Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier‐born offspring are more likely to survive through their first winter and are larger following that winter, than are later‐born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent–offspring conflict in the evolution of maternal effects on parturition date.     

Stress avoidance in a common annual: reproductive timing is important for local adaptation and geographic distribution

Adaptation to local environments may be an important determinant of species' geographic range. However, little is known about which traits contribute to adaptation or whether their further evolution would facilitate range expansion. In this study, we assessed the adaptive value of stress avoidance traits in the common annual Cocklebur (Xanthium strumarium) by performing a reciprocal transplant across a broad latitudinal gradient extending to the species' northern border. Populations were locally adapted and stress avoidance traits accounted for most fitness differences between populations. At the northern border where growing seasons are cooler and shorter, native populations had evolved to reproduce earlier than native populations in the lower latitude gardens. This clinal pattern in reproductive timing corresponded to a shift in selection from favouring later to earlier reproduction. Thus, earlier reproduction is an important adaptation to northern latitudes and constraint on the further evolution of this trait in marginal populations could potentially limit distribution.     

Geographic variation in thermal sensitivity of early life traits in a widespread reptile

Taxa with large geographic distributions generally encompass diverse macroclimatic conditions, potentially requiring local adaptation and/or phenotypic plasticity to match their phenotypes to differing environments. These eco‐evolutionary processes are of particular interest in organisms with traits that are directly affected by temperature, such as embryonic development in oviparous ectotherms. Here we examine the spatial distribution of fitness‐related early life phenotypes across the range of a widespread vertebrate, the painted turtle (Chrysemys picta). We quantified embryonic and hatchling traits from seven locations (in Idaho, Minnesota, Oregon, Illinois, Nebraska, Kansas, and New Mexico) after incubating eggs under constant conditions across a series of environmentally relevant temperatures. Thermal reaction norms for incubation duration and hatchling mass varied among locations under this common‐garden experiment, indicating genetic differentiation or pre‐ovulatory maternal effects. However, latitude, a commonly used proxy for geographic variation, was not a strong predictor of these geographic differences. Our findings suggest that this macroclimatic proxy may be an unreliable surrogate for microclimatic conditions experienced locally in nests. Instead, complex interactions between abiotic and biotic factors likely drive among‐population phenotypic variation in this system. Understanding spatial variation in key life‐history traits provides an important perspective on adaptation to contemporary and future climatic conditions.     

Effects of Maternal Basking and Food Quantity during Gestation Provide Evidence for the Selective Advantage of Matrotrophy in a Viviparous Lizard

The evolution of matrotrophy (i.e., direct supply of nutrients by the mother during gestation) may be associated with high maternal energy availability during gestation. However, we lack knowledge about the selective advantages of matrotrophic viviparity (live-bearing) in reptiles. In reptiles, the interaction between body temperature and food intake affect maternal net energy gain. In the present study, we examined the effects of basking and food availability (2 by 2 factorial design) during gestation on offspring phenotype in a matrotrophic viviparous lizard (Pseudemoia entrecasteauxii). Subsequently, we investigated if the maternal effects were context-dependent using offspring growth rate as an indicator of the adaptive significance of matrotrophy. Offspring were exposed either to the same thermal conditions as their mothers experienced or to thermal conditions different from those experienced by their mothers. We provide the first evidence that an interaction between maternal thermal and maternal food conditions during gestation strongly affects offspring phenotype, including date of birth, body size and performance ability, which affect offspring fitness. Offspring growth rate was dependent on offspring thermal conditions, but was not influenced by maternal effects or offspring sex. Matrotrophic viviparity provided gravid females with the means to enhance offspring fitness through greater energetic input to offspring when conditions allowed it (i.e., extended basking opportunity with high food availability). Therefore, we suggest that selective advantages of matrotrophic viviparity in P. entrecasteauxii may be associated with high maternal energy availability during gestation.     

