Stress and body condition as prenatal and postnatal determinants of dispersal in the common lizard (Lacerta vivipara)

Dispersal is a complex phenomenon affected by multiple factors. Among the factors that influence dispersal in the common lizard (Lacerta vivipara), poor maternal body condition and stress are known to decrease dispersal propensity of juveniles. But the effect of individual factors on dispersal could change when several of them act concurrently or at different developmental stages. Prenatal factors can affect clutch and/or juvenile characteristics that later affect dispersal. Postnatal influences are mainly exerted on juvenile dispersal behavior. We investigated the role of body condition and stress on dispersal at a prenatal and a postnatal stage. Stress was mimicked by experimentally increasing corticosterone levels in pregnant females and recently born juveniles. We considered (1). the influence of maternal body condition and prenatal corticosterone treatment on clutch, juvenile characteristics and on dispersal behavior and (2). the influence of juvenile body condition and postnatal corticosterone treatment on juvenile dispersal behavior. There was an interaction between maternal condition and prenatal corticosterone treatment on juvenile dispersal. Dispersal decreased with maternal corticosterone increase only in juveniles from the more corpulent females, while it increased with juvenile body condition. Good maternal body condition affected clutch and juvenile characteristics favoring dispersal, while elevation of corticosterone level (stress) exerted the opposite effect. Juvenile body condition favored dispersal, while there was no effect of postnatal corticosterone treatment on juvenile dispersal propensity.     

Maternal effects on offspring locomotion: influence of density and corticosterone elevation in the lizard Lacerta vivipara

Offspring phenotype can be affected by maternal history before and during gestation. Offspring sensitivity to maternal conditions is believed to have evolved to favor preadaptation of offspring to environmental factors they are likely to encounter. Because the locomotor capacity of an individual is likely to have important fitness consequences, we examined the role of long-term and short-term prenatal conditions on offspring's locomotor performance in the lizard Lacerta vivipara. To examine long-term prenatal effects, we manipulated the density of two populations, leaving two additional populations as unmanipulated. We then collected pregnant females within these four populations (Cévennes, Massif Central, France) and kept them in the laboratory until parturition. To examine short-term prenatal effects, we manipulated the corticosterone level of half the females within each population. We took two different measurements of offspring locomotion: sprint speed and endurance. As already documented, sprint speed was positively correlated with offspring body size. Although population density significantly affected female fecundity, neither the density manipulation nor the population of origin influenced offspring phenotype. Corticosterone administered during gestation decreased juvenile sprint speed but did not affect juvenile endurance. Furthermore, we observed that the motivation to run was influenced by maternal hormonal treatment. Juveniles born from corticosterone-treated mothers needed more stimuli than those born from control mothers. We conclude, therefore, that the action of corticosterone on sprint speed could be more behavioral than physiological. Offspring phenotype as measured by endurance and sprint speed appeared partly under maternal control.     

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.     

Delayed dispersal and prolonged brood care in a family‐living beetle

Delayed juvenile dispersal is an important prerequisite for the evolution of family‐based social systems, such as cooperative breeding and eusociality. In general, young adults forego dispersal if there are substantial benefits to remaining in the natal nest and/or the likelihood of dispersing and breeding successfully is low. We investigate some general factors thought to drive delayed juvenile dispersal in the horned passalus beetle, a family‐living beetle in which young adults remain with their families in their natal nest for several months before dispersing. Fine‐scale population genetic structure indicated high gene flow between nest sites, suggesting that constraints on mobility are unlikely to explain philopatry. Young adults do not breed in their natal log and likely disperse before reaching breeding age, suggesting that they do not gain direct reproductive benefits from delayed dispersal. We also examined several ways in which parents might incentivize delayed dispersal by providing prolonged care to adult offspring. Although adult beetles inhibit fungal growth in the colony by manipulating both the nest site and deceased conspecifics, this is unlikely to be a major explanation for family living as both parents and adult offspring seem capable of controlling fungal growth. Adult offspring that stayed with their family groups also neither gained more mass nor experienced faster exoskeleton development than those experimentally removed from their families. The results of these experiments suggest that our current understanding of the factors underlying prolonged family living may be insufficient to explain delayed dispersal in at least some taxa, particularly insects.     

