because the expression of male ornaments is heritable and highly ornamented males are at a sexual selection advantage.     

Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis

The immunocompetence hypothesis predicts that testosterone (T)enhances the expression of male secondary sexual characterswhile exerting a suppressive effect on the immune system therebyexposing hosts to higher intensities of parasite infestations.In a natural population of barn swallow (Hirundo rustica) males,the intensity of infestation by some ectoparasites was negativelycorrelated with tail length and was positively correlated withimmunoglobulin levels, but no clear relationship was observedbetween immune responses (leukocyte counts, immunoglobulins)and tail length. Males implanted with T had higher intensitiesof parasite infestations at the time of recapture than controlmales, and T-implanted males experienced an increase in countsof eosinophils. In T-implanted males, immunoglobulin levelsinitially decreased and then increased as time from implantationelapsed. Among T-implanted males, those with longer tails hada smaller increase in eosinophil counts, tended to experiencea smaller increase of parasite infestations, and were more likelyto survive until the following breeding season than those withshorter tails. The relationships between parasite burden, immunesystem, and exaggeration of tail length in the natural populationof males are consistent with some aspects of the immunocompetencehandicap hypothesis. The results from the manipulation of Tplasma levels are also partly consistent with the hypothesis,since T-implantation resulted in higher levels of parasite infestations,but contradict the assumption of an obligatory immunosuppressiveeffect of T. Higher activation of the immune system of T-implantedmales indicate that high T plasma levels imposed a two-foldcost because of the effects on parasites and the immune responseto parasites, and this suggests that the effect of T on parasitesmight not be mediated by the immune system of the host. Theresults of the manipulation of T plasma levels support the handicapversion of the immunocompetence hypothesis since high quality,long-tailed males paid less in terms of activation of the immunesystem, change in parasite infestations, and chances of survivalthan low-quality, short-tailed males.     

A test of the Darwin–Fisher theory for the evolution of male secondary sexual traits in monogamous birds

The Darwin–Fisher theory proposes that the presence of male secondary sexual traits in monogamous birds is selected for by early season breeding of females that are in good condition. These early breeding females have high fecundity because of their good condition, and they select mates based on secondary sex traits. We tested whether this hypothesis may be responsible for the presence of male sexual ornaments in the great frigatebird, a socially and genetically monogamous seabird. Consistent with the Darwin–Fisher theory, we found that reproductive success declined over the season. However, males with more exaggerated ornaments were not chosen as mates earlier in the season than males with less exaggerated ornaments, and selection gradients on these ornaments were not significantly different from zero.     

Immunological development in nestling American kestrels Falco sparverius: post-hatching ontogeny of the antibody response

Avian research involving examination of immune function or testing of immunocompetence in wild birds has been based upon information on Galliforms, (chicken and quail) even though they are precocial, whereas most wild species with which ecologists, biologists and toxicologists work are altricial; blind, naked and completely dependent at hatching. Here we begin to address this gap in knowledge, offering insight into the early, post-hatching, humoral immune response in an altricial bird, the American kestrel (Falco sparverius). Over two breeding seasons, nestling kestrels were immunized with a non-pathogenic antigen, dinitrophenol keyhole limpet hemocyanin (DNP-KLH), between 3 and 9 days post-hatching and boostered 6 days later. Background levels, primary and secondary immune responses were measured using an enzyme linked immunosorbent assay. The specificity of our laboratory produced rabbit, anti-kestrel antibody was determined using a double immunodiffusion assay. Results showed the rabbit antiserum to have specific anti-kestrel IgG activity. Birds as young as three days old could successfully mount an antibody response, the magnitude of which increased with age at first vaccination. Early immunization did not compromise growth rate, nor did it affect the maximum secondary response. Comparatively, adult kestrels immunized during the same season and following the same protocol, had antibody levels four times higher than those of the nestlings.     

Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Sexual dimorphism in immunocompetence: what does life-history theory predict?

