A parasite-induced maternal effect can reduce survival times of fleas feeding on great tit nestlings

Parents can increase their reproductive success by assisting their neonate offspring in parasite defence. In birds, parental tactics include post-hatching parental responses such as increased parental care and pre-hatching maternal effects such as the transfer of maternal antibodies via the egg. These parasite-induced parental responses are known to reduce the effects of parasites on offspring, but their costs for the parasite are largely unknown. In two separate experiments on great tits Parus major we assessed these costs for hen fleas Ceratophyllus gallinae . Half of the parents where exposed to fleas during egg-laying to induce the parental response, while control nests were left flea-free. In experiment 1 parents raised their own young and we measured the effect of combined pre- and post-hatching parental effects, while in experiment 2 a cross-foster design allowed us to assess the effects of pre-hatching maternal effects alone. In both experiments we let fleas take a blood meal on nestlings from either flea-exposed or unexposed parents. We then measured flea-feeding duration, the quantity of extracted blood, and the fleas' subsequent survival time. We found in both experiments that on the largest nestlings of a brood flea survival was significantly reduced by the parental effects, whereas on the smaller nestlings it was independent of parental effects. The pre- and post-hatching parental responses did neither affect duration nor size of a flea blood meal. These results suggest first that the pre-hatching maternal effects, i.e. the substances transferred to the nestling via the egg, have the potential to harm fleas without reducing flea feeding capacity, and second that the strength of the maternal response varies between the nestlings, either because maternal products are unequally distributed among eggs within a clutch, or because large nestlings can build up a response that enhances the effect of the maternal products.     

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.     

Influence of maternal infection on offspring resistance towards parasites

Immunoglobulins, parasite circulating antigens, immune cells, cytokines and other cell-related products can be transferred from infected mothers to their young. They can combine their effects to interact with the invading parasites, as well as to induce a long-term modulation of the offspring's capacity to mount an immune response to subsequent exposure to parasites. The protective effect of maternally derived antibodies may be limited by the selective transfer of immunoglobulin isotypes. Maternal antibodies may also prevent the priming of specific cells in offspring or inhibit the progeny's antibody production by interacting with B-cell receptors or with the idiotypic repertoire. The potentially beneficial priming effect of transferred parasitic antigens may be altered by the Th2-cell-biased foetal environment and such antigens may also induce deletion or anergy of T- and B-cell clones in offspring. Therefore, besides protective effects, maternal infection may downregulate the offspring's immune response. If such hyporesponsiveness may be clearly harmful (in increasing the risk or in worsening congenital or postnatally acquired infections in offspring), it can also be beneficial (in limiting the pathogenesis of some infections). Here, Yves Carlier and Carine Truyens review the rationale of these complex foeto-maternal relationships in parasitic diseases.     

Parental guidance? Trans-generational influences on offspring life history in mosquitoes

Parental effects are important factors that might influence evolutionary and ecological aspects of parasite vectors and the parasites they transmit. A recent study demonstrated the importance of parental rearing conditions on the malaria vector Anopheles stephensi. When parents are reared in a food-limited environment their offspring have increased bloodmeal sizes and larger clutches. The study highlights that ecological studies are vital for understanding vectors of disease and ultimately for developing effective control strategies.     

The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents

Understanding the selective pressures shaping the number of offspring per breeding event is a key area in the study of life-history strategies. However, in species with parental care, costs incurred in offspring production, rather than rearing, have been largely ignored in both theoretical and empirical studies until relatively recently. Furthermore, the few experimental studies that have manipulated production costs have not yet teased apart effects that operate via the parental phenotype from effects on the quality of the resulting young. To examine whether increased egg production influences parental brood rearing capacity independently of effects operating via egg quality, we experimentally increased egg production in gulls and then examined their capacity to rear a control clutch. We found that the capacity of parents to rear the control brood was substantially reduced solely as a consequence of having themselves produced one extra egg. The paradox that, in many species, parents apparently aim for fewer young per breeding event than the experimentally and theoretically demonstrated optimum, has partly arisen from the failure to take into account the constraints imposed by production costs.     

