Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon)

The reproductive costs associated with the upregulation of immunity have been well-documented and constitute a fundamental trade-off between reproduction and self-maintenance. However, recent experimental work suggests that parents may increase their reproductive effort following immunostimulation as a form of terminal parental investment as prospects for future reproduction decline. We tested the trade-off and terminal investment hypotheses in a wild population of house wrens (Troglodytes aedon) by challenging the immune system of breeding females with lipopolysaccharide, a potent but non-lethal antigen. Immunized females showed no evidence of reproductive costs; instead, they produced offspring of higher phenotypic quality, but in a sex-specific manner. Relative to control offspring, sons of immunized females had increased body mass and their sisters exhibited higher cutaneous immune responsiveness to phytohaemagglutinin injection, constituting an adaptive strategy of sex-biased allocation by immune-challenged females to enhance the reproductive value of their offspring. Thus, our results are consistent with the terminal investment hypothesis, and suggest that maternal immunization can induce pronounced transgenerational effects on offspring phenotypes.     

No evidence for long‐term effects of reproductive effort on parasite prevalence in great tits Parus major

Allocation of resources between the life history traits reproduction and parasite defence are expected because both are energetically costly. Experimental evidence for such allocation has been found in short‐term effects of reproduction on parasite prevalence or immune function. However, there is increasing evidence for long‐term negative effects of reproductive effort on individuals. This study investigates whether long‐term effects of reproductive effort on parasite prevalence exist. Brood sizes of great tits Parus major were experimentally altered in one breeding season and in the subsequent breeding season the prevalence of three parasites types (blood parasites, ticks and fleas) on the surviving parents were investigated. We detected no long‐term effects of brood size manipulation on the prevalence of parasites in the next year and therefore provide no evidence for inter‐seasonal effects of reproductive effort on parasite prevalence. The post hoc level of statistical power was reasonable for effects on blood parasite and flea prevalence, but low for effects on tick prevalence.     

Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health

Blood parasites may act as modulators of their hosts' ecology, life histories and fitness. We studied the prevalence of Plasmodium sp., Haemoproteus sp. and Leucocytozoon sp. and their effects on morphological, biochemical and haematological variables and on breeding effort of Great Tits Parus major . Total prevalence (percentage of individuals infected by any parasite) ranged from 7.7% to 61.1%. There was an overall positive association in prevalence between the three haematozoan parasites. No effect of sex or age on infection status was observed. Negative impacts of infection on physiological condition depended largely on year and/or season and included effects on body condition index, plasma protein and haemoglobin index. There were also indications that parasite infection increased immune response and stress levels and activated antioxidant defence mechanisms. Males with higher fledging success had a higher probability of Haemoproteus infection, and females laying heavier eggs had a higher probability of Plasmodium infection. However, clutch size was negatively associated with the probability of infection by Leucocytozoon and Haemoproteus . Surprisingly, males raising second broods had a lower prevalence of both Haemoproteus and Leucocytozoon . Only 5.7% of first-brood nestlings were infected, but those in infected nestboxes had a lower heterophil/lymphocyte ratio. This study confirms the pathogenicity of blood parasites to the host by demonstrating negative effects of infection on both physiology and breeding performance.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.     

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.     

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.     

Effect of restricted preen-gland access on maternal self maintenance and reproductive investment in mallards

Background

As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg.

Methodology/Principal Findings

Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access.

Conclusion/Significance

Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.     

Transgenerational immunity in a bird–ectoparasite system: do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas?

