Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

A chemical signal of offspring quality affects maternal care in a social insect

Begging signals of offspring are condition-dependent cues that are usually predicted to display information about the short-term need (i.e. hunger) to which parents respond by allocating more food. However, recent models and experiments have revealed that parents, depending on the species and context, may respond to signals of quality (i.e. offspring reproductive value) rather than need. Despite the critical importance of this distinction for life history and conflict resolution theory, there is still limited knowledge of alternative functions of offspring signals. In this study, we investigated the communication between offspring and caring females of the common earwig, Forficula auricularia, hypothesizing that offspring chemical cues display information about nutritional condition to which females respond in terms of maternal food provisioning. Consistent with the prediction for a signal of quality we found that mothers exposed to chemical cues from well-fed nymphs foraged significantly more and allocated food to more nymphs compared with females exposed to solvent (control) or chemical cues from poorly fed nymphs. Chemical analysis revealed significant differences in the relative quantities of specific cuticular hydrocarbon compounds between treatments. To our knowledge, this study demonstrates for the first time that an offspring chemical signal reflects nutritional quality and influences maternal care.     

Spying on your neighbours? Social information affects timing of breeding and stress hormone levels in a colonial seabird

A good overlap between offspring energetic requirements and availability of resources is required for successful reproduction. Accordingly, individuals from numerous species fine-tune their timing of breeding by integrating cues that predict environmental conditions during the offspring period. Besides acquiring information from their direct interaction with the environment (personal information), individuals can integrate information by observing the behaviours or performance of others (social information). The use of social information is often beneficial because the accumulated knowledge of conspecifics may represent a source of information more reliable than the intrinsically more limited personal information. However, although social information constitutes the major source of information in a wide range of contexts, studies investigating its use in the context of timing of breeding are scarce. We investigated whether black-legged kittiwakes (Rissa tridactyla) used social information to adjust the timing of egg-laying. We manipulated social information using a food-supplementation experiment, known to advance kittiwakes' reproductive phenology. We expected food-supplemented and unsupplemented pairs to delay and advance, respectively, their timing of laying when surrounded by a majority of neighbours from the opposite food-treatment. However, both unsupplemented and food-supplemented kittiwakes delayed egg-laying when surrounded by a higher proportion of neighbours from the opposite food-treatment. This result shows that kittiwakes use social information to time egg-laying, but that it is not used to match the seasonal peak of food availability. We suggest that when social and personal cues give contradictory environmental information, individuals may benefit from delaying laying to gather more information to make better decisions about investment into eggs. Further, we explored a potential proximate mechanism for the pattern we report. We show that baseline corticosterone, known to mediate reproductive decisions, was lower in unsupplemented females facing a higher proportion of food-supplemented neighbours. Altogether, our results suggest that to fine-tune their timing of laying, kittiwakes use complex decision-making processes in which social and personal information interplay.

     

Investigating disease severity in an animal model of concurrent babesiosis and Lyme disease

The incidence of babesiosis, Lyme disease and other tick-borne diseases has increased steadily in Europe and North America during the last five decades. Babesia microti is transmitted by species of Ixodes, the same ticks that transmit the Lyme disease-causing spirochete, Borrelia burgdorferi. B. microti can also be transmitted through transfusion of blood products and is the most common transfusion-transmitted infection in the U.S.A. Ixodes ticks are commonly infected with both B. microti and B. burgdorferi, and are competent vectors for transmitting them together into hosts. Few studies have examined the effects of coinfections on humans and they had somewhat contradictory results. One study linked coinfection with B. microti to a greater number of symptoms of overall disease in patients, while another report indicated that B. burgdorferi infection either did not affect babesiosis symptoms or decreased its severity. Mouse models of infection that manifest pathological effects similar to those observed in human babesiosis and Lyme disease offer a unique opportunity to thoroughly investigate the effects of coinfection on the host. Lyme disease has been studied using the susceptible C3H mouse infection model, which can also be used to examine B. microti infection to understand pathological mechanisms of human diseases, both during a single infection and during coinfections. We observed that high B. microti parasitaemia leads to low haemoglobin levels in infected mice, reflecting the anaemia observed in human babesiosis. Similar to humans, B. microti coinfection appears to enhance the severity of Lyme disease-like symptoms in mice. Coinfected mice have lower peak B. microti parasitaemia compared to mice infected with B. microti alone, which may reflect attenuation of babesiosis symptoms reported in some human coinfections. These findings suggest that B. burgdorferi coinfection attenuates parasite growth while B. microti presence exacerbates Lyme disease-like symptoms in mice.     