Maternal Aggression and Litter Size in the Female House Mouse

It has been commonly argued that, in house mice, female post-partum fighting against a male intruder functions to protect the offspring from infanticide. The aim of this study was to test the hypothesis that maternal aggression is actually related to pup defence and, specifically, according to parental investment theory, that its intensity should increase with litter size. 60 nulliparous albino female mice were mated and randomly assigned to four experimental groups in which litters were culled at birth to 0, 4, 8, or 12 pups, respectively. On day 8 after delivery all females were tested for maternal aggression against a stranger adult male conspecific (5-min exposure). No aggression occurred in the group in which all pups had been removed. In the other groups, the proportion of females displaying overt aggression increased with litter size. Several scores of female agonistic behaviour (proportion of females displaying overt aggression, total attacking time, frequency of tail rattling) were significantly higher for the females rearing 8 and 12 pups than for the females rearing 4 pups. Aggressive behaviour of females rearing 12 pups was not significantly higher than that of females rearing 8 pups. No male committed infanticide. These results support the hypothesis that rodent maternal aggression is strictly related to offspring defence and are consistent with the theoretical prediction that, the costs of the defence being equal and the gain in fitness increasing with litter size, the intensity of maternal defence of the young should increase with their number.     

Exploring the Relation of Harsh Parental Discipline with Child Emotional and Behavioral Problems by Using Multiple Informants. The Generation R Study

Parental harsh disciplining, like corporal punishment, has consistently been associated with adverse mental health outcomes in children. It remains a challenge to accurately assess the consequences of harsh discipline, as researchers and clinicians generally rely on parent report of young children''s problem behaviors. If parents rate their parenting styles and their child''s behavior this may bias results. The use of child self-report on problem behaviors is not common but may provide extra information about the relation of harsh parental discipline and problem behavior. We examined the independent contribution of young children''s self-report above parental report of emotional and behavioral problems in a study of maternal and paternal harsh discipline in a birth cohort. Maternal and paternal harsh discipline predicted both parent reported behavioral and parent reported emotional problems, but only child reported behavioral problems. Associations were not explained by pre-existing behavioral problems at age 3. Importantly, the association with child reported outcomes was independent from parent reported problem behavior. These results suggest that young children''s self-reports of behavioral problems provide unique information on the effects of harsh parental discipline. Inclusion of child self-reports can therefore help estimate the effects of harsh parental discipline more accurately.     

Modeling the ecology of symbiont-mediated protection against parasites

There is increasing evidence that many maternally transmitted symbionts protect their hosts against parasites, thus ensuring their own persistence. Despite the protection they provide, such symbionts are typically found in only a fraction of the host population. This suggests that symbiont-conferred resistance is costly or that the maternal inheritance of symbionts is not perfect. To investigate these hypotheses and other properties of this complex ecological system, we develop a mathematical model based on the example of bacterial endosymbionts that protect aphids against parasitoid wasps. Simulations show that in the absence of more complex effects, a very fine balance between the costs of harboring symbionts and the strength of protection they provide is required to maintain coexistence of protected and unprotected hosts. These constraints are significantly relaxed and coexistence becomes a common outcome if deployment of symbiont-provided defenses upon a parasite attack entails an additional (induced) cost. Transmission rates of symbionts also affect coexistence, which is more frequently observed under high (but not perfect) fidelity of vertical transfer and low rates of horizontal transfer. Finally, we show that the prevalence of defensive symbionts has a strong influence on the population dynamics of hosts and parasites: population sizes are stable if and only if protected hosts dominate.     

Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus).

The Hamilton and Zuk hypothesis on haemoparasite-mediated sexual selection and certain studies of reproductive costs are based on the assumption that avian blood parasite infections are detrimental to their hosts. However, there is no experimental evidence demonstrating harmful effects of blood parasites on fitness in wild populations, it even having been suggested that they may be non-pathogenic. Only an experimental manipulation of natural blood parasite loads may reveal their harmful effects. In this field experiment we reduced through medication the intensity of infection by Haemoproteus majoris and the prevalence of infection by Leucocytoazoon majoris in blue tits (Parus caeruleus), and demonstrated detrimental effects of natural levels of infection by these common parasite species on host reproductive success and condition. The fact that some of the costs of infection were paid by offspring indicates that blood parasites reduce parental working capacity while feeding nestlings. Medicated females may be able to devote more resources to parental care through being released from the drain imposed upon them by parasites and/or through a reduced allocation to an immune response. Therefore, this work adds support to previous findings relating hosts' life-history traits and haematozoan infections.     

