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.     

A mother’s legacy: the strength of maternal effects in animal populations

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such ‘maternal effects’ are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.     

Viviparous mothers impose stronger glucocorticoid‐mediated maternal stress effects on their offspring than oviparous mothers

Maternal stress during gestation has the potential to affect offspring development via changes in maternal physiology, such as increases in circulating levels of glucocorticoid hormones that are typical after exposure to a stressor. While the effects of elevated maternal glucocorticoids on offspring phenotype (i.e., “glucocorticoid‐mediated maternal effects”) have been relatively well established in laboratory studies, it remains poorly understood how strong and consistent such effects are in natural populations. Using a meta‐analysis of studies of wild mammals, birds, and reptiles, we investigate the evidence for effects of elevated maternal glucocorticoids on offspring phenotype and investigate key moderators that might influence the strength and direction of these effects. In particular, we investigate the potential importance of reproductive mode (viviparity vs. oviparity). We show that glucocorticoid‐mediated maternal effects are stronger, and likely more deleterious, in mammals and viviparous squamate reptiles compared with birds, turtles, and oviparous squamates. No other moderators (timing and type of manipulation, age at offspring measurement, or type of trait measured) were significant predictors of the strength or direction of the phenotypic effects on offspring. These results provide evidence that the evolution of a prolonged physiological association between embryo and mother sets the stage for maladaptive, or adaptive, prenatal stress effects in vertebrates driven by glucocorticoid elevation.     

A novel larval diet interacts with nutritional stress to modify juvenile behaviors and glucocorticoid responses

Developmental plasticity can allow the exploitation of alternative diets. While such flexibility during early life is often adaptive, it can leave a legacy in later life that alters the overall health and fitness of an individual. Species of the spadefoot toad genus Spea are uniquely poised to address such carryover effects because their larvae can consume drastically different diets: their ancestral diet of detritus or a derived shrimp diet. Here, we use Spea bombifrons to assess the effects of developmental plasticity in response to larval diet type and nutritional stress on juvenile behaviors and stress axis reactivity. We find that, in an open‐field assay, juveniles fed shrimp as larvae have longer latencies to move, avoid prey items more often, and have poorer prey‐capture abilities. While juveniles fed shrimp as larvae are more exploratory, this effect disappears if they also experienced a temporary nutritional stressor during early life. The larval shrimp diet additionally impairs juvenile jumping performance. Finally, larvae that were fed shrimp under normal nutritional conditions produce juveniles with higher overall glucocorticoid levels, and larvae that were fed shrimp and experienced a temporary nutritional stressor produce juveniles with higher stress‐induced glucocorticoid levels. Thus, while it has been demonstrated that consuming the novel, alternative diet can be adaptive for larvae in nature, doing so has marked effects on juvenile phenotypes that may recalibrate an individual''s overall fitness. Given that organisms often utilize diverse diets in nature, our study underscores the importance of considering how diet type interacts with early‐life nutritional adversity to influence subsequent life stages.     

Is sexual dimorphism affected by the combined action of prenatal stress and sex ratio?

During embryonic development, offspring are exposed to hormones of both maternal and sibling origin. Maternal stress increases offspring exposure to corticosterone, and, in polytocous animals, the sex ratio or intrauterine position can influence the levels of androgens and estrogens experienced by the offspring. Such hormone exposure has the potential to influence many important morphological and behavioural aspects of offspring, in particular sexually dimorphic traits. Although well known in rodents, the impact of prenatal hormone exposure in other vertebrates is poorly documented. We experimentally investigated the relationship between maternal stress, population density, sex ratio (a surrogate for the degree of exposure to steroids produced by siblings), and sexual dimorphism in a viviparous lizard, Lacerta vivipara. Our results show that prenatal sex ratios have consequences for sexually dimorphic morphology (ventral scale count) in both sexes, but with no effect of maternal stress or any interaction between the two. Embryonic steroid exposure can potentially be an important factor in generating individual variation in natural populations of viviparous animals.     