The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage

The evolution of exploitative specificity can be influenced by environmental variability in space and time and the intensity of trade-offs. Coevolution, the process of reciprocal adaptation in two or more species, can produce variability in host exploitation and as such potentially drive patterns in host and parasite specificity. We employed the bacterium Pseudomonas fluorescens SBW25 and its DNA phage Phi2 to investigate the role of coevolution in the evolution of phage infectivity range and its relation with phage growth rate. At the phage population level, coevolution led to the evolution of broader infectivity range, but without an associated decrease in phage growth rate relative to the ancestor, whereas phage evolution in the absence of bacterial evolution led to an increased growth rate but no increase in infectivity range. In contrast, both selection regimes led to phage adaptation (in terms of growth rates) to their respective bacterial hosts. At the level of individual phage genotypes, coevolution resulted in within-population diversification in generalist and specialist infectivity range types. This pattern was consistent with a multilocus gene-for-gene interaction, further confirmed by an observed cost of broad infectivity range for individual phage. Moreover, coevolution led to the emergence of bacterial genotype by phage genotype interactions in the reduction of bacterial growth rate by phage. Our study demonstrates that the strong reciprocal selective pressures underlying the process of coevolution lead to the emergence and coexistence of different strategies within populations and to specialization between selective environments.     

Delayed parturition: constraint or coping mechanism in a viviparous gekkonid?

The extended gestation of fully developed embryos in viviparous reptiles can be the consequence of a lack of appropriate environmental conditions and/or an adaptive contribution to increased offspring viability. I examined the cause and effects of extended gestation in a gekkonid lizard Hoplodactylus maculatus , which delays parturition of developed embryos for up to 9 months from autumn into a second spring. Comparisons of microhabitat temperatures showed that thermal opportunities were equally conducive to birth in autumn and spring. The responsiveness of females to a hormonal stimulant for parturition also did not differ between these seasons. Multiple offspring traits were measured, including body size, locomotory ability and lipid reserves, and were found not to increase with extended gestation. Incorporating these results with previously published evidence for microhabitat thermal variation, I discuss whether delayed parturition may be an adaptive mechanism maintained by the selective pressures of an uncertain thermal environment on components of reproduction, including vitellogenesis, maternal birthing cues and neonatal survival.     

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.     

Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation

A recently developed integrative framework proposes that the vulnerability of a species to environmental change depends on the species' exposure and sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change. These vulnerability criteria require behavioural, physiological and genetic data. With this information in hand, biologists can predict organisms most at risk from environmental change. Biologists and managers can then target organisms and habitats most at risk. Unfortunately, the required data (e.g. optimal physiological temperatures) are rarely available. Here, we evaluate the reliability of potential proxies (e.g. critical temperatures) that are often available for some groups. Several proxies for ectotherms are promising, but analogous ones for endotherms are lacking. We also develop a simple graphical model of how behavioural thermoregulation, acclimation and adaptation may interact to influence vulnerability over time. After considering this model together with the proxies available for physiological sensitivity to climate change, we conclude that ectotherms sharing vulnerability traits seem concentrated in lowland tropical forests. Their vulnerability may be exacerbated by negative biotic interactions. Whether tropical forest (or other) species can adapt to warming environments is unclear, as genetic and selective data are scant. Nevertheless, the prospects for tropical forest ectotherms appear grim.     

Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy

We used analytic and simulation models to determine the ecological conditions favoring evolution of a matrotrophic fish from a lecithotrophic ancestor given a complex set of trade-offs. Matrotrophy is the nourishment of viviparous embryos by resources provided between fertilization and parturition, while lecithotrophy describes embryo nourishment provided before fertilization. In fishes and reptiles, embryo nourishment encompasses a continuum from solely lecithotrophic to primarily matrotrophic. Matrotrophy has evolved independently from lecithotrophic ancestors many times in many groups. We assumed matrotrophy increased the number of offspring a viviparous female could gestate and evaluated conditions of food availability favoring lecithotrophy or matrotrophy. The matrotrophic strategy was superior when food resources exceeded demand during gestation but at a risk of overproduction and reproductive failure if food intake was limited. Matrotrophic females were leaner during gestation than lecithotrophic females, yielding shorter life spans. Our models suggest that matrotrophic embryo nourishment evolved in environments with high food availability, consistently exceeding energy requirements for maintaining relatively large broods. Embryo abortion with some resorption of invested energy is a necessary preadaptation to the evolution of matrotrophy. Future work should explore trade-offs of age-specific mortality and reproductive output for females maintaining different levels of fat storage during gestation.     