Malformed offspring,sibling matings,and selection against inbreeding in the sand lizard (Lacerta agilis)

We demonstrated that sand lizards (Lacerta agilis) are more likely to have malformed offspring when they mate with siblings. Offspring with malformations, such as deformed limbs and heads, have zero survival in a natural population. Normal-looking siblings of malformed hatchlings also had a reduced survival in the wild, compared to offspring from clutches in which all siblings appeared normal. The proportion of malformed hatchlings in the natural population was ca. 10%, in spite of differences in juvenile dispersal between males and females. Male juveniles disperse significantly further from their natal sites than do female juveniles.     

Effects of Paternal Reproductive Tactic on Juvenile Behaviour and Kin Recognition in Chinook Salmon (Oncorhynchus tshawytscha)

Salmonids are characterized by alternative reproductive tactics, which can lead to an asymmetry in relatedness among offspring within nests and consequently the benefit of discriminating among nestmates. In this study, we examined the effect of paternal reproductive tactic on juvenile behaviour and kin discrimination in Chinook salmon. We created maternal half‐sibling families by collecting eggs from mature females and fertilizing one‐half with the milt of a precocious 2‐yr‐old male and the other half with the milt of a non‐precocious 4‐yr‐old male. These families were reared in full‐sibling groups for approximately 9 mo, and social interactions were then observed in groups of six fish of mixed relatedness. We found evidence for kin discrimination, as significantly less aggression was directed towards related fish than unrelated fish, and the same trends were observed regardless of whether social interactions included full‐siblings or half‐siblings. These results show that familiarity is not required to recognize kin and thereby implicate phenotype matching as the mechanism of kin recognition. We also found that the offspring of 2‐yr‐old males were larger and more aggressive than the offspring of 4‐yr‐old males, which is consistent with other studies showing that precocious males are the fastest‐growing members of their cohort. However, kin‐directed behaviours did not differ between the offspring of 2‐ and 4‐yr‐old males.     

Mother-offspring interactions affect natal dispersal in a lizard

Interactions between relatives operate strong selective pressures on dispersal. Recently, a correlative study in the common lizard (Lacerta vivipara) suggested that natal dispersal might respond plastically to mother-offspring interactions. Here, we describe a factorial experiment supporting this observation. Two crossed treatments were applied to experimental patches of the common lizard: (i) presence versus absence of the mother, inducing a difference of kinship in offspring neighbourhoods; and (ii) high versus low patch density, resulting in two levels of conspecific abundance and modulating the effect of mother presence on the average kinship within a patch. Dispersal of the same cohort of offspring was observed at the juvenile and yearling stages. We found a sex-dependent response of offspring dispersal to the removal of the mother at the two stages. During the juvenile stage, higher dispersal was found in females in the presence of the mother, with males unaffected. During the yearling stage, the responses of both sexes to the presence of the mother opposed each other. In addition, we found a negative relationship between dispersal and patch density at the juvenile stage. No interaction between density and the presence of the mother was detected, which suggests that behavioural responses to kinship and density are disconnected and that kinship is assessed at a small social scale. We discuss the role of competition and inbreeding avoidance to explain the observed pattern.     

