Lisa E. Schwanz

Climate Change and Temperature‐Dependent Sex Determination: Can Individual Plasticity in Nesting Phenology Prevent Extreme Sex Ratios?

Under temperature‐dependent sex determination (TSD), temperatures experienced by embryos during development determine the sex of the offspring. Consequently, populations of organisms with TSD have the potential to be strongly impacted by climatic warming that could bias offspring sex ratio, a fundamental demographic parameter involved in population dynamics. Moreover, many taxa with TSD are imperiled, so research on this phenomenon, particularly long‐term field study, has assumed great urgency. Recently, turtles with TSD have joined the diverse list of taxa that have demonstrated population‐level changes in breeding phenology in response to recent climate change. This raises the possibility that any adverse impacts of climate change on populations may be alleviated by individual plasticity in nesting phenology. Here, we examine data from a long‐term study on a population of painted turtles (Chrysemys picta) to determine whether changes in phenology are due to individual plasticity and whether individual plasticity in the timing of nesting has the capacity to offset the sex ratio effects of a rise in climatic temperature. We find that individual females show plasticity in the date of first nesting each year, and that this plasticity depends on the climate from the previous winter. First nesting date is not repeatable within individuals, suggesting that it would not respond to selection. Sex ratios of hatchlings within a nest declined nonsignificantly over the nesting season. However, small increases in summer temperature had a much stronger effect on nest sex ratios than did laying nests earlier in the season. For this and other reasons, it seems unlikely that individual plasticity in the timing of nesting will offset the effects of climate change on sex ratios in this population, and we hypothesize that this conclusion applies to other populations with TSD.

Climate and predation dominate juvenile and adult recruitment in a turtle with temperature-dependent sex determination.

Conditions experienced early in life can influence phenotypes in ecologically important ways, as exemplified by organisms with environmental sex determination. For organisms with temperature-dependent sex determination (TSD), variation in nest temperatures induces phenotypic variation that could impact population growth rates. In environments that vary over space and time, how does this variation influence key demographic parameters (cohort sex ratio and hatchling recruitment) in early life stages of populations exhibiting TSD? We leverage a 17-year data set on a population of painted turtles, Chrysemys picta, to investigate how spatial variation in nest vegetation cover and temporal variation in climate influence early life-history demography. We found that spatial variation in nest cover strongly influenced nest temperature and sex ratio, but was not correlated with clutch size, nest predation, total nest failure, or hatching success. Temporal variation in climate influenced percentage of total nest failure and cohort sex ratio, but not depredation rate, mean clutch size, or mean hatching success. Total hatchling recruitment in a year was influenced primarily by temporal variation in climate-independent factors, number of nests constructed, and depredation rate. Recruitment of female hatchlings was determined by stochastic variation in nest depredation and annual climate and also by the total nest production. Overall population demography depends more strongly on annual variation in climate and predation than it does on the intricacies of nest-specific biology. Finally, we demonstrate that recruitment of female hatchlings translates into recruitment of breeding females into the population, thus linking climate (and other) effects on early life stages to adult demographics.

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Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination

Nesting behaviour is critical for reproductive success in oviparous organisms with no parental care. In organisms where sex is determined by incubation temperature, nesting behaviour may be a prime target of selection in response to unbalanced sex ratios. To produce an evolutionary change in response to sex-ratio selection, components of nesting behaviour must be heritable. We estimated the field heritability of two key components of nesting behaviour in a population of painted turtles (Chrysemys picta) with temperature-dependent sex determination by applying the ‘animal model’ to a pedigree reconstructed from genotype data. We obtained estimates of low to non-detectable heritability using repeated records across all environments. We then determined environment-specific heritability by grouping records with similar temperatures for the winter preceding the nesting season, a variable known to be highly associated with our two traits of interest, nest vegetation cover and Julian date of nesting. The heritability estimates of nest vegetation cover and Julian date of nesting were qualitatively highest and significant, or nearly so, after hot winters. Additive genetic variance for these traits was not detectable after cold winters. Our analysis suggests that the potential for evolutionary change of nesting behaviour may be dependent on the thermal conditions of the preceding winter, a season that is predicted to be especially subject to climate change.

Chronic parasitic infection alters reproductive output in deer mice

Parasitized animals may alter their life histories to minimize the costs of parasitism. Organisms are predicted to decrease investment in current reproduction when parasitism has the greatest impact on current reproductive ability. In contrast, if parasitism decreases residual reproductive value, hosts should increase current reproductive investment, referred to as fecundity compensation or terminal investment. In mammalian hosts, parasitic infection most often leads to reductions in current host reproduction, perhaps attributable to the emphasis on parasites that are unlikely to impact the host’s residual reproductive value. In this study, the life history response of a rodent, Peromyscus maniculatus, to infection with a parasite that should strongly impact the residual reproductive value of its host (Schistosomatium douthitti, Trematoda) was examined. Infection decreased survival for hosts exposed to a high dose of parasites and was chronic in survivors, confirming that infection had strong impacts for the residual reproductive value of the host. As predicted, infected mice increased their reproductive output, producing litters of greater mass due to heavier offspring. However, this increased output was observed after a greater delay to begin breeding in infected mice and was not observed in animals that suffered early mortality. The deer mouse S. douthitti system may provide a rare example of fecundity compensation in mammals.

