Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets.

The evolution of nuptial gifts has traditionally been considered a harmonious affair, providing benefits to both mating partners. There is growing evidence, however, that receiving a nuptial gift can be actively detrimental to the female. In decorated crickets (Gryllodes sigillatus), males produce a gelatinous spermatophylax that enhances sperm transfer but provides little nutritional benefit and hinders female post-copulatory mate choice. Here, we examine the sexually antagonistic coevolution of the spermatophylax and the female feeding response to this gift in G. sigillatus maintained in experimental populations with either a male-biased or female-biased adult sex ratio. After 25 generations, males evolving in male-biased populations produced heavier spermatophylaxes with a more manipulative combination of free amino acids than those evolving in female-biased populations. Moreover, when the spermatophylax originated from the same selection regime, females evolving in male-biased populations always had shorter feeding durations than those evolving in female-biased populations, indicating the evolution of greater resistance. Across populations, female feeding duration increased with the mass and manipulative combination of free amino acids in the spermatophylax, suggesting sexually antagonistic coevolution. Collectively, our work demonstrates a key role for interlocus sexual conflict and sexually antagonistic coevolution in the mating system of G. sigillatus.

Transcriptomic responses of females to consumption of nuptial food gifts as a potential mediator of sexual conflict in decorated crickets.

Nuptial food gift provisioning by males to females at mating is a strategy in many insects that is thought to be shaped by sexual conflict or sexual selection, as it affords males access to a female's physiology. While males often attempt to use these gifts to influence female behaviour to their own advantage, females can evolve counter mechanisms. In decorated crickets, the male's nuptial gift comprises part of the spermatophore, the spermatophylax, the feeding on which deters the female from prematurely terminating sperm transfer. However, ingested compounds in the spermatophylax and attachment of the sperm-containing ampulla could further influence female physiology and behaviour. We investigated how mating per se and these two distinct routes of potential male-mediated manipulation influence the female transcriptomic response. We conducted an RNA sequencing experiment on gut and head tissues from females for whom nuptial food gift consumption and receipt of an ejaculation were independently manipulated. In the gut tissue, we found that females not permitted to feed during mating exhibited decreased overall gene expression, possibly caused by a reduced gut function, but this was countered by feeding on the spermatophylax or a sham gift. In the head tissue, we found only low numbers of differentially expressed genes, but a gene co-expression network analysis revealed that ampulla attachment and spermatophylax consumption independently induce distinct gene expression patterns. This study provides evidence that spermatophylax feeding alters the female post-mating transcriptomic response in decorated crickets, highlighting its potential to mediate sexual conflict in this system.

Decision rules for egg-color-based rejection by two cavity-nesting hosts of the brown-headed cowbird.

Hosts of obligate avian brood parasites often evolve defense mechanisms to avoid rearing unrelated young. One common defense is egg rejection, for which hosts often rely on eggshell color. Most research has assumed that hosts respond to perceived color differences between their own eggs and parasite eggs regardless of the particular color; however, recent experiments have found that many hosts respond more strongly to brown foreign eggs than to equally dissimilar blue eggs. Yet, none of these prior studies tested a brown-egg-laying species and, with only one exception, all were conducted in open nests where light levels are considered sufficient for effective color-based egg discrimination. Here, we explored how two cavity-nesting hosts of the parasitic brown-headed cowbird (Molothrus ater) - the blue-egg-laying eastern bluebird (Sialia sialis) and the brown-egg-laying house wren (Troglodytes aedon) - respond to experimental eggs painted six distinct colors ranging from blue to brown. Rejection responses of both hosts were best predicted by perceived differences in color between the model egg and their own eggs. Specifically, we found that house wrens preferentially rejected eggs bluer than their own eggs. However, although we found that bluebirds relied on perceived differences in color for their egg rejection decisions, further tests are needed to determine whether they preferentially rejected brown eggs or simply responded to absolute perceived differences in color. These findings demonstrate that these cavity-nesting birds treat perceived color differences in distinct ways, which has important implications on the coevolutionary arms races and the interpretation of avian-perceived color differences.