Social instability in laying quail: consequences on yolk steroids and offspring's phenotype

Individual phenotypic characteristics of many species are influenced by non-genetic maternal effects. Female birds can influence the development of their offspring before birth via the yolk steroid content of their eggs. We investigated this prenatal maternal effect by analysing the influence of laying females' social environment on their eggs' hormonal content and on their offspring's development. Social instability was applied to groups of laying Japanese quail females. We evaluated the impact of this procedure on laying females, on yolk steroid levels and on the general development of chicks. Agonistic interactions were more frequent between females kept in an unstable social environment (unstable females) than between females kept in a stable social environment (stable females). Testosterone concentrations were higher in unstable females' eggs than in those of stable females. Unstable females' chicks hatched later and developed more slowly during their first weeks of life than those of stable females. The emotional reactivity of unstable females' chicks was higher than that of stable females' chicks. In conclusion, our study showed that social instability applied to laying females affected, in a non-genetic way, their offspring's development, thus stressing the fact that females' living conditions during laying can have transgenerational effects.     

Maternal effects in the highly communal sociable weaver may exacerbate brood reduction and prepare offspring for a competitive social environment

Maternal effects can influence offspring phenotype with short- and long-term consequences. Yet, how the social environment may influence egg composition is not well understood. Here, we investigate how laying order and social environment predict maternal effects in the sociable weaver, Philetairus socius, a species that lives in massive communal nests which may be occupied by only a few to 100+ individuals in a single nest. This range of social environments is associated with variation in a number of phenotypic and life-history traits. We investigate whether maternal effects are adjusted accordingly. We found no evidence for the prediction that females might benefit from modifying brood hierarchies through an increased deposition of androgens with laying order. Instead, females appear to exacerbate brood reduction by decreasing the costly production of yolk mass and antioxidants with laying order. Additionally, we found that this effect did not depend on colony size. Finally, in accordance with an expected increased intensity of environmental stress with increasing colony size, we found that yolk androgen concentration increased with colony size. This result suggests that females may enhance the competitive ability of offspring raised in larger colonies, possibly preparing the offspring for a competitive social environment.     

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal

Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.     

Infection before pregnancy affects immunity and response to social challenge in the next generation

Natural selection should favour parents that are able to adjust their offspring's life-history strategy and resource allocation in response to changing environmental and social conditions. Pathogens impose particularly strong and variable selective pressure on host life histories, and parental genes will benefit if offspring are appropriately primed to meet the immunological challenges ahead. Here, we investigated transgenerational immune priming by examining reproductive resource allocation by female mice in response to direct infection with Babesia microti prior to pregnancy. Female mice previously infected with B. microti gained more weight over pregnancy, and spent more time nursing their offspring. These offspring generated an accelerated response to B. microti as adults, clearing the infection sooner and losing less weight as a result of infection. They also showed an altered hormonal response to novel social environments, decreasing instead of increasing testosterone production upon social housing. These results suggest that a dominance-resistance trade-off can be mediated by cues from the previous generation. We suggest that strategic maternal investment in response to an infection leads to increased disease resistance in the following generation. Offspring from previously infected mothers downregulate investment in acquisition of social dominance, which in natural systems would reduce access to mating opportunities. In doing so, however, they avoid the reduced disease resistance associated with increased testosterone and dominance. The benefits of accelerated clearance of infection and reduced weight loss during infection may outweigh costs associated with reduced social dominance in an environment where the risk of disease is high.     

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.     

Nonlinear maternal effects on personality in a rodent species with fluctuating densities

Consistent among individual variation in behavior,or animal personality,is present in a wide variety of species.This behavioral variation is maintained by both genetic and environmental factors.Parental effects are a special case of environmental variation and are expected to evolve in populations experiencing large fluctuations in their environment.They represent a non-genetic pathway by which parents can transmit information to their offspring,by modulating their personality.While it is expected that parental effects contribute to the observed personality variation,this has rarely been studied in wild populations.We used the multimammate mouse Mastomys natalensis as a model system to investigate the potential effects of maternal personality on offspring behavior.We did this by repeatedly recording the behavior of individually housed juveniles which were born and raised in the lab from wild caught females.A linear correlation,between mother and offspring in behavior,would be expected when the personality is only affected by additive genetic variation,while a more complex relationship would suggests the presence of maternal effects.We found that the personality of the mother predicted the behavior of their offspring in a non-linear pattern.Exploration behavior of mother and offspring was positively correlated,but only for slow and average exploring mothers,while this correlation became negative for fast exploring mothers.This may suggests that early maternal effects could affect personality in juvenile M.natalensis,potentially due to density-dependent and negative frequency-dependent mechanisms,and therefore contribute to the maintenance of personality variation.     