During egg formation, female birds deposit antibodies against parasites and pathogens they were exposed to before egg laying into the yolk. In captive bird species, it has been shown that these maternal immunoglobulins (maternal yolk IgGs) can protect newly hatched offspring against infection. However, direct evidence for such benefits in wild birds is hitherto lacking. We investigated (1) if nestling Great Tits Parus major originating from eggs with naturally high levels of maternal yolk IgG are less susceptible to a common, nest-based ectoparasite, (2) if maternal yolk IgGs influence nestling development and in particular, their own immune defence, and (3) if there is a negative correlation between levels of maternal yolk IgG in host eggs and the reproductive success of ectoparasitic fleas feeding on the nestlings. Counter to expectations, we found no indication that maternally transferred yolk IgGs have direct beneficial effects on nestling development, nestling immune response or nestling resistance or tolerance to fleas. Furthermore, we found no negative correlation between host yolk IgG levels and parasite fecundity. Thus, whereas previous work has unequivocally shown that prenatal maternal effects play a crucial role in shaping the parasite resistance of nestling birds, our study indicates that other egg components, such as hormones, carotenoids or other immuno-active substances, which bird females can adjust more quickly than yolk IgG, might mediate these effects.     

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.     

Antioxidants in eggs of great tits <Emphasis Type="Italic">Parus major</Emphasis> from Chernobyl and hatching success

Antioxidants are powerful protectors against the damaging effects of free radicals that constitute the inevitable by-products of aerobic metabolism. Growing embryos are particularly susceptible to the damaging effects of free radicals produced during rapid growth, and mothers of many species provide protection against such damage by allocating antioxidants to their eggs. Birds living in radioactively contaminated areas use dietary antioxidants to cope with the damaging effects of radiation, but females also allocate dietary antioxidants to eggs, potentially enforcing a physiological trade-off between self-maintenance and reproductive investment. Here we tested whether female great tits Parus major breeding in radioactively contaminated study areas near Chernobyl allocated less dietary antioxidants to eggs, and whether such reduced allocation of dietary antioxidants to eggs had fitness consequences. Concentrations of total yolk carotenoids and vitamins A and E were depressed near Chernobyl compared to concentrations in a less contaminated Ukrainian study area and a French control study area, and all antioxidants showed dose-dependent relationships with all three dietary antioxidants decreasing with increasing level of radiation at nest boxes. These effects held even when controlling statistically for potentially confounding habitat variables and covariation among antioxidants. Laying date was advanced and clutch size increased at nest boxes with high dose rates. Hatching success increased with increasing concentration of vitamin E, implying that hatching success decreased at boxes with high levels of radiation, eventually eliminating and even reversing the higher potential reproductive output associated with early reproduction and large clutch size. These findings are consistent with the hypothesis that radioactive contamination reduced levels of dietary antioxidants in yolks, with negative consequences for hatching success and reproductive success.     

Assessing the cost of mounting an immune response

The evolution of parasite resistance has often been assumed to be governed by antagonistic selection pressures. Defense against pathogens, by mounting an immune response, confers evident benefits but may also incur costs, so that the optimal level of defense is expected to depend on the balance between benefits and costs. Although the benefits of immune surveillance are well known, estimates of costs are still equivocal. Here we studied the behavioral and physiological modifications associated with exposure to a nonreplicating antigen (lipopolysaccharide [LPS] of Escherichia coli) in a passerine species, the house sparrow (Passer domesticus). We further investigated whether the behavioral and physiological changes provoked by LPS induced measurable repercussions on life-history traits, such as the breeding effort and reproductive success. Finally, we tested whether the trade-off between immune activation and breeding effort was modulated by the workload required to feed the brood. Exposure to LPS reduced activity and increased body mass loss of captive individuals; similarly, LPS injection induced a dramatic drop in feeding rate and reproductive success of breeding females. However, this reduction depended on brood size, suggesting that the strength of the trade-off between immune activation and reproduction was affected by the workload required to feed the brood. Overall, this study stresses the magnitude of costs associated with mounting immune responses and the ecological and evolutionary consequences for natural populations.     