Evolution of immune function in response to dietary macronutrients in male and female decorated crickets.

Although dietary macronutrients are known to regulate insect immunity, few studies have examined their evolutionary effects. Here, we evaluate this relationship in the cricket Gryllodes sigillatus by maintaining replicate populations on four diets differing in protein (P) to carbohydrate (C) ratio (P- or C-biased) and nutritional content (low- or high-nutrition) for >37 generations. We split each population into two; one maintained on their evolution diet and the other switched to their ancestral diet. We also maintained populations exclusively on the ancestral diet (baseline). After three generations, we measured three immune parameters in males and females from each population. Immunity was higher on P-biased than C-biased diets and on low- versus high-nutrition diets, although the latter was most likely driven by compensatory feeding. These patterns persisted in populations switched to their ancestral diet, indicating genetic divergence. Crickets evolving on C-biased diets had lower immunity than the baseline, whereas their P-biased counterparts had similar or higher immunity than the baseline, indicating that populations evolved with dietary manipulation. Although females exhibited superior immunity for all assays, the sexes showed similar immune changes across diets. Our work highlights the important role that macronutrient intake plays in the evolution of immunity in the sexes.

Genetic covariance in immune measures and pathogen resistance in decorated crickets is sex and pathogen specific.

Insects are important models for studying immunity in an ecological and evolutionary context. Yet, most empirical work on the insect immune system has come from phenotypic studies meaning we have a limited understanding of the genetic architecture of immune function in the sexes. We use nine highly inbred lines to thoroughly examine the genetic relationships between a suite of commonly used immune assays (haemocyte count, implant encapsulation, total phenoloxidase activity, antibacterial zone of inhibition and pathogen clearance) and resistance to infection by three generalist insect pathogens (the gram-negative bacterium Serratia marcescens, the gram-positive bacterium Bacillus cereus and the fungus Metarhizium robertsii) in male and female Gryllodes sigillatus. There were consistent positive genetic correlations between haemocyte count, antibacterial and phenoloxidase activity and resistance to S. marcescens in both sexes, but these relationships were less consistent for resistance to B. cereus and M. robertsii. In addition, the clearance of S. marcescens was genetically correlated with the resistance to all three pathogens in both sexes. Genetic correlations between resistances to the different pathogen species were inconsistent, indicating that resistance to one pathogen does not necessarily mean resistance to another. Finally, while there is ample genetic (co)variance in immune assays and pathogen resistance, these genetic estimates differed across the sexes and many of these measures were not genetically correlated across the sexes, suggesting that these measures could evolve independently in the sexes. Our finding that the genetic architecture of immune function is sex and pathogen specific suggests that the evolution of immune function in male and female G. sigillatus is likely to be complex. Similar quantitative genetic studies that measure a large number of assays and resistance to multiple pathogens in both sexes are needed to ascertain if this complexity extends to other species.

Sex-specific effects of hatching order on nestling baseline corticosterone in a wild songbird.

Variation in nestling growth and survival is often influenced by hatching order, with first-hatched offspring having an advantage over later-hatched younger siblings. In house wrens (Troglodytes aedon), this effect of hatching order is especially evident in asynchronously hatched broods and can lead to sex-specific differences in the size and condition of nestlings. Females appear to allocate the sex of their offspring across the laying order to capitalize on these differences. We hypothesized that levels of circulating corticosterone, the primary metabolic hormone in birds, mediates these sex-specific effects in nestlings. We predicted that: i) baseline levels of corticosterone in nestlings should vary along the hatching order, ii) effects of hatching order on baseline corticosterone should be sex specific, and iii) any sex-specificity of hatching order on baseline corticosterone could be contingent on the degree of hatching synchrony. We tested these predictions in a study in which we measured baseline corticosterone in first- and last-hatched nestlings in synchronously and asynchronously hatching broods. To assess whether any differences in nestling baseline corticosterone levels could be attributed to pre-natal maternal effects, the post-natal environment, or both, we conducted two additional studies in which we measured i) yolk corticosterone in first- and last-laid eggs and ii) baseline corticosterone in nestlings that were cross-fostered to create simulated 'asynchronously' hatched broods. There was a significant interaction between sex and relative hatching order in their effects on nestling baseline corticosterone, but no effect of hatching synchrony. Corticosterone levels remained relatively constant across the hatching order in males but decreased in females. There was a significant effect of laying order on yolk corticosterone, with first-laid eggs containing significantly higher levels of yolk corticosterone than last-laid eggs. Cross-fostering of nestlings at different points of development had no significant effect on nestling corticosterone levels. These results indicate that sex-dependent differences in corticosterone levels across the hatching order may arise, at least in part, from embryonic exposure to maternally derived corticosterone, whereas the post-natal rearing environment plays, at best, a minimal role in determining nestling baseline corticosterone levels.