Maternal diet affects juvenile Carpetan rock lizard performance and personality

Differences in both stable and labile state variables are known to affect the emergence and maintenance of consistent interindividual behavioral variation (animal personality or behavioral syndrome), especially when experienced early in life. Variation in environmental conditions experienced by gestating mothers (viz. nongenetic maternal effects) is known to have significant impact on offspring condition and behavior; yet, their effect on behavioral consistency is not clear. Here, by applying an orthogonal experimental design, we aimed to study whether increased vitamin D₃ content in maternal diet during gestation (vitamin‐supplemented vs. vitamin control treatments) combined with corticosterone treatment (corticosterone‐treated vs. corticosterone control treatments) applied on freshly hatched juveniles had an effect on individual state and behavioral consistency of juvenile Carpetan rock lizards (Iberolacerta cyreni). We tested the effect of our treatments on (a) climbing speed and the following levels of behavioral variation, (b) strength of animal personality (behavioral repeatability), (c) behavioral type (individual mean behavior), and (d) behavioral predictability (within‐individual behavioral variation unrelated to environmental change). We found higher locomotor performance of juveniles from the vitamin‐supplemented group (42.4% increase), irrespective of corticosterone treatment. While activity personality was present in all treatments, shelter use personality was present only in the vitamin‐supplemented × corticosterone‐treated treatment and risk‐taking personality was present in corticosterone control treatments. Contrary to our expectations, behavioral type was not affected by our treatments, indicating that individual quality can affect behavioral strategies without affecting group‐level mean behavior. Behavioral predictability decreased in individuals with low climbing speed, which could be interpreted as a form of antipredator strategy. Our results clearly demonstrate that maternal diet and corticosterone treatment have the potential to induce or hamper between‐individual variation in different components of boldness, often in interactions.     

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.     

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.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Early life maternal sociality predicts juvenile sociality in blue monkeys

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.     

Contrasting the Effects of Maternal and Behavioral Characteristics on Fawn Birth Mass in White-Tailed Deer

Maternal care influences offspring quality and can improve a mother’s inclusive fitness. However, improved fitness may only occur when offspring quality (i.e., offspring birth mass) persists throughout life and enhances survival and/or reproductive success. Although maternal body mass, age, and social rank have been shown to influence offspring birth mass, the inter-dependence among these variables makes identifying causation problematic. We established that fawn birth mass was related to adult body mass for captive male and female white-tailed deer (Odocoileus virginianus), thus maternal care should improve offspring fitness. We then used path analysis to identify which maternal characteristic(s) most influenced fawn birth mass of captive female white-tailed deer. Maternal age, body mass and social rank had varying effects on fawn birth mass. Maternal body mass displayed the strongest direct effect on fawn birth mass, followed by maternal age and social rank. Maternal body mass had a greater effect on social rank than age. The direct path between social rank and fawn birth mass may indicate dominance as an underlying mechanism. Our results suggest that heavier mothers could use dominance to improve access to resources, resulting in increased fitness through production of heavier offspring.     

Maternal food quantity affects offspring feeding rate in Daphnia magna

Maternal effects have wide-ranging effects on life-history traits. Here, using the crustacean Daphnia magna, we document a new effect: maternal food quantity affects offspring feeding rate, with low quantities of food triggering mothers to produce slow-feeding offspring. Such a change in the rate of resource acquisition has broad implications for population growth or dynamics and for interactions with, for instance, predators and parasites. This maternal effect can also explain the previously puzzling situation that the offspring of well-fed mothers, despite being smaller, grow and reproduce better than the offspring of food-starved mothers. As an additional source of variation in resource acquisition, this maternal effect may also influence relationships between life-history traits, i.e. trade-offs, and thus constraints on adaptation. Maternal nutrition has long-lasting effects on health and particularly diet-related traits in humans; finding an effect of maternal nutrition on offspring feeding rate in Daphnia highlights the utility of this organism as a powerful experimental model for exploring the relationship between maternal diet and offspring fitness.     