Variation in parental rearing expenditure triggers short‐term physiological effects on offspring in a long‐lived seabird

Parental care in long‐lived bird species involves a trade‐off between the benefits of increasing the effort expended on current offspring and the costs that this represents for future reproductive output. Under regimes of high environmental variability, long‐lived seabirds can adjust their breeding effort to buffer the negative effects of this variability on their offspring. However, the potential impacts of variation in breeding effort on offspring physiology in the short term and on longer‐term survival are poorly understood. In this study, we manipulated brood age through a cross‐fostering experiment to assess whether increasing or decreasing parental reproductive expenditure led to costs in Blue‐footed Booby Sula nebouxii chicks. Specifically, we tested the consequences of altered parental reproductive expenditure on the offspring's physiological condition (plasma metabolites, heterophil to lymphocyte ratio (H/L) and body condition index (BCI)) and survival. Offspring from broods in which parental investment was experimentally increased showed a lower BCI and lower alkaline phosphatase levels and higher H/L ratios than controls. Conversely, offspring showed the opposite pattern when reproductive expenditure was experimentally decreased. We observed no effects of manipulation of parental investment on triglyceride levels or on survival rates. Although our findings suggest that Blue‐footed Booby parents have the ability to adjust their breeding effort according to the demands of their offspring, parental effort could influence the effect of hatching order by suppressing the aggressive tendency of the senior chick.     

Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica)

In vertebrates, offspring have a relatively inefficient immune system soon after birth. Female birds transmit immunoglobulins to the egg, which can confer protection against parasites to their offspring after hatching, but allocation of immune factors can depend on the reproductive value of the offspring as affected, for example, by the quality of their father. We analyse the variation in immunoglobulin levels of female barn swallows (Hirundo rustica) during the breeding cycle in relation to the expression of a secondary sexual character of their mates. Circulating immunoglobulins peaked on approximately the day before that of laying of their first egg, but postlaying concentration was similar to the concentration well before laying. Immunoglobulin levels per unit volume of plasma were lower for females breeding late compared with those breeding early. Haematocrit of females reached an absolute minimum on the day of laying of the third egg. In males, concentration of immunoglobulins relative to other plasma proteins did not change in relation to the breeding stage. Smaller relative concentrations of immunoglobulins and haematocrit were observed in males breeding late in the season. Immunoglobulin concentration of females was positively correlated with the level of ornamentation of their mates. These results suggest that females alter their immune profile to transmit humoral factors providing immune defence against pathogens to their offspring after hatching. This enhancement of immune protection is larger when the offsprings are of relatively large reproductive value as when sired by high quality males. Alternatively, females with relatively large immunoglobulin concentration preferentially mate with the most ornamented males.     

Field study of the relationship between personality and reproductive strategy in the White-collared Blackbird Turdus albocinctus

The discovery of personality traits in animal populations may help to explain individual variation in breeding strategies. In the White-collared Blackbird Turdus albocinctus, females, but not males, exhibited different nest defence behaviours that can be used to classify them into bold and shy personalities. Bold females had higher nest success, lower fecundity and higher parental investment than shy females, and the social mates of bold females had lower parental investment than that of shy females. Our findings suggest that the reproductive strategy of birds may be closely related to their personality traits.     

Effects of malaria double infection in birds: one plus one is not two

Avian malaria parasites are supposed to exert negative effects on host fitness because these intracellular parasites affect host metabolism. Recent advances in molecular genotyping and microscopy have revealed that coinfections with multiple parasites are frequent in bird-malaria parasite systems. However, studies of the fitness consequences of such double infections are scarce and inconclusive. We tested if the infection with two malaria parasite lineages has more negative effects than single infection using 6 years of data from a natural population of house martins. Survival was negatively affected by both types of infections. We found an additive cost from single to double infection in body condition, but not in reproductive parameters (double-infected had higher reproductive success). These results demonstrate that malaria infections decrease survival, but also have different consequences on the breeding performance of single- and double-infected wild birds.     

Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni)

We studied the consequences of chronic infections by three different lineages of avian malaria, two Plasmodium (RTSR1, LK6) and one Haemoproteus (LK2), on reproductive performance of Lesser Kestrels (Falco naumanni). Malaria infections in male and female parents had no effect on clutch size, hatching success or nesting success. However, when only successful nests were considered, we found that males parasitized by LK6 raised a lower number of fledglings, suggesting that the level of parental effort by males may be limited by this particular lineage of Plasmodium. This effect was not evident in females, probably due to the higher investment of males during the chick rearing period in this species. Overall, we have found that chronic stages of specific malaria lineages have certain negative consequences on host reproductive performance, highlighting the importance of considering genetic differences among malaria parasites to study their consequences on natural bird populations.     