Male and female genotype and a genotype-by-genotype interaction mediate the effects of mating on cellular but not humoral immunity in female decorated crickets.

Sexually antagonistic coevolution is predicted to lead to the divergence of male and female genotypes related to the effects of substances transferred by males at mating on female physiology. The outcome of mating should thus depend on the specific combination of mating genotypes. Although mating has been shown to influence female immunity in diverse insect taxa, a male-female genotype-by-genotype effect on female immunity post mating remains largely unexplored. Here, we investigate the effects of mating on female decorated cricket baseline immunity and the potential for a male-genotype-by-female-genotype interaction affecting this response. Females from three distinct genotypic backgrounds were left unmated or singly mated in a fully reciprocal design to males from the same three genotypic backgrounds. Hemocytes and hemocyte microaggregations were quantified for female cellular immunity, and phenoloxidase, involved in melanization, and antibacterial activity for humoral immunity. In this system, female cellular immunity was more reactive to mating, and mating effects were genotype-dependent. Specifically, for hemocytes, a genotype-by-mating status interaction mediated the effect of mating per se, and a significant male-female genotype-by-genotype interaction determined hemocyte depletion post mating. Microaggregations were influenced by the female's genotype or that of her mate. Female humoral immune measures were unaffected, indicating that the propensity for post-mating effects on females is dependent on the component of baseline immunity. The genotype-by-genotype effect on hemocytes supports a role of sexual conflict in post-mating immune suppression, suggesting divergence of male genotypes with respect to modification of female post-mating immunity, and divergence of female genotypes in resistance to these effects.

Female birds monitor the activity of their mates while brooding nest-bound young.

In addition to food and protection, altricial young in many species are ectothermic and require that endothermic parents provide warmth to foster growth, yet only one parent-typically the female-broods these young to keep them warm. When this occurs, reduced provisioning by males obliges females to forage instead of providing warmth for offspring, favoring the temporal mapping of male activities. We assessed this in a wild house wren population while experimentally feeding nestlings to control offspring satiety. While brooding, females look out from the nest to inspect their surroundings, and we hypothesized that this helps to determine if their mate is nearby and likely to deliver food to the brood (males pass food to brooding females, which pass the food to nestlings). Females looked out from the nest less often when their partner was singing nearby and when his singing and provisioning were temporally linked, signaling his impending food delivery. Females also left to forage less often when their mate was nearby and likely to deliver food. Nestling begging did not affect these behaviors. Females looking out from the nest more often also provisioned at a higher rate and were more likely to divorce and find a new mate prior to nesting again within seasons, as expected if females switch mates when a male fails to meet expectations. Our results suggest anticipatory effects generated by male behavior and that brooding females temporally map male activity to inform decisions about whether to continue brooding or to leave the nest to forage.

Condition-Dependent Begging Elicits Increased Parental Investment in a Wild Bird Population.