Sexual dimorphism in immunocompetence, usually in the directionof inferior male immunocompetence, has historically been explainedas the result of proximate physiological mechanisms such asthe immunosuppressive effects of the male hormone testosterone.More recently, it has been argued that this pattern is bestunderstood as a result of resource-based trade-offs betweenmale mating effort and immune defense, a trade-off that femalesdo not make. The central prediction of this hypothesis is thatas the strength of sexual selection on males increases, themagnitude of the sex differences in immunocompetence will increase.Two implicit assumptions of this argument are that 1) longevityis of more importance for female than for male fitness and 2)that the primary benefit of immunocompetence is increased longevity.However, both of these assumptions may not be as broadly applicableas has been argued. We have modeled the optimal allocation toimmunocompetence for males and females without making theseassumptions. We find that the optimal allocation to immune defensefor males decreases as the strength of sexual selection increases,as predicted. However, males may still invest more, relativeto females, into immunocompetence if the impact of parasiteson condition differs for the sexes and/or if the relationshipbetween condition and reproduction differs for the sexes. Weargue that these previously overlooked assumptions may be criticalfor predicting sex-specific patterns of immunocompetence.     

‘Good-genes’ and ‘compatible-genes’ effects in an Alpine whitefish and the information content of breeding tubercles over the course of the spawning season

Some models of sexual selection predict that individuals vary in their genetic quality and reveal some of this variation in their secondary sexual characteristics. Alpine whitefish (Coregonus sp.) develop breeding tubercles shortly before their spawning season. These tubercles are epidermal structures that are distributed regularly along the body sides of both males and females. There is still much unexplained variation in the size of breeding tubercles within both sexes and with much overlap between the sexes. It has been suggested that breeding tubercles function to maintain body contact between the mating partners during spawning, act as weapons for defence of spawning territories, or are sexual signals that reveal aspects of genetic quality. We took two samples of whitefish from their spawning place, one at the beginning and one around the peak of spawning season. We found that females have on average smaller breeding tubercles than males, and that tubercle size partly reveals the stage of gonad maturation. Two independent full-factorial breeding experiments revealed that embryo mortality was significantly influenced by male and female effects. This finding demonstrates that the males differed in their genetic quality (because offspring get nothing but genes from their fathers). Tubercle size was negatively linked to some aspects of embryo mortality in the first breeding experiment but not significantly so in the second. This lack of consistency adds to inconsistent results that were reported before and suggests that (i) some aspects of genetic quality are not revealed in breeding tubercles while others are, or (ii) individuals vary in their signaling strategies and the information content of breeding tubercles is not always reliable. Moreover, the fact that female whitefish have breeding tubercles of significant size while males seem to have few reasons to be choosy suggests that the tubercles might also serve some functions that are not linked to sexual signaling.     

Leucocytozoonosis and trypanosomiasis in redstarts in Finland.

Leucocytozoon spp. and Trypanosoma spp. blood parasites in the redstart (Phoenicurus phoenicurus) were studied during spring migration 1994 in southern Finland (53 individuals) and the breeding season 1992-1994 in northern Finland (69). Parasite prevalence was higher during the breeding season (48%) than during the migration period (13%), with no age or sex differences in the breeding site birds. In both periods, redstarts were infected by the same blood parasites Leucocytozoon shaartusicum (46% prevalence at the breeding site and 71% during the migration period) and Trypanosoma avium, complex (58% and 43%, respectively). One individual at the breeding site had contracted L. dubreuili and one at the stop-over site had T. everetti. Our results may support the assumption that tissue-hidden parasites relapse during the breeding season when birds may have diminished immune response related to egg production and brood rearing. Another explanation could be that the high abundance of ornithophilic vectors enhance parasite transmission during breeding season in northern Finland.     

Seasonal changes in reproductive and physical condition, sexual dimorphism, and male mating tactics in the jewelled blenny Salarias fasciatus

To investigate seasonal changes in reproductive and physical condition, sexual dimorphism, and mating tactics in the jewelled blenny Salarias fasciatus, monthly collections were conducted on the fringing reef in northern Okinawa, Japan. Monthly variation in the female gonadosomatic index suggested that the breeding season of this species is from April to June. The physical condition and hepatosomatic index of both sexes considerably deteriorated during the course of the breeding season. Such declines may be primarily due to egg production in females and brood care in males. Males’ elongated anal spines were longer than females’, but no other apparent sexual dimorphisms were detected, indicating that S. fasciatus exhibits a low degree of sexual dimorphism. Examinations of testes size and the testicular gland area during the estimated breeding season revealed that the gonadosomatic index values of smaller males did not differ from those of larger males. This result may differ from other blenny species that exhibit alternative male reproductive tactics. However, patterns of male testicular glands of S. fasciatus were similar to those of other blennies with alternative tactics, i.e., smaller males had poorly developed testicular glands compared with larger males.     

Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl

Resistance to disease is frequently suggested to be important in mate choice, but information about how immune status can be conveyed is lacking. During the breeding season, male red jungle fowl with large combs, a sexually selected trait, have lower levels of lymphocytes, but greater cell-mediated immunity, indicated by a cutaneous hypersensitivity response. Before the breeding season, however, both cell-mediated immunity and proportion of lymphocytes are positively correlated with comb length. Cell-mediated immunity is particularly important to jungle fowl during the breeding season, because the likelihood of injury during sexual competition is high and cell-mediated immunity is essential for healing wounds and resisting infection. This seasonal change in one aspect of immunity but not another suggests that the birds adaptively maintain certain immune system abilities, and that it can be misleading to use a single aspect of immune response in evaluating immunocompetence.     

Father–offspring phenotypic correlations suggest intralocus sexual conflict for a fitness-linked trait in a wild sexually dimorphic mammal

In sexually dimorphic and polygynous mammals, sexual selection often favours large males with well-developed weaponry, as these secondary sexual characters confer advantages in intrasexual competition and are often preferred by females. Little is known, however, about the effects of sexually selected paternal traits on offspring phenotype in wild mammals, especially when considering that shared phenotypic traits and selection can also differ greatly between genders. Here, we conducted molecular parentage analyses in a long-term study population of mountain goats (Oreamnos americanus), an ungulate exhibiting high sexual dimorphism in mass, to first assess the determinants of yearly reproductive success (YRS) in males. We then examined the effects of paternal characteristics on offspring mass at 1 year of age. Paternity was highly skewed, with 9 per cent of 57 males siring 51 per cent of 96 offspring assigned over 12 years. Male YRS increased with age until apparent reproductive senescence at 9 years, but mass was a stronger determinant of siring success than age, horn length or social rank. Mass of sons increased with paternal mass, but the mass of daughters was negatively related to that of their father, a finding consistent with recent theory on intralocus sexual conflict. Because early differences in mass persisted to early adulthood, sex-specific effects of paternal mass can have important fitness consequences, as adult mass is positively linked with reproduction in both sexes. Divergent father–offspring phenotypic correlations may partly explain the maintenance of sexual dimorphism in mountain goats and the large variance observed for this homologous trait within each gender in polygynous mammals.     

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.     

The costs of reproduction to males and females of a paternal mouthbrooding cardinalfish Apogon notatus

In the cardinalfish Apogon notatus , starving males mouthbrood the eggs, and females are more active than males in courtship and in attacks against conspecific intruders upon their breeding territory, but sexual ornaments are developed in males. Condition factor, hepatosomatic index and fat body-somatic index declined in both sexes during the breeding season. The deterioration of somatic condition was more severe in females, suggesting that the overall energetic costs were larger for females which produced more than twice as many clutches as males brooded in a season. Selective mortality of females could be due primarily to the depletion of their energy reserves. The increased mortality in females is a possible mechanism for the male-biased operational sex ratio which may provide the potential for sexual selection on males.     

The postnatal ontogeny of the sexually dimorphic vocal apparatus in goitred gazelles (Gazella subgutturosa)

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male‐specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age‐classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade‐off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826–844, 2016. © 2016 Wiley Periodicals, Inc.     

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.     

Selection on multiple sexual signals in two Central and Eastern European populations of the barn swallow

Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations, although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Central and East European barn swallow (Hirundo rustica rustica) populations from Czech Republic and Romania over multiple years. We then related these differences in selection to variation in sexual characters among barn swallow populations. Our results show that tail length and ventral coloration vary between populations, sexes, and age classes (first‐time breeders vs. experienced birds). We found that selection on tail length was stronger in first‐time breeders than in experienced birds and in males than in females in the Romanian population, while these differences between age groups and sexes were weak in Czech birds. We suggest that the populational difference in selection on tail length might be related to the differences in breeding conditions. Our results show that ventral coloration is darker (i.e., has lower brightness) in the Romanian than in the Czech population, and in experienced birds and males compared with first‐time breeders and females, respectively. The sexual difference in ventral coloration may suggest sexual selection on this trait, which is supported by the significant directional selection of ventral coloration in first‐time breeding males on laying date. However, after controlling for the confounding effect of wing length and tarsus length, the partial directional selection gradient on this trait turned nonsignificant, suggesting that the advantage of dark ventral coloration in early breeding birds is determined by the correlated traits of body size. These findings show that ventral coloration may be advantageous over the breeding season, but the underlying mechanism of this relationship is not clarified.