Is evolution necessary for range expansion? Manipulating reproductive timing of a weedy annual transplanted beyond its range

Ecologists often consider how environmental factors limit a species' geographic range. However, recent models suggest that geographic distribution also may be determined by a species' ability to adapt to novel environmental conditions. In this study, we empirically tested whether further evolution would be necessary for northern expansion of the weedy annual cocklebur (Xanthium strumarium) in its native North American range. We transplanted seedlings beyond the northern border and photoperiodically manipulated reproductive timing, a trait important for adaptation to shorter growing seasons at higher latitudes within the range, to determine whether further evolution of this trait would result in a phenotype viable beyond the range. Earlier reproductive induction enabled plants to produce mature seeds beyond the range and to achieve a reproductive output similar to those grown within the range. Therefore, evolution of earlier reproduction in marginal populations would be necessary for northward range expansion. This study is the first to empirically show that evolution in an ecologically important trait would enable a species to survive and reproduce beyond its current range. These results suggest that relatively few traits may limit a species' range and that identifying evolutionary constraints on such traits could be important for predicting geographic distribution.     

A meta-analysis of factors affecting local adaptation between interacting species

Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.     

Cuticular hydrocarbon synthesis and its maternal provisioning to embryos in the viviparous cockroach Diploptera punctata

Embryos of the viviparous cockroach Diploptera punctata accumulate large amounts of hydrocarbon (HC) of either maternal or embryonic origin. HC synthesis and its accumulation in maternal and embryonic tissues were measured over the course of gestation. Female abdominal integument was the only tissue that synthesized appreciable amounts of HC in vitro, and did so at an increasing rate from the time of mating to mid-pregnancy, when rates of synthesis declined. The embryos synthesized HC at rates <1% those of the female, showing that the majority of HC detected in and on embryos was of maternal origin. The brood sac that houses the developing embryos did not synthesize HC in vitro, indicating that HC must be transported from the female abdominal integument to the embryos. The mass of female epicuticular HC was constant at approximately 183 microg, while her internal HC increased fourfold from mating to mid-pregnancy, then declined until parturition. The decline in internal HC reflected both declining HC synthesis in the female and greater export to the embryos, as embryonic internal HC increased 250-fold prior to parturition. An external HC coating over the oothecal covering and chorion of the embryos increased to mid-pregnancy, then declined. Unlike oviparous cockroaches, D. punctata females fed throughout the reproductive cycle, reflecting the nutritional demands of continuously provisioning the developing embryos.     

Inter- and intrapopulation variation in thermal reaction norms for growth rate: evolution of latitudinal compensation in ectotherms with a genetic constraint

In ectotherms, lower temperatures in high-latitude environments would theoretically reduce the annual growth rates of individuals. If slower growth and resultant smaller body size reduce fitness, individuals in higher latitudes may evolve compensatory responses. Two alternative models of such latitudinal compensation are possible: Model I: thermal reaction norms for growth rates of high-latitude individuals may be horizontally shifted to a lower range of temperatures, or Model II: reaction norms may be vertically shifted so that high-latitude individuals can grow faster across all temperatures. Model I is expected when annual growth rates in the wild are only a function of environmental temperatures, whereas Model II is expected when individuals in higher latitudes can only grow during a shorter period of a year. A variety of mixed strategies of these two models are also possible, and the magnitude of horizontal versus vertical variation in reaction norms among latitudinal populations will be indicative of the importance of "temperature" versus "seasonality" in the evolution of latitudinal compensation. However, the form of latitudinal compensation may be affected by possible genetic constraints due to the genetic architecture of reaction norms. In this study, we examine the inter- and intrapopulation variations in thermal reaction norms for growth rate of the medaka fish Oryzias latipes. Common-environment experiments revealed that average reaction norms differed primarily in elevation among latitudinal populations in a manner consistent with Model II (adaptation to "seasonality"), suggesting that natural selection in high latitudes prefers individuals that grow faster even within a shorter growing season to individuals that have longer growing seasons by growing at lower temperatures. However, intrapopulation variation in reaction norms was also vertical: some full-sibling families grew faster than others across all temperatures examined. This tendency in intrapopulation genetic variation for thermal reaction norms may have restricted the evolution of latitudinal compensation, irrespective of the underlying selection pressure.     