The coevolution of parental supply and offspring demand has long been thought to involve offspring need driving begging and parental care, leaving other hypotheses underexplored. In a population of wild birds, we experimentally tested whether begging serves as a negatively condition-dependent signal of need or a positively condition-dependent signal of quality. Across multiple years, we supplemented nestling house wrens with food shortly after hatching and simultaneously manipulated corticosterone levels to simulate the hunger-induced increase in glucocorticoids thought to mediate begging. This allowed us to also test whether begging is simply a proximate signal of hunger. Days after supplementation ended, food-supplemented nestlings were in better condition than nonsupplemented nestlings and begged for food at an increased rate; their parents, in turn, increased provisioning to a greater extent than parents of nonsupplemented young, as begging positively predicted provisioning. Food-supplemented nestlings therefore attained above-average condition, which predicted their recruitment as breeding adults in the local population. Glucocorticoids increased begging in the short term, but this transient effect depended on satiety. Thus, glucocorticoids promoted begging as a proximate response to hunger, whereas the longer-term changes in nestling condition, begging, and food provisioning suggest that begging ultimately signals offspring quality to elicit increased investment, thereby enhancing offspring survival.

Inbreeding alters context-dependent reproductive effort and immunity in male crickets.

Infection can cause hosts to drastically alter their investment in key life-history traits of reproduction and defence. Infected individuals are expected to increase investment in defence (e.g., by increasing immune function) and, due to trade-offs, investment in other traits (e.g., current reproduction) should decrease. However, the terminal investment hypothesis postulates that decreased lifespan due to infection and the associated reduction in the expectation for future offspring will favour increased investment towards current reproduction. Variation in intrinsic condition will likely influence shifts in reproductive investment post-infection, but this is often not considered in such assessments. For example, the extent of inbreeding can significantly impact an individual's lifetime fitness and may influence its reproductive behaviour following a threat of infection. Here, we investigated the effects of inbreeding status on an individual's reproductive investment upon infection, including the propensity to terminally invest. Male crickets (Gryllodes sigillatus) from four genetically distinct inbred lines and one outbred line were subjected to a treatment from an increasing spectrum of simulated infection cue intensities, using heat-killed bacteria. We then measured reproductive effort (calling effort), survival and immune function (antibacterial activity, circulating haemocytes and haemocyte microaggregations). Inbred and outbred males diverged in how they responded to a low-dose infection cue: relative to unmanipulated males, outbred males decreased calling effort, whereas inbred males increased calling effort. Moreover, we found that inbred males exhibited higher antibacterial activity and numbers of circulating haemocytes compared with outbred males. These results suggest that an individual's inbreeding status may have consequences for context-dependent shifts in reproductive strategies, such as those triggered by infection.

The Geometry of Nutrient Space-Based Life-History Trade-Offs: Sex-Specific Effects of Macronutrient Intake on the Trade-Off between Encapsulation Ability and Reproductive Effort in Decorated Crickets.

Life-history theory assumes that traits compete for limited resources, resulting in trade-offs. The most commonly manipulated resource in empirical studies is the quantity or quality of diet. Recent studies using the geometric framework for nutrition, however, suggest that trade-offs are often regulated by the intake of specific nutrients, but a formal approach to identify and quantify the strength of such trade-offs is lacking. We posit that trade-offs occur whenever life-history traits are maximized in different regions of nutrient space, as evidenced by nonoverlapping 95% confidence regions of the global maximum for each trait and large angles (θ) between linear nutritional vectors and Euclidean distances (d) between global maxima. We then examined the effects of protein and carbohydrate intake on the trade-off between reproduction and aspects of immune function in male and female Gryllodes sigillatus. Female encapsulation ability and egg production increased with the intake of both nutrients, whereas male encapsulation ability increased with protein intake but calling effort increased with carbohydrate intake. The trade-offs between traits was therefore larger in males than in females, as demonstrated by significant negative correlations between the traits in males, nonoverlapping 95% confidence regions, and larger estimates of θ and d. Under dietary choice, the sexes had similar regulated intakes, but neither optimally regulated nutrient intake for maximal trait expression. We highlight the fact that greater consideration of specific nutrient intake is needed when examining nutrient space-based trade-offs.

Offspring dependence on parental care and the role of parental transfer of oral fluids in burying beetles.