Low temperatures during ontogeny increase fluctuating asymmetry and reduce maternal aggression in the house mouse,Mus musculus

Maternal aggression is behavior displayed by post‐partum lactating female mice toward unfamiliar conspecifics, presumably as a defense against infanticide. A variety of perinatal stressors can impair maternal care in adulthood. Previous studies on associations between developmental perturbations and maternal aggression have produced mixed results. To address this issue, we employed a proxy for developmental instability, namely fluctuating asymmetry (FA) to further elucidate the relationship between low temperature stress and maternal aggression. FA, small, random deviations from perfect symmetry in bilateral characters is used as a quantitative measure of stress during ontogeny. Dams were either maintained in standard laboratory temperatures (21 ± 2°C), or cold temperatures (8 ± 2°C) during gestation. During lactation, their progeny either remained in the temperature condition in which they were gestated or were transferred to the other temperature condition. Four individual measures of FA, a composite of these measures, and three measures of maternal aggression were assessed in the female progeny in adulthood. Exposure to low temperatures during both pre‐ and early post‐natal development increased composite FA and reduced all three measures of maternal aggression compared to controls. Exposure to low temperatures during the pre‐ or post‐natal period alone did not induce either high FA or altered maternal aggression. Certain measures of FA and nest defense were negatively correlated. Our results suggest that low temperatures experienced during gestation and lactation may have important fitness costs. Low maternal aggression toward infanticidal conspecifics is likely to limit the number of offspring surviving into adulthood. Overall, FA appears to be a reliable indicator of chronic developmental stress with implications for fitness.     

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.     

Adaptive significance of maternal induction of density-dependent phenotypes

Density has been demonstrated to impact life history traits such as growth, fecundity and survival. Some authors have proposed that morphological and behavioral traits have evolved in response to density conditions. To escape the adverse effect of density, individuals can either adapt to crowding or avoid crowding by dispersing. The aim of this work is to study the interplay between local adaptation and dispersal in four populations of the common lizard, Lacerta vivipara, where densities of both the maternal and juvenile environment have been experimentally manipulated. Density was decreased in the spring by removing a quarter of the population at two sites and was un-manipulated in two other sites. One month later, we caught some pregnant females and kept them in the laboratory until parturition. To manipulate density of postnatal neonates and juveniles, we divided each clutch into two, and released half of the juveniles either in a reduced density site or in a control one. We then recaptured individuals a year after release and recorded their size and weight. When density was reduced, females increased their clutch size, but produced offspring of lower body condition than in the control sites. The conspicuous ventral color of females was likewise increased when density was reduced. However, offspring growth rate, local survival and dispersal were not influenced by maternal density. Juvenile females released in the reduced-density site had lower survival rate than those released in the control density site. Contrary to expectations, offspring dispersal was significantly higher at the reduced compared to control density sites. There was no interaction between maternal density habitat and the juvenile release habitat indicating that maternal effects did not influence juvenile life history traits in a different way according to the level of density. Moreover, clutch size and offspring size had no effect on juvenile growth or survival.     

Heterochrony and the evolution of poecilogony: generating larval diversity

Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.     

Sex-biased dispersal in eastern chipmunks, Tamias striatus

I investigated the effect of male mate competition and inbreeding avoidance on natal dispersal of chipmunks by longitudinally monitoring known individuals from 1986 to 1990. Natal males exhibited greater absolute and effective dispersal distances but dispersed at the same proportion as natal females. Recruitment of juvenile males was negatively affected by density of resident males, but there was no evidence of local mate competition among male kin. Analysis of the spatial distribution of neighbors showed that natal males settled farther from their mothers than did their female siblings and farther than unrelated juvenile males. In addition, mothers apparently tolerated daughters as close neighbors and occasionally shared den sites with grandprogeny. Sexually mature males were never neighbors of their mothers and were never observed at maternal mating bouts. Males may disperse to improve reproductive opportunities by avoiding competition with resident males, and by increasing access to unrelated females. Maternal tolerance of daughters but not sons may result in the close affiliation between mothers and daughters, and indirectly contribute to dispersal of natal males. Hence male-biased dispersal could be a consequence of mate competition and maternal avoidance of incestuous matings. This revised version was published online in July 2006 with corrections to the Cover Date.     