Effects of experimentally manipulated yolk thyroid hormone levels on offspring development in a wild bird species

Maternal effects are a crucial mechanism in a wide array of taxa to generate phenotypic variation, thereby affecting offspring development and fitness. Maternally derived thyroid hormones (THs) are known to be essential for offspring development in mammalian and fish models, but have been largely neglected in avian studies, especially in respect to natural variation and an ecological context. We studied, for the first time in a wild species and population, the effects of maternally derived THs on offspring development, behavior, physiology and fitness-related traits by experimental elevation of thyroxine and triiodothyronine in ovo within the physiological range in great tits (Parus major). We found that elevated yolk TH levels had a sex-specific effect on growth, increasing male and decreasing female growth, relative to controls, and this effect was similar throughout the nestling period. Hatching or fledging success, motor coordination behavior, stress reactivity and resting metabolic rate were not affected by the TH treatment. We conclude that natural variation in maternally derived THs may affect some offspring traits in a wild species. As this is the first study on yolk thyroid hormones in a wild species and population, more such studies are needed to investigate its effects on pre-hatching development, and juvenile and adult fitness before generalizations on the importance of maternally derived yolk thyroid hormones can be made. However, this opens a new, interesting avenue for further research in the field of hormone mediated maternal effects.     

Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal

The transfer of antibodies from mother to offspring provides crucial protection against infection to offspring during early life in humans and domestic and laboratory animals. However, few studies have tested the consequences of variation in maternal antibody transfer for offspring fitness in the wild. Further, separating the immunoprotective effects of antibodies from their association with nutritional resources provided by mothers is difficult. Here, we measured plasma levels of total and parasite-specific antibodies in neonatal (less than 10 days old) wild Soay sheep over 25 years to quantify variation in maternal antibody transfer and test its association with offspring survival. Maternal antibody transfer was predicted by maternal age and previous antibody responses, and was consistent within mothers across years. Neonatal total IgG antibody levels were positively related to early growth, suggesting they reflected nutritional transfer. Neonatal parasite-specific IgG levels positively predicted first-year survival, independent of lamb weight, total IgG levels and subsequent lamb parasite-specific antibody levels. This relationship was partly mediated via an indirect negative association with parasite burden. We show that among-female variation in maternal antibody transfer can have long-term effects on offspring growth, parasite burden and fitness in the wild, and is likely to impact naturally occurring host–parasite dynamics.     

Maternal effects on offspring consumption can stabilize fluctuating predator–prey systems

Maternal effects, where the conditions experienced by mothers affect the phenotype of their offspring, are widespread in nature and have the potential to influence population dynamics. However, they are very rarely included in models of population dynamics. Here, we investigate a recently discovered maternal effect, where maternal food availability affects the feeding rate of offspring so that well-fed mothers produce fast-feeding offspring. To understand how this maternal effect influences population dynamics, we explore novel predator–prey models where the consumption rate of predators is modified by changes in maternal prey availability. We address the ‘paradox of enrichment'', a theoretical prediction that nutrient enrichment destabilizes populations, leading to cycling behaviour and an increased risk of extinction, which has proved difficult to confirm in the wild. Our models show that enriched populations can be stabilized by maternal effects on feeding rate, thus presenting an intriguing potential explanation for the general absence of ‘paradox of enrichment'' behaviour in natural populations. This stabilizing influence should also reduce a population''s risk of extinction and vulnerability to harvesting.     

Older mothers follow conservative strategies under predator pressure: The adaptive role of maternal glucocorticoids in yellow-bellied marmots

When the maternal environment is a good predictor of the offspring environment, maternal glucocorticoid (GC) levels might serve to pre-program offspring to express certain phenotypes or life-history characteristics that will increase their fitness. We conducted a field study to assess the effects of naturally occurring maternal GC levels on their offspring in yellow-bellied marmots (Marmota flaviventris) subjected to different predator pressures. Maternal fecal corticosteroid metabolites (FCM) were positively correlated with predator pressure. Predators had both direct and indirect effects on pups. We found that older mothers with higher FCM levels had smaller and female-biased litters. Moreover, sons from older mothers with high FCM levels dispersed significantly more than those from older mothers with low FCM levels, whereas the opposite pattern was found in pups from younger mothers. These age-related effects may permit females to make adaptive decisions that increase their pups' fitness according to their current situation.     