BACKGROUND: Immature stages of many animals can forage and feed on their own, whereas others depend on their parents' assistance to obtain or process food. But how does such dependency evolve, and which offspring and parental traits are involved? Burying beetles (Nicrophorus) provide extensive biparental care, including food provisioning to their offspring. Interestingly, there is substantial variation in the reliance of offspring on post-hatching care among species. Here, we examine the proximate mechanisms underlying offspring dependence, focusing on the larvae of N. orbicollis, which are not able to survive in the absence of parents. We specifically asked whether the high offspring dependence is caused by (1) a low starvation tolerance, (2) a low ability to self-feed or (3) the need to obtain parental oral fluids. Finally, we determined how much care (i.e. duration of care) they require to be able to survive. RESULTS: We demonstrate that N. orbicollis larvae are not characterized by a lower starvation tolerance than larvae of the more independent species. Hatchlings of N. orbicollis are generally able to self-feed, but the efficiency depends on the kind of food presented and differs from the more independent species. Further, we show that even when providing highly dependent N. orbicollis larvae with easy ingestible liquefied mice carrion, only few of them survived to pupation. However, adding parental oral fluids significantly increased their survival rate. Finally, we demonstrate that survival and growth of dependent N. orbicollis larvae is increased greatly by only a few hours of parental care. CONCLUSIONS: Considering the fact that larvae of other burying beetle species are able to survive in the absence of care, the high dependence of N. orbicollis larvae is puzzling. Even though they have not lost the ability to self-feed, an easily digestible, liquefied carrion meal is not sufficient to ensure their survival. However, our results indicate that the transfer of parental oral fluids is an essential component of care. In the majority of mammals, offspring rely on the exchange of fluids (i.e. milk) to survive, and our findings suggest that even in subsocial insects, such as burying beetles, parental fluids can significantly affect offspring survival.

Size of nest-cavity entrance influences male attractiveness and paternal provisioning in house wrens.

In altricial birds, parental provisioning is plastic and can respond to a variety of environmental stimuli. In this study, we manipulated the size of entrances into artificial nest cavities (i.e., nestboxes) in a population of house wrens (Troglodytes aedon) as a means of manipulating a male's sexual attractiveness, and examined changes in parental provisioning. Nest cavities with large entrances are less desirable as nesting sites, and the males at these sites are less attractive to females. Therefore, we predicted that males at boxes that had large entrances would invest more in parental care (i.e., those that succeeded in finding a mate would provision their offspring at a higher rate) than males at nestboxes with small entrances. As predicted, males provisioned their offspring with food at the highest rates at nestboxes with enlarged entrances, and male provisioning effort positively predicted the number of fledglings they produced per egg. Males at these boxes provisioned more than their mates and more than females and males at nestboxes with small entrances. At nestboxes with small entrances, males provisioned at the same rate as females, and female provisioning did not differ significantly between treatments, on average. Male and female provisioning rates were negatively correlated, such that the increase in provisioning by males at nestboxes with enlarged entrances did not enhance nestling condition, likely because food delivery by females declined with increased provisioning by males. However, the amount of time females spent providing warmth for their ectothermic young increased with increases in male provisioning, suggesting that levels of male parental care altered the mode, not necessarily the extent, of care provided by females. These findings suggest that male provisioning is related to sexual attractiveness, and that sexual conflict over biparental care may not be as simple as the assessment of food provisioning might otherwise suggest.

Spring temperatures influence selection on breeding date and the potential for phenological mismatch in a migratory bird.