Proximate and ultimate causes of natal dispersal in the great bustard Otis tarda

Between 1991 and 1997 we studied the offspring independenceand juvenile dispersal in a wild population of great bustards(Otis tarda). Young males were independent and began their juveniledispersal at an earlier age (6–11 months) than young females(8–15 months). The juvenile dispersal period was longerand the distances reached farther in males than in females.Natal dispersal distances were also longer in males, all ofwhich dispersed from their natal areas and established as adultsat 5–65 km from their natal nests. In contrast, most femaleswere strongly philopatric, settling at 0.5–5 km from theirnatal nests. These marked sex differences in offspring independenceand dispersal may have evolved originally to maintain geneticdiversity and are probably reinforced through male competitionfor mates. Young males that had fed at higher rates and receivedmore feedings from their mothers during the early maternal dependenceperiod became indepthdent and tended to disperse earlier. Theyalso integrated earlier into adult male flocks and settled earlierat their definitive leks, which were closer to their natal sites,in areas of higher adult male density. None of these correlationswas found among young females. These results suggest that enhancedfood intake and maternal care of male offspring are vitallyimportant in increasing their competitive ability during theimmature period and probably also in their fitness as breedingadults. These results are in accordance with the selective valueof large size in males and suggest how this species might havereached such a marked sexual dimorphism in size.     

Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows

Kin-based societies, where families represent the basic social unit, occur in a relatively small number of vertebrate species. In the majority of avian kin societies, families form when offspring prolong their association with the parents on the natal territory. Therefore, the key to understanding the evolution of families in birds is to understand natal philopatry (i.e. the tendency to remain on the natal territory). It has been shown that, within populations, the strength of the association between parents and offspring (i.e. family stability) increases when offspring dispersal is constrained by external environmental factors, but it is unclear whether and how family wealth influences juvenile dispersal decisions. Here, we show that young carrion crows (Corvus corone corone) from territories that were food-supplemented year-round were more philopatric and more likely to help at their family's nest than the unfed ones. The results suggest that offspring philopatry and helping behaviour are influenced by the quality of 'home' and that the availability of food resources positively affects the cohesion of the family.     

Environmental maternal effects on locomotor performance in the common lizard (Lacerta vivipara)

Environmental (i.e. non-genetic) maternal effects have the potential to associate the environmental conditions faced by mothers during gestation or before egg laying with the phenotype of their offspring. For this reason, maternal effects may play a major role in determining offspring phenotype independently of the genotype of the individuals, and can thus be considered a mechanistic basis of phenotypic plasticity. Despite the ecological and evolutionary implications of environmental maternal effects, few studies have experimentally investigated this phenomenon in reptiles. Here we report the results of an experimental laboratory study on the effects of maternal feeding rate and density on offspring locomotor performance in the common lizard (Lacerta vivipara). Lacerta vivipara is a viviparous lizard, and viviparity enhances the probability of a maternal influence on offspring phenotype. We focused on a particular phenotypic trait, maximal sprint running speed, because this trait is thought to be selectively important in squamates. Sprint speed was a repeatable trait, and it varied significantly among families. Maternal feeding rate significantly affected sprint speed, whereas density had no effect on this trait. The effect of maternal feeding rate differed according to the sex of the offspring and their body size, resulting in significant two-way and three-way interactions among these factors. In other words, the maternal feeding rate changed the shape of the allometric relationship between speed and size, but differently for males and females. The complexity of such effects makes it extremely difficult to offer an adaptive interpretation, but emphasizes the role played by the environment in shaping phenotypes among generations.     

Kin selection and natal dispersal in an age-structured population

We examine the effect of iteroparity on the evolution of dispersal for a species living in a stable but fragmented habitat. We use a kin selection model that incorporates the effects of demographic stochasticity on the local age structure and age-specific genetic identities. We consider two cases: when the juvenile dispersal rate is allowed to change with maternal age and when it is not. In the latter case, we find that the unconditional evolutionarily stable dispersal rate increases when the adult survival rate increases. Two antagonistic forces act upon the evolution of age-specific dispersal rates. First, when the local age structure varies between patches of habitat, the intensity of competition between adults and juveniles in the natal patch is, on average, lower for offspring born to older senescent mothers. This selects for decreasing dispersal with maternal age. Second, offspring born to older parents are on average more related to other juveniles in the same patch and they experience a higher intensity of kin competition, which selects for increasing dispersal with maternal age. We show that the evolutionary outcome results from a balance between these two opposing forces, which depends on the amount of variance in age structure among sub-populations.     