Asexual and sexual reproductive strategies in clonal plants

Most plants can reproduce both sexually and asexually (or vegetatively),and the balance between the two reproductive modes may vary widely between and within species.Extensive clonal growth may affect the evolution of life history traits in many ways.First,in some clonal species,sexual reproduction and sex ratio vary largely among populations.Variation in sexual reproduction may strongly affect plant's adaptation to local environments and the evolution of the geographic range.Second,clonal growth can increase floral display,and thus pollinator attraction,while it may impose serious constraints and evolutionary challenges on plants through geitonogamy that may strongly influence pollen dispersal.Geitonogamous pollination can bring a cost to plant fitness through both female and male functions.Some co-evolutionary interactions,therefore,may exist between the spatial structure and the mating behavior of clonal plants.Finally,a trade-off may exist between sexual reproduction and clonal growth.Resource allocation to the two reproductive modes may depend on environmental conditions,competitive dominance,life span,and genetic factors.If different reproductive modes represent adaptive strategies for plants in different environments,we expect that most of the resources should be allocated to sexual reproduction in habitats with fluctuating environmental conditions and strong competition,while clonal growth should be dominant in stable habitats.Yet we know little about the consequence of natural selection on the two reproductive modes and factors which control the balance of the two reproductive modes.Future studies should investigate the reproductive strategies of clonal plants simultaneously from both sexual and asexual perspectives.     

Evolution of dispersal in a predator-prey metacommunity

Dispersal is crucial to allowing species inhabiting patchy or spatially subdivided habitats to persist globally despite the possibility of frequent local extinctions. Theoretical studies have repeatedly demonstrated that species that exhibit a regional metapopulation structure and are subject to increasing rates of local patch extinctions should experience strong selective pressures to disperse more rapidly despite the costs such increased dispersal would entail in terms of decreased local fitness. We extend these studies to consider how extinctions arising from predator-prey interactions affect the evolution of dispersal for species inhabiting a metacommunity. Specifically, we investigate how increasing a strong extinction-prone interaction between a predator and prey within local patches affects the evolution of each species' dispersal. We found that for the predator, as expected, evolutionarily stable strategy (ESS) dispersal rates increased monotonically in response to increasing local extinctions induced by strong predator top-down effects. Unexpectedly for the prey, however, ESS dispersal rates displayed a nonmonotonic response to increasing predator-induced extinction rates-actually decreasing for a significant range of values. These counterintuitive results arise from how extinctions resulting from trophic interactions play out at different spatial scales: interactions that increase extinction rates of both species locally can, at the same time, decrease the frequency of interaction between the prey and predator at the metacommunity scale.     

Prenatal sex ratios influence sexual dimorphism in a reptile

The prenatal environment influences offspring traits in a variety of ways and in a wide range of taxa. For example, maternal allocation of steroids to the eggs influences offspring traits in birds, and in some mammals the intrauterine position influences morphological, behavioural, and physiological traits due to sex-related steroid transfer between sibling fetuses. We show that similar phenomena occur in the common lizard (Lacerta vivipara), a viviparous reptile. Females developing in male-biased clutches had a more masculine allometry (relatively larger heads) at parturition than females developing in female-biased clutches. Males were correspondingly feminized in female-biased clutches. The effects could either be due to diffusion of steroids produced by the offspring or by a general tendency for females to allocate steroids according to the sex ratio of her clutch. Subsequent to parturition, the sexes differed in their growth trajectories depending on sex ratio environment. In males, the difference in allometry between sex ratio environments remained over time, whereas in females the corresponding effect disappeared.     