Climate change has affected the seasonal phenology of a variety of taxa, including that of migratory birds and their critical food resources. However, whether climate-induced changes in breeding phenology affect individual fitness, and how these changes might therefore influence selection on breeding date remain unresolved. Here, we use a 36-yr dataset from a long-term, individual-based study of House Wrens (Troglodytes aedon) to test whether the timing of avian breeding seasons is associated with annual changes in temperature, which have increased to a small but significant extent locally since the onset of the study in 1980. Increasing temperature was associated with an advancement of breeding date in the population, as the onset of breeding within years was closely associated with daily spring temperatures. Warmer springs were also associated with a reduced incubation period, but reduced incubation periods were associated with a prolonged duration of nestling provisioning. Nest productivity, in terms of fledgling production, was not associated with temperature, but wetter springs reduced fledging success. Most years were characterized by selection for earlier breeding, but cool and wet years resulted in stabilizing selection on breeding date. Our results indicate that climate change and increasing spring temperatures can affect suites of life-history traits, including selection on breeding date. Increasing temperatures may favor earlier breeding, but the extent to which the phenology of populations might advance may be constrained by reductions in fitness associated with early breeding during cool, wet years. Variability in climatic conditions will, therefore, shape the extent to which seasonal organisms can respond to changes in their environment.

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird.

Glucocorticoids circulating in breeding birds during egg production accumulate within eggs, and may provide a potent form of maternal effect on offspring phenotype. However, whether these steroids affect offspring development remains unclear. Here, we employed a non-invasive technique that experimentally elevated the maternal transfer of corticosterone to eggs in a wild population of house wrens. Feeding corticosterone-injected mealworms to free-living females prior to and during egg production increased the number of eggs that females produced and increased corticosterone concentrations in egg yolks. This treatment also resulted in an increase in the amount of yolk allocated to eggs. Offspring hatching from these eggs begged for food at a higher rate than control offspring and eventually attained increased prefledging body condition, a trait predictive of their probability of recruitment as breeding adults in the study population. Our results indicate that an increase in maternal glucocorticoids within the physiological range can enhance maternal investment and offspring development.

Immune activation generates corticosterone-mediated terminal reproductive investment in a wild bird.

Despite classical expectations of a trade-off between immune activity and reproduction, an emergent view suggests that individuals experiencing activation of their immune system actually increase reproductive effort and allocation to offspring as a form of terminal investment in response to reduced survival probability. However, the components and mechanisms of increased parental investment following immunostimulation are currently unknown. We hypothesize that increased glucocorticoid production following immunostimulation modulates the increase in reproductive effort that constitutes terminal investment. We activated the immune system of breeding female house wrens (Troglodytes aedon) with an immunogen and cross-fostered the eggs that they subsequently produced to separate prenatal and postnatal components of maternal investment. Cross-fostering revealed an increase in both pre- and postnatal allocation from immunostimulated females, which was confirmed by quantification of egg constituents and maternal provisioning behavior. The increase in maternal provisioning was mediated, at least in part, by increased corticosterone in these females. Offspring immune responsiveness was also enhanced through transgenerational immune priming via the egg. Thus, our results indicate that maternal immunostimulation induces transgenerational effects on offspring through both pre- and postnatal parental effects and support an important role for corticosterone in mediating parental investment.

Persistent sex-by-environment effects on offspring fitness and sex-ratio adjustment in a wild bird population.

A major component of sex-allocation theory, the Trivers-Willard model (TWM), posits that sons and daughters are differentially affected by variation in the rearing environment. In many species, the amount of parental care received is expected to have differing effects on the fitness of males and females. When this occurs, the TWM predicts that selection should favour adjustment of the offspring sex ratio in relation to the expected fitness return from offspring. However, evidence for sex-by-environment effects is mixed, and little is known about the adaptive significance of producing either sex. Here, we test whether offspring sex ratios vary according to predictions of the TWM in the house wren (Troglodytes aedon, Vieillot). We also test the assumption of a sex-by-environment effect on offspring using two experiments, one in which we manipulated age differences among nestlings within broods, and another in which we held nestling age constant but manipulated brood size. As predicted, females with high investment ability overproduced sons relative to those with lower ability. Males were also overproduced early within breeding seasons. In our experiments, the body mass of sons was more strongly affected by the sibling-competitive environment and resource availability than that of daughters: males grew heavier than females when reared in good conditions but were lighter than females when in poor conditions. Parents rearing broods with 1:1 sex ratios were more productive than parents rearing broods biased more strongly towards sons or daughters, suggesting that selection favours the production of mixed-sex broods. However, differences in the condition of offspring as neonates persisted to adulthood, and their reproductive success as adults varied with the body mass of sons, but not daughters, prior to independence from parental care. Thus, selection should favour slight but predictable variations in the sex ratio in relation to the quality of offspring that parents are able to produce. Offspring sex interacts with the neonatal environment to influence offspring fitness, thus favouring sex-ratio adjustment by parents. However, increased sensitivity of males to environmental conditions, such as sibling rivalry and resource availability, reduces the fitness returns from highly male-biased broods.