Mother's timing and duration of corticosterone exposure modulate offspring size and natal dispersal in the common lizard (Lacerta vivipara)

Although multiple condition dependence in dispersal is common, the proximate mechanisms that integrate information from multiple sources remain largely unknown. In the common lizard (Lacerta vivipara), earlier studies have shown that maternal plasma corticosterone level interacts with maternal phenotype to affect offspring phenotype and dispersal strategy, and may reflect the mother's external and/or internal environment. However, the mechanism by which these two types of environmental information are integrated has not been identified. We explored the possibility that the timing and duration of the corticosterone signal are the key factors by which the message is modulated. We found that the timing of corticosterone exposure affects the juvenile phenotype: an exposure to corticosterone early in development has negative effects on juvenile size, weight, and body condition, that can nevertheless be restored in the case of a prolonged exposure. The duration of corticosterone exposure affects the dispersal strategy, although the precise effect depends on the sex ratio of the clutch. That is, in female-biased clutches, a prolonged exposure during gestation promotes philopatry of juveniles, while a short exposure enhances their dispersal, a result that is consistent with kin competition theory. Therefore, our results demonstrate that while corticosterone titer may signal a mother's external and/or internal environment to her developing young, differences in the timing and duration of this endocrine signal produce offspring with specialized phenotypes that exhibit different dispersal strategies.     

Prenatal and postnatal effects of corticosterone on behavior in juveniles of the common lizard, Lacerta vivipara

Many animals exhibit dramatic responses when subjected to a stressor. A classic marker of the stress response is an increase in plasma glucocorticoids, but this constitutes only one step in the cascade from experience of a stressor to wider organismal changes, including behavior. The behavioral sensitivity to glucocorticoids would determine the consequences of the stress-related alteration of behavior for the organism. In this study we explored, under laboratory conditions, the prenatal and postnatal effects of corticosterone on activity and thermoregulation of juveniles of the common lizard, Lacerta vivipara. Activity was measured as the time spent moving and the time spent scratching the wall in an empty terrarium. Thermoregulatory behavior was measured as the time spent motionless under a light bulb. Activity and thermoregulation of juveniles of the common lizard showed a different sensitivity to prenatal and postnatal corticosterone treatment, modulated by juvenile sex and maternal condition. Prenatal corticosterone manipulation influenced the time spent moving in both sexes. By contrast, only juvenile females increased the time spent scratching the walls of the terrarium when corticosterone was delivered both at the prenatal and postnatal stage. Prenatal hormone manipulation increased the time spent basking by juveniles issued from large females. These results suggest that, in addition to influencing a variety of behavioral and morphological traits, corticosterone may also play an important role in the regulation of activity and thermoregulation of juvenile lizards, modulated by individual sex and maternal condition.     

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.     

Conditional dispersal under kin competition: extension of the Hamilton-May model to brood size-dependent dispersal

I consider a site-based model with contest competition among siblings, and assume that dispersal is conditional on the number of offspring in the natal site. Evolutionarily stable populations contain threshold dispersal strategies, which retain a certain number of offspring in the natal site and disperse the rest (if the actual number of offspring is less than the threshold, then all offspring are retained). Due to the discrete nature of the strategy set (the threshold must be integer), the ESS may not be unique or may not exist. In the latter case, two neighboring threshold strategies coexist in the evolutionarily stable population. Dispersal first decreases and then increases as a function of dispersal mortality, such that all but one offspring should be dispersed both when dispersal mortality is very small or very high. Population-level dispersal fractions are often similar to the unconditional ESS, but differ strongly when fecundity is small and dispersal mortality is high.