Sex-specific costs of reproduction in Eastern Bluebirds Sialia sialis

In species with bi-parental care, individuals must partition energy between parental effort and mating effort. Typically, female songbirds invest more than males in reproductive activities such as egg-laying and incubation, but males invest more in secondary sexual traits used in attracting mates. Animals that breed more than once within a season must also allocate time and energy between first and subsequent breeding attempts and between current and future breeding seasons. To investigate strategies of reproductive investment by males and females and the consequences of such strategies, we manipulated the size of broods of Eastern Bluebirds Sialia sialis . Pairs with enlarged first broods were less likely to produce a second clutch or took longer to initiate one than pairs with reduced broods. After rearing enlarged broods, females were less likely than males to survive to the following year. Although plumage coloration is a sexually selected trait in Eastern Bluebirds that is influenced by nutritional stress, we did not detect an effect of brood-size manipulation on female coloration. Past research, however, demonstrates that, in males, plumage colour is negatively affected by increasing brood size. We suggest that there are sex-specific strategies of reproductive investment in Eastern Bluebirds, and that researchers should incorporate measures of residual reproductive value in studies of life-history evolution.     

Immune defence,extra-pair paternity,and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.     

The Sicker Sex: Understanding Male Biases in Parasitic Infection,Resource Allocation and Fitness

The “sicker sex” idea summarizes our knowledge of sex biases in parasite burden and immune ability whereby males fare worse than females. The theoretical basis of this is that because males invest more on mating effort than females, the former pay the costs by having a weaker immune system and thus being more susceptible to parasites. Females, conversely, have a greater parental investment. Here we tested the following: a) whether both sexes differ in their ability to defend against parasites using a natural host-parasite system; b) the differences in resource allocation conflict between mating effort and parental investment traits between sexes; and, c) effect of parasitism on survival for both sexes. We used a number of insect damselfly species as study subjects. For (a), we quantified gregarine and mite parasites, and experimentally manipulated gregarine levels in both sexes during adult ontogeny. For (b), first, we manipulated food during adult ontogeny and recorded thoracic fat gain (a proxy of mating effort) and abdominal weight (a proxy of parental investment) in both sexes. Secondly for (b), we manipulated food and gregarine levels in both sexes when adults were about to become sexually mature, and recorded gregarine number. For (c), we infected male and female adults of different ages and measured their survival. Males consistently showed more parasites than females apparently due to an increased resource allocation to fat production in males. Conversely, females invested more on abdominal weight. These differences were independent of how much food/infecting parasites were provided. The cost of this was that males had more parasites and reduced survival than females. Our results provide a resource allocation mechanism for understanding sexual differences in parasite defense as well as survival consequences for each sex.     

Is female investment in defence correlated with breeding success in Hen Harriers Circus cyaneus

CapsuleThe intensity of parental defence, irrespective of the value of offspring, may be one of the proximate causes of breeding success, reflecting the quality of breeders.

Aims To test whether female Hen Harrier investment in defence towards a human predator influences breeding success.

Methods Generalized linear mixed models were used, with nest content, date of visit, the interaction (nest content*date), breeding success (number of fledglings/clutch size) and presence or absence of male as explanatory variables. ‘Female’ was included as a random variable in the model. Alarm call rate by a female Hen Harrier during the first three minutes after my arrival at a nest was used as a dependent variable (as an indicator of parental investment in defence towards a human predator).

Results Females were present and alarmed in 100% of visits whereas males were present in 37% of visits. The individual variations in female investment in defence, after controlling for the principal determinants of nest defence, were significantly correlated with breeding success of each pair.

Conclusion The relationship between female investment in nest defence and reproductive success can be explained through differences in female quality. Good quality females, as measured by the level of investment in nest defence, probably also invested more in other breeding aspects not controlled in this study obtaining higher reproductive success.