Drug treatment of malaria infections can reduce levels of protection transferred to offspring via maternal immunity

Maternally transferred immunity can have a fundamental effect on the ability of offspring to deal with infection. However, levels of antibodies in adults can vary both quantitatively and qualitatively between individuals and during the course of infection. How infection dynamics and their modification by drug treatment might affect the protection transferred to offspring remains poorly understood. Using the rodent malaria parasite Plasmodium chabaudi, we demonstrate that curing dams part way through infection prior to pregnancy can alter their immune response, with major consequences for offspring health and survival. In untreated maternal infections, maternally transferred protection suppressed parasitaemia and reduced pup mortality by 75 per cent compared with pups from naïve dams. However, when dams were treated with anti-malarial drugs, pups received fewer maternal antibodies, parasitaemia was only marginally suppressed, and mortality risk was 25 per cent higher than for pups from dams with full infections. We observed the same qualitative patterns across three different host strains and two parasite genotypes. This study reveals the role that within-host infection dynamics play in the fitness consequences of maternally transferred immunity. Furthermore, it highlights a potential trade-off between the health of mothers and offspring suggesting that anti-parasite treatment may significantly affect the outcome of infection in newborns.     

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.     

Low survival of parasite chicks may result from their imperfect adaptation to hosts rather than expression of defenses against parasitism

Host parents exhibit a variety of behaviors toward avian brood parasites, but not all of their actions have necessarily evolved in response to costs imposed by parasites. To investigate whether common waxbills (Estrilda astrild) have evolved defenses specifically against parasitic pin-tailed whydahs (Vidua macroura), I studied the specificity and flexibility of host behaviors toward nestlings at two sites that differed significantly in parasitism rates and intensities. I focused on documenting nestling survival because V. macroura young match the elaborate gape morphology of E. astrild nestlings, a pattern that suggests hosts may possess unique defenses against parasite chicks. Parasite young survived significantly worse than host young in mixed broods. However, this apparent discrimination was not associated with parasitism risk as would be expected if defenses had evolved specifically to counter parasitism. Parasite young may have survived poorly compared to host young because individual chicks were less able to stimulate sufficient care from foster parents or because they were more susceptible to nestling competition, disease, or reduced provisioning by hosts. Mortality may have also been exacerbated by poor timing of parasite egg laying. In nonparasitized and parasitized nests, rates of nestling survival were similar, further suggesting that parenting behaviors that result in chick mortality did not evolve solely in response to parasite young. In addition, orange-breasted waxbills (Amandava subflava) and zebra finches (Taeniopygia guttata), rarely parasitized and nonparasitized relatives of E. astrild, experience similar levels of nestling mortality presumably as a result of phylogenetically widespread parenting strategies. Despite the similarity of parasitic V. macroura nestlings and E. astrild nestlings, I found no evidence that E. astrild parents possess defenses that allow for specific discrimination against parasite chicks during the nestling period. Rather than being subject to host defenses evolved in an arms race, Vidua chicks may simply be imperfectly adapted to life in the nests of their hosts.     

Reproductive investment and parasite susceptibility in the Great Tit

1. Reproduction and parasite defence are assumed to be costly activities for hosts, and therefore trade-offs might exist between reproduction and parasite defence.
2. Brood sizes were manipulated in a population of Great Tits ( Parus major L.) to assess trade-offs between reproduction and parasite defence. Blood samples were taken from males and females during the late nestling phase, and parasite prevalence was compared among parents raising enlarged, reduced and control broods.
3. A higher prevalence of protozoan blood parasites dominated by Haemoproteus majoris was found among parents with enlarged broods, as compared with parents with control and reduced broods, respectively. Brood size manipulation did not affect parasite prevalence between the sexes or between age classes differently.
4. Mean parasite intensity (number of parasites per microscope field) among adult birds only infected with H. majoris was higher for parents with experimentally enlarged broods than controls and reduced broods, respectively.
5. These results support the hypothesis of a trade-off between parasite defence and reproduction.     

Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides

1.  A key component of parental care involves defending resources destined for offspring from a diverse array of potential interspecific competitors, such as social parasites, fungi and bacteria.
2.  Just as with other aspects of parental care, such as offspring provisioning or brood defence, sexual conflict between parents may arise over how to share the costs of this form of care. There has been little previous work, however, to investigate how this particular burden might be shared.
3.  Here, we describe a hitherto uncharacterized form of parental care in burying beetles Nicrophorus vespilloides , a species which prepares carrion for its young and faces competition from microbes for this resource. We found that parents defend the carcass with antibacterial anal exudates, and that the antibacterial activity of these exudates is only upregulated following the discovery of a corpse. At the same time, phenoloxidase activity in the anal exudates is downregulated, indicating parallels with the internal insect immune system.
4.  In unmanipulated breeding pairs, females had higher antibacterial activity in their anal exudates than males, suggesting sex-specific roles in this aspect of parental care.
5.  When we experimentally widowed males, we found that they increased levels of antibacterial activity in their anal exudates. Experimentally widowing females, however, led them to decrease levels of antibacterial activity in their anal exudates. Widowed beetles of each sex thus produced anal exudates of comparable antibacterial activity. We suggest that this flexible division of antibacterial activity may be coordinated by Juvenile Hormone.     

Innate development of acoustic signals for host parent–offspring recognition in the brood‐parasitic Screaming Cowbird Molothrus rufoaxillaris

Young birds communicate their need to parents through complex begging displays that include visual and acoustic cues. Nestlings of interspecific brood parasites must ‘tune’ into these communication channels to secure parental care from their hosts. Various studies show that parasitic nestlings can effectively manipulate host parental behaviour through their begging calls, but how these manipulative acoustic signals develop in growing parasites remains poorly understood. We investigated the influence of social experience on begging call development in a host‐specialist brood parasite, the Screaming Cowbird Molothrus rufoaxillaris. Screaming Cowbird nestlings look and sound similar to those of the primary host, the Greyish Baywing Agelaioides badius. This resemblance is likely to be adaptive because Baywings discriminate against fledglings unlike their own and provision nests at higher rates in response to Baywing‐like begging calls than to non‐mimetic begging calls. By means of cross‐fostering and playback experiments, we tested whether the acoustic cues that elicit recognition by Baywings develop innately in Screaming Cowbird nestlings or are acquired through social experience with host parents or nest mates. Our results suggest that begging call structure was partially modulated by experience because Baywing‐reared Screaming Cowbird and host nestlings were acoustically more similar as age increased, whereas acoustic similarity between cross‐fostered and Baywing‐reared Screaming Cowbird nestlings decreased from 4–5 to 8–10 days of age. Cross‐fostered Screaming Cowbirds developed begging calls of lower minimum frequency and broader bandwidth than those of Baywing‐reared Screaming Cowbirds by the age of 8–10 days. Despite the observed differences in begging call structure, however, adult Baywings responded similarly to begging calls of 8‐ to 10‐day‐old cross‐fostered and Baywing‐reared Screaming Cowbirds, suggesting that these were functionally equivalent from the host's perspective. These findings support the idea that, although rearing environment can influence certain begging call parameters, the acoustic cues that serve for offspring recognition by Baywings develop in young Screaming Cowbirds independently of social experience.     

Brood size and immunity costs in zebra finches Taeniopygia guttata

Birds rearing experimentally enlarged broods have lower antibody responses to a novel antigen, and we tested three hypotheses that could explain this result. We used zebra finches Taeniopygia guttata inoculated with sheep red blood cells (SRBC) as a study system, for which this trade-off was previously demonstrated. 1. Compensatory cellular immunity: The humoral immune response is slow, and removal of SRBC through up-regulated cellular immunity could pre-empt an antibody response. However, cellular immune response to PHA decreased with increasing brood size, allowing rejection of this hypothesis. 2. Costs of antibody-production: Chicks in large broods grow less well, and birds with large broods may allocate resources to chicks instead of antibodies when these are costly. Compared to saline controls, SRBC suppressed metabolic rate in the hours following immunisation, but there was no effect in the following night, or at any time 4 and 8 days later. Fitness costs were measured by repeatedly immunising parents with SRBC while rearing young. Chick growth, parental condition, and subsequent reproduction of the parents were not affected by SRBC. We conclude that the costs of antibody formation cannot explain the trade-off between brood size and antibody responsiveness. 3. Costs of immune system maintenance: Maintaining a system enabling antibody-formation may be very costly, and birds rearing large broods may have down-regulated this system. Based on this hypothesis we predicted that antibody formation would still be reduced in parents rearing large broods when immunised after rearing the chicks. Our results confirmed this prediction, and we suggest that birds rearing large broods have lower antibody responses because they economised on the maintenance costs of the immune system.     