Estimates of direct and indirect effects for early juvenile survival in captive populations maintained for conservation purposes: the case of Cuvier's gazelle

Together with the avoidance of any negative impact of inbreeding, preservation of genetic variability for life‐history traits that could undergo future selective pressure is a major issue in endangered species management programmes. However, most of these programmes ignore that, apart from the direct action of genes on such traits, parents, as contributors of offspring environment, can influence offspring performance through indirect parental effects (when parental genotype and phenotype exerts environmental influences on offspring phenotype independently of additive genetic effects). Using quantitative genetic models, we estimated the additive genetic variance for juvenile survival in a population of the endangered Cuvier's gazelle kept in captivity since 1975. The dataset analyzed included performance recording for 700 calves and a total pedigree of 740 individuals. Results indicated that in this population juvenile survival harbors significant additive genetic variance. The estimates of heritability obtained were in general moderate (0.115–0.457) and not affected by the inclusion of inbreeding in the models. Maternal genetic contribution to juvenile survival seems to be of major importance in this gazelle's population as well. Indirect genetic and indirect environmental effects assigned to mothers (i.e., maternal genetic and maternal permanent environmental effects) roughly explain a quarter of the total variance estimated for the trait analyzed. These findings have major evolutionary consequences for the species as show that offspring phenotypes can evolve strictly through changes in the environment provided by mothers. They are also relevant for the captive breeding programme of the species. To take into account, the contribution that mothers have on offspring phenotype through indirect genetic effects when designing pairing strategies might serve to identify those females with better ability to recruit, and, additionally, to predict reliable responses to selection in the captive population.     

Maternal environmental effects of competition influence evolutionary potential in rapeseed (<Emphasis Type="Italic">Brassica</Emphasis><Emphasis Type="Italic">rapa</Emphasis>)

Maternal environmental effects reflect the contribution of the maternal environment to the offspring phenotype. Maternal effects are prevalent in plants and animals and may undergo adaptive evolution and affect patterns of natural selection within and across generations. Here, we raise two generations of a rapeseed (Brassica rapa) population derived from a cross between a rapid-cycling and an oilseed genotype in competitive and noncompetitive settings. Maternal environment had little effect on average offspring phenotypes. Maternal genotypes, however, differed in the sensitivity of almost all offspring phenotypes to the maternal environment, demonstrating genetic variation in maternal effects for traits expressed throughout ontogeny. Maternal environment did not significantly affect progeny seed production, and maternal genotypes were not variable for this trait, indicating no evidence for direct maternal effects on offspring fitness. Maternal environment influenced natural selection in the progeny generation; disruptive selection acted on seed mass among seeds matured in the noncompetitive maternal environment versus no significant selection on this trait for seeds matured in the competitive maternal environment. Although maternal effects did not directly increase fitness, they did affect evolutionary potential and selection in the progeny generation. These results suggest that diverse phenotypes of both wild and cultivated B. rapa genotypes will depend on the maternal environment in which the seeds are matured.     

Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird

Stressful conditions experienced by individuals during their early development have long-term consequences on various life-history traits such as survival until first reproduction. Oxidative stress has been shown to affect various fitness-related traits and to influence key evolutionary trade-offs but whether an individual''s ability to resist oxidative stress in early life affects its survival has rarely been tested. In the present study, we used four years of data obtained from a free-living great tit population (Parus major; n = 1658 offspring) to test whether pre-fledging resistance to oxidative stress, measured as erythrocyte resistance to oxidative stress and oxidative damage to lipids, predicted fledging success and local recruitment. Fledging success and local recruitment, both major correlates of survival, were primarily influenced by offspring body mass prior to fledging. We found that pre-fledging erythrocyte resistance to oxidative stress predicted fledging success, suggesting that individual resistance to oxidative stress is related to short-term survival. However, local recruitment was not influenced by pre-fledging erythrocyte resistance to oxidative stress or oxidative damage. Our results suggest that an individual ability to resist oxidative stress at the offspring stage predicts short-term survival but does not influence survival later in life.     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.