Sex roles in nest keeping – how information asymmetry contributes to parent‐offspring co‐adaptation

Parental food provisioning and offspring begging influence each other reciprocally. This makes both traits agents and targets of selection, which may ultimately lead to co‐adaptation. The latter may reflect co‐adapted parent and offspring genotypes or could be due to maternal effects. Maternal effects are in turn likely to facilitate in particular mother‐offspring co‐adaptation, further emphasized by the possibility that mothers are sometimes found to be more responsive to offspring need. However, parents may not only differ in their sensitivity, but often play different roles in postnatal care. This potentially impinges on the access to information about offspring need. We here manipulated the information on offspring need as perceived by parents by playing back begging calls at a constant frequency in the nest‐box of blue tits (Cyanistes caeruleus). We measured the parental response in provisioning to our treatment, paying particular attention to sex differences in parental roles and whether such differences alter the perception of the intensity of our manipulation. This enabled us to investigate whether an information asymmetry about offspring need exists between parents and how such an asymmetry relates to co‐adaptation between parental provisioning and offspring begging. Our results show that parents indeed differed in the frequency how often they perceived the playback due to the fact that females spent more time with their offspring in the nest box. Correcting for the effective exposure of an adult to the playback, the parental response in provisioning covaried more strongly (positive) with offspring begging intensity, independent of the parental sex, indicating coadaptation on the phenotypic level. Females were not more sensitive to experimentally increased offspring need than males, but they were exposed to more broadcasted begging calls. Therefore, sex differences in access to information about offspring need, due to different parental roles, have the potential to impinge on family conflicts and their resolution.     

Borrelia burgdorferi Promotes the Establishment of Babesia microti in the Northeastern United States

Babesia microti and Borrelia burgdorferi, the respective causative agents of human babesiosis and Lyme disease, are maintained in their enzootic cycles by the blacklegged tick (Ixodes scapularis) and use the white-footed mouse (Peromyscus leucopus) as primary reservoir host. The geographic range of both pathogens has expanded in the United States, but the spread of babesiosis has lagged behind that of Lyme disease. Several studies have estimated the basic reproduction number (R ₀) for B. microti to be below the threshold for persistence (<1), a finding that is inconsistent with the persistence and geographic expansion of this pathogen. We tested the hypothesis that host coinfection with B. burgdorferi increases the likelihood of B. microti transmission and establishment in new areas. We fed I. scapularis larva on P. leucopus mice that had been infected in the laboratory with B. microti and/or B. burgdorferi. We observed that coinfection in mice increases the frequency of B. microti infected ticks. To identify the ecological variables that would increase the probability of B. microti establishment in the field, we integrated our laboratory data with field data on tick burden and feeding activity in an R ₀ model. Our model predicts that high prevalence of B. burgdorferi infected mice lowers the ecological threshold for B. microti establishment, especially at sites where larval burden on P. leucopus is lower and where larvae feed simultaneously or soon after nymphs infect mice, when most of the transmission enhancement due to coinfection occurs. Our studies suggest that B. burgdorferi contributes to the emergence and expansion of B. microti and provides a model to predict the ecological factors that are sufficient for emergence of B. microti in the wild.     

Mother knows best,even when stressed? Effects of maternal exposure to a stressor on offspring performance at different life stages in a wild semelparous fish

The environment mothers are exposed to has resonating effects on offspring performance. In iteroparous species, maternal exposure to stressors generally results in offspring ill-equipped for survival. Still, opportunities for future fecundity can offset low quality offspring. Little is known, however, as to how intergenerational effects of stress manifest in semelparous species with only a single breeding episode. Such mothers would suffer a total loss of fitness if offspring cannot survive past multiple life stages. We evaluated whether chronic exposure of female sockeye salmon (Oncorhynchus nerka) to a chase stressor impaired offspring performance traits. Egg size and early offspring survival were not influenced by maternal exposure to the repeated acute stressor. Later in development, fry reared from stressed mothers swam for shorter periods of time but possessed a superior capacity to re-initiate bouts of burst swimming. In contrast to iteroparous species, the mechanisms driving the observed effects do not appear to be related to cortisol, as egg hormone concentrations did not vary between stressed and undisturbed mothers. Sockeye salmon appear to possess buffering strategies that protect offspring from deleterious effects of maternal stress that would otherwise compromise progeny during highly vulnerable stages of development. Whether stressed sockeye salmon mothers endow offspring with traits that are matched or mismatched for survival in the unpredictable environment they encountered is discussed. This study highlights the importance of examining intergenerational effects among species-specific reproductive strategies, and across offspring life history to fully determine the scope of impact of maternal stress.     

Maternal antibodies contribute to sex-based difference in hantavirus transmission dynamics

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole (Myodes glareolus). Populations were founded with either females or males that were infected with PUUV, whereas the other sex was immunized against PUUV infection. The likelihood of the next generation being infected was lower when the infected founders were females, underlying the putative importance of adult males in PUUV transmission and persistence in host populations. However, we show that this effect probably results from transient immunity that infected females provide to their offspring, rather than any sex-biased transmission efficiency per se. Our study proposes a potential contrasting nature of female and male hosts in the transmission dynamics of hantaviruses.     