Evidence for placental transfer of maternal corticosterone in a viviparous lizard

In mammals, there is experimental evidence that circulating maternal cortisol is transferred to the embryos across the placenta during gestation. Direct effects of this maternal cortisol may allow embryos to display phenotypic plasticity to cope with postnatal environments (i.e., pre-programming). The potential for maternal hormone induced-adaptation may be of considerable evolutionary significance in viviparous animals. However, to date, there is no such direct evidence that circulating maternal corticosterone passes through the placenta and into the embryos of viviparous reptiles. In this study, we assessed the transfer of (3)H-corticosterone injected into females of the lizard Pseudemoia entrecasteauxii into maternal blood, maternal liver, the embryo, the yolk and the amniotic fluid during mid-to-late gestation. We provide direct evidence that circulating maternal corticosterone passes through the placenta into the embryos in this species. Transfer of maternal corticosterone into the embryos significantly decreased at the end of embryonic development. We discuss these results in terms of the relationships between the degree of corticosterone transfer and embryonic stage. These results demonstrate the potential for direct effects of maternal corticosterone, including endocrine pre-programming, upon the developing embryos in viviparous lizards.     

A novel pattern of placental leucine transfer during mid to late gestation in a highly placentotrophic viviparous lizard

Placentotrophy is the nourishment of embryos by resources provided via the placenta during gestation. The magnitude and timing of placental nutrient support during pregnancy are important for embryonic growth, especially in highly placentotrophic animals such as mammals. However, no study has yet investigated how placental organic nutrient support may change during pregnancy in highly placentotrophic viviparous reptiles. Amino acids are essential nutrients for embryonic growth and leucine is a common amino acid. The magnitude and timing of placental leucine transfer may affect embryonic growth and mass and, therefore, offspring phenotype. In this study, female Pseudemoia entrecasteauxii, a highly placentotrophic viviparous skink, were collected throughout gestation. We injected (3)H-leucine into these gravid females and assessed the transfer of (3)H-leucine into maternal compartments (i.e., the blood and the liver), and into embryonic compartments (i.e., the embryo, the yolk, and the amniotic fluid). At either 60 or 120 min post-injection, the radioactivity in each sample was extracted and then counted, and the transfer ratio was calculated. Our results provide direct evidence that circulating maternal leucine passes through the placenta into the embryos in this species. The relative rate of placental leucine transfer did not alter during mid to late gestation. This suggests the steady somatic growth of the embryos during mid-late pregnancy is dependent upon the placental transfer of nutrients rather than yolk stores. This pattern of placental nutrient support may determine offspring body size at birth and, therefore, offspring fitness in P. entrecasteauxii.     

Are babies better in autumn or spring? The consequences of extending gestation in a biennially reproducing viviparous lizard

Niveoscincus microlepidotus, the southern snow skink, is a biennially reproducing alpine viviparous lizard with an extremely protracted gestation period: embryos are fully developed in autumn, but held over winter so that offspring are born in spring. The obvious benefits for offspring survival of delaying birth until spring have been demonstrated previously. To examine the consequences of deferred parturition for offspring characteristics, we compared neonates obtained in autumn by dissection with neonates born naturally in the spring. Our results demonstrate that deferral of parturition until spring represents a trade-off between key offspring characteristics (spring neonates exhibit lower growth rates, reduced sprint speed after birth, reduced condition and decreased energy reserves) and offspring size [spring neonates are heavier (wet mass) and longer (snout-vent length)]. Furthermore, when females are placed into cold experimental conditions in spring around the time of natural parturition, this species is able to defer parturition for an additional 4 weeks with no significant effect on offspring characteristics. Our results provide further evidence that flexibility in birth date provides a significant advantage to viviparous lizards living in cold climates.     

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.