The role of the 19-kDa region of merozoite surface protein 1 and whole-parasite-specific maternal antibodies in directing neonatal pups' responses to rodent malaria infection

Maternal Abs generated as a result of prior exposure to infectious agents such as the malaria parasite are transferred from the mother through the placenta to the fetus. Numerous studies have attributed the resistance to malaria infection observed in neonates and infants up to 6 mo of age to the presence of maternally derived Abs. However, recent studies have produced conflicting results suggesting that alternative protective mechanisms may be responsible. Although the presence of maternally derived Abs in the infant is not disputed, their exact role in the infant is unknown. Even less clear is the effect that maternally derived Abs, if generated in response to vaccination, may have on the infant's ability to respond to malaria infection. Studies on mouse pups were performed to determine the role of the 19-kDa region of merozoite surface protein 1 (MSP1(19)) and Plasmodium yoelii-specific Abs in neonatal malaria infection and to examine their effect on the development of a specific immune response in the pup. It was shown that P. yoelii- and MSP1(19)-specific Abs transferred to the pup from the mother act to suppress the growth of the parasite in the pup. However, the maternally derived Abs interfered with the development of the pups' own Ab response to the parasite by altering the fine specificity of the response. These results suggest that immunizing women of child-bearing age with a malaria vaccine candidate such as MSP1(19) would not prevent the infant from producing Abs in response to malaria infection, but it may affect the region of the Ag to which it responds.     

Food-sharing in cotton-top tamarins (Saguinus oedipus)

Food-sharing behaviour was observed in 9 captive families of cotton-top tamarins (range 4-14 individuals per group), during meals of fresh fruit. Food was transferred to infants by their parents and older sibs in response to begging, and was also offered to them without prior solicitation. Older, mature, reproductively suppressed individuals shared more than young immature monkeys. Infants in larger families received more food than those in smaller ones, though individuals in smaller families shared more. Transfer to infants increased to a maximum at 12 weeks of age and then declined gradually. At one year of age they no longer received food from others. Food sharing by older siblings is a form of helping behaviour which may increase their inclusive fitness, and benefit parents, both directly, by reducing the costs they incur in rearing young, and indirectly, by increasing the amount of food available to infants.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Induced responses of nestling great tits reduce hen flea reproduction

The dynamics of host–parasite interactions depend to a large extent on the effect of host responses on parasite fitness. Exposure to parasites may induce behavioural or physiological responses in hosts that may reduce the subsequent survival or reproductive output of the parasite. Neonate hosts may further directly obtain immunologically active substances from their mother, for instance via milk in mammals or egg yolk in birds. However, the relative importance of maternally‐derived and self‐generated responses in inducing parasite resistance is poorly understood, especially in free‐living vertebrates. Here we investigate the complementary effect of experimentally induced maternal and neonate responses in great tit (Parus major) hosts on the reproductive success of their common ectoparasite, the hen flea (Ceratophyllus gallinae). In the laboratory we measured the number of eggs and larvae produced by individual flea females collected from host nests. In addition, the total number of larvae produced by an experimentally set number of flea females in the host's nestbox was assessed under field conditions. There was no indication of maternally‐transferred parasite resistance, since exposing the mother to fleas during the laying period did not affect the reproductive rate of fleas exploiting her offspring early or late in the nestling cycle. Independent of the maternal treatment, exposure of neonates to fleas early in the nestling period reduced the reproductive output of fleas late in the nestling cycle. The effect of the induced nestling response was seasonal, reducing flea reproduction in nests of early‐breeding hosts but not in nests of late‐breeding ones. Larvae production in the nestbox and in the laboratory was positively correlated, but under natural conditions the neonate response did not affect the size of the flea larvae population. Our results indicate induced responses as a means by which neonate avian hosts resist ectoparasites. Other factors, such as the environmental temperature and density‐dependent larval competition, may be more important in determining the size of the future parasite populations.