Mass-based condition measures and their relationship with fitness: in what condition is condition?

Mass or body-size measures of 'condition' are of central importance to the study of ecology and evolution, and it is often assumed that differences in condition measures are positively and linearly related to fitness. Using examples drawn from ecological studies, we show that indices of condition frequently are unlikely to be related to fitness in a linear fashion. Researchers need to be more explicit in acknowledging the limitations of mass-based condition measures and accept that, under some circumstances, they may not relate to fitness as traditionally assumed. Any relationship between a particular condition measure and fitness should first be empirically validated before condition is used as a proxy for fitness. In the absence of such evidence, researchers should explicitly acknowledge that assuming such a relationship may be unrealistic.

Genetic and environmental variation in condition, cutaneous immunity, and haematocrit in house wrens.

BACKGROUND: Life-history studies of wild bird populations often focus on the relationship between an individual's condition and its capacity to mount an immune response, as measured by a commonly-employed assay of cutaneous immunity, the PHA skin test. In addition, haematocrit, the packed cell volume in relation to total blood volume, is often measured as an indicator of physiological performance. A multi-year study of a wild population of house wrens has recently revealed that those exhibiting the highest condition and strongest PHA responses as nestlings are most likely to be recruited to the breeding population and to breed through two years of age; in contrast, intermediate haematocrit values result in the highest recruitment to the population. Selection theory would predict, therefore, that most of the underlying genetic variation in these traits should be exhausted resulting in low heritability, although such traits may also exhibit low heritability because of increased residual variance. Here, we examine the genetic and environmental variation in condition, cutaneous immunity, and haematocrit using an animal model based on a pedigree of approximately 2,800 house wrens. RESULTS: Environmental effects played a paramount role in shaping the expression of the fitness-related traits measured in this wild population, but two of them, condition and haematocrit, retained significant heritable variation. Condition was also positively correlated with both the PHA response and haematocrit, but in the absence of any significant genetic correlations, it appears that this covariance arises through parallel effects of the environment acting on this suite of traits. CONCLUSIONS: The maintenance of genetic variation in different measures of condition appears to be a pervasive feature of wild bird populations, in contradiction of conventional selection theory. A major challenge in future studies will be to explain how such variation persists in the face of the directional selection acting on condition in house wrens and other species.

Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population.

Measures of body condition, immune function, and hematological health are widely used in ecological studies of vertebrate populations, predicated on the assumption that these traits are linked to fitness. However, compelling evidence that these traits actually predict long-term survival and reproductive success among individuals in the wild is lacking. Here, we show that body condition (i.e., size-adjusted body mass) and cutaneous immune responsiveness to phytohaemagglutinin (PHA) injection among neonates positively predict recruitment and subsequent longevity in a wild, migratory population of house wrens (Troglodytes aedon). However, neonates with intermediate hematocrit had the highest recruitment and longevity. Neonates with the highest PHA responsiveness and intermediate hematocrit prior to independence eventually produced the most offspring during their lifetime breeding on the study site. Importantly, the effects of PHA responsiveness and hematocrit were revealed while controlling for variation in body condition, sex, and environmental variation. Thus, our data demonstrate that body condition, cutaneous immune responsiveness, and hematocrit as a neonate are associated with individual fitness. Although hematocrit's effect is more complex than traditionally thought, our results suggest a previously underappreciated role for this trait in influencing survival in the wild.