Do gravid females become selfish? Female allocation of energy during gestation

Net energy availability depends on plasma corticosterone concentrations, food availability, and their interaction. Limited net energy availability requires energy trade-offs between self-maintenance and reproduction. This is important in matrotrophic viviparous animals because they provide large amounts of energy for embryos, as well as self-maintenance, for the extended period of time during gestation. In addition, gravid females may transmit environmental information to the embryos in order to adjust offspring phenotype. We investigated effects of variation in maternal plasma corticosterone concentration and maternal food availability (2 × 2 factorial design) during gestation on offspring phenotype in a matrotrophic viviparous lizard (Pseudemoia entrecasteauxii). Subsequently, we tested preadaptation of offspring phenotype to their postnatal environment by measuring risk-averse behavior and growth rate using reciprocal transplant experiments. We found that maternal net energy availability affected postpartum maternal body condition, offspring snout-vent length, offspring mass, offspring performance ability, and offspring fat reserves. Females treated with corticosterone allocated large amounts of energy to their own body condition, and their embryos allocated more energy to energy reserves than somatic growth. Further, offspring from females in high plasma corticosterone concentration showed compensatory growth. These findings suggest that while females may be selfish when gestation conditions are stressful, the embryos may adjust their phenotype to cope with the postnatal environment.     

Trans-Generational Influence of Human Disturbances in Japanese Quail: Egg Quality Influences Male Social and Sexual Behaviour

In many bird species prenatal exposure to yolk androgens of maternal origin has been found to influence offspring behavioural phenotype. In contrast to altricial birds, far less is known about maternal effects in precocial birds. In a previous experiment we found that female quail ( Coturnix japonica ) that were not previously habituated to humans (NH) produced eggs with less androgens (testosterone, androstenedione) and more progesterone when exposed to human disturbances than females habituated to humans (H). Here, we analysed social motivation and sexual behaviour of the male offspring of NH and H females. Classical behavioural test procedures were applied including separation, runway, partner choice and female encounter tests. As chicks, offspring of the NH females spent more time far from conspecifics than offspring of the H females. As adults, the same NH males showed less crowing and courtship behaviour (ritual preening) in female encounter tests than H males. Thus, maternal environment and egg quality may be key factors in the emergence of individual variability of appetitive behaviour, such as social proximity and courtship behaviour. Human disturbance of the mother seems to have triggered trans-generational effects resulting in consistently reduced social and sexual motivation in offspring until adulthood.     

Embryonic programming of heart disease in response to obesity during pregnancy

Obesity during pregnancy programs adult-onset heart disease in the offspring. Clinical studies indicate that exposure to an adverse environment in utero during early, as compared to late, gestation leads to a higher prevalence of adult-onset heart disease. This suggests that the early developing heart is particularly sensitive to an adverse environment. Accordingly, growing evidence from clinical studies and animal models demonstrates that obesity during pregnancy alters the function of the fetal heart, programming a higher risk of cardiovascular disease later in life. Moreover, gene expression patterns and signaling pathways that promote initiation and progression of cardiovascular disease are altered in the hearts in offspring born to obese mothers. However, the mechanisms mediating the long-term effects of an adverse environment in utero on the developing heart leading to adult-onset disease are not clear. Here, we review clinical and experimental evidence documenting the effects of maternal obesity during pregnancy on the fetal and post-natal heart and emphasize on the potential mechanisms of disease programming.     

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.     

Do maternal food deprivation and offspring predator cues interactively affect maternal effort in fish?

The state of the environment parents are exposed to during reproduction can either facilitate or impair their ability to take care of their young. Thus, the environmental conditions experienced by parents can have a transgenerational impact on offspring phenotype and survival. Parental energetic needs and the variance in offspring predation risk have both been recognized as important factors influencing the quality and amount of parental care, but surprisingly, they are rarely manipulated simultaneously to investigate how parents adjust care to these potentially conflicting demands. In the maternally mouthbrooding cichlid Simochromis pleurospilus, we manipulated female body condition before spawning and exposure to offspring predator cues during brood care in a two‐by‐two factorial experiment. Subsequently, we measured the duration of brood care and the number and size of the released young. Furthermore, we stimulated females to take up their young by staged predator attacks and recorded the time before the young were released again. We found that food‐deprived females produced smaller young and engaged less in brood care behaviour than well‐nourished females. Final brood size and, related to this, female protective behaviour were interactively determined by nutritional state and predator exposure: well‐nourished females without a predator encounter had smaller broods than all other females and at the same time were least likely to take up their young after a simulated predator attack. We discuss several mechanisms by which predator exposure and maternal nutrition might have influenced brood and offspring size. Our results highlight the importance to investigate the selective forces on parents and offspring in combination, if we aim to understand reproductive strategies.