Schistosome infection in deer mice (Peromyscus maniculatus):impacts on host physiology, behavior and energetics

SUMMARY Animals routinely encounter environmental stressors and may employ phenotypic plasticity to compensate for the costs of these perturbations. Parasites represent an ecologically important stressor for animals, which may induce host plasticity. The present study examined the effects of a trematode parasite, Schistosomatium douthitti, on deer mouse (Peromyscus maniculatus) physiology, behavior and energetics. Measures were taken to assess direct parasite pathology as well as potential host plasticity used to reduce the costs of these pathologies. Parasitized mice had increased liver and spleen masses, as well as decreased liver protein synthesis. Parasitism also led to increased gastrointestinal (GI) mass, either directly due to parasite presence or as host compensation for decreased GI function. No additional plasticity was recorded - infected animals did not consume more food, decrease in body mass or reduce their activity. Parasitism led to reduced thermoregulation during short-term cold exposure, indicating that there may be fitness costs of parasitism. There were no changes in the other measures of energetics taken here, namely basal metabolic rate (BMR) and cold-induced maximal metabolic rate (MRmax). Together, the results suggest that many costs of parasite infection are largely ameliorated through physiological or morphological compensatory mechanisms.

State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta).

SUMMARY Energy allocation among somatic maintenance, reproduction and growth varies not only among species, but among individuals according to states such as age, sex and season. Little research has been conducted on the somatic (physiological) maintenance of long-lived organisms, particularly ectotherms such as reptiles. In this study, we examined sex differences and age- and season-related variation in immune function and DNA repair efficiency in a long-lived reptile, the painted turtle (Chrysemys picta). Immune components tended to be depressed during hibernation, in winter, compared with autumn or spring. Increased heterophil count during hibernation provided the only support for winter immunoenhancement. In juvenile and adult turtles, we found little evidence for senescence in physiological maintenance, consistent with predictions for long-lived organisms. Among immune components, swelling in response to phytohemagglutinin (PHA) and control injection increased with age, whereas basophil count decreased with age. Hatchling turtles had reduced basophil counts and natural antibodies, indicative of an immature immune system, but demonstrated higher DNA repair efficiency than older turtles. Reproductively mature turtles had reduced lymphocytes compared with juvenile turtles in the spring, presumably driven by a trade-off between maintenance and reproduction. Sex had little influence on physiological maintenance. These results suggest that components of physiological maintenance are modulated differentially according to individual state and highlight the need for more research on the multiple components of physiological maintenance in animals of variable states.

SEX ALLOCATION BASED ON RELATIVE AND ABSOLUTE CONDITION

Traditional models predict that organisms should allocate to sex based on their condition relative to the condition of their competitors, tracking shifts in mean condition in fluctuating environments, and maintaining an equilibrium sex ratio. In contrast, when individuals are constrained to define their condition absolutely, environmental fluctuations induce fluctuating sex ratios and the evolutionary loss of condition‐dependent sex allocation in short‐lived organisms. Here, we present a simulation model of temperature‐dependent sex determination (TSD) in fluctuating environments that specifically examines the importance of relativity in defining individual condition. When relativity in condition is allowed to evolve, short‐lived organisms evolve switchlike TSD reaction norms and define their condition relative to the annual temperature distribution, thus preventing biased cohort sex ratios in extreme years. Long‐lived organisms also evolve switchlike reaction norms, but define condition less relatively and experience biased cohort sex ratios. The predictions are supported by data from painted turtles, where TSD reaction norms exhibit pivotal temperatures of sex determination that partially track mean annual temperature. Examining relativity in amniotic vertebrates provides a conceptual framework for multifactorial sex determination and suggests new ways of exploring adaptive hypotheses of sex allocation by focusing on the importance of frequency‐dependent selection on sex.

Offspring sex varies with maternal investment ability: empirical demonstration based on cross-fostering

Despite decades of interest, adaptive explanations for biased offspring sex ratios in mammals remain contentious, largely because direct tests of the underlying fitness assumptions of adaptive hypotheses are rarely conducted. These tests are complicated by the difficulty of manipulating offspring sex prior to significant maternal investment owing to the biological constraints of viviparity. We test the adaptive advantage of sex allocation through cross-fostering offspring by sex in tammar wallabies. We examine whether offspring sex is correlated with maternal investment ability (i.e. Trivers–Willard hypothesis, TWH). In addition, we test the assumption that maternal investment has a greater influence on the fitness of sons than of daughters. We failed to find statistical support for maternal investment ability influencing a sons weaning success or body size more than a daughters, although this result was probably owing to small sample sizes. In support of the TWH, females that gave birth to a son had higher investment ability (likelihood of weaning an offspring) regardless of the sex of offspring fostered.

Maternal Condition and Facultative Sex Ratios in Populations with Overlapping Generations

Facultative investment in offspring sex is related to maternal condition in many organisms. In mammals, empirical support for condition‐dependent sex allocation is equivocal, and there is some doubt as to theoretical expectations. Much theory has been developed to make predictions for condition‐dependent sex ratios in populations with discrete generations. However, the extension of these predictions to populations with overlapping generations (OLGs; e.g., mammals) has been limited, leaving doubt as to the specific prediction for maternal‐condition‐dependent sex ratios in mammals. We develop a population genetics model that incorporates maternal effects on multiple offspring fitness components in a population with OLGs. Using a rare‐gene and evolutionarily stable strategy approach, we demonstrate that sex ratio predictions of this model are identical to those for equivalent discrete generations models. We show that the predicted sex ratios depend on the sex‐specific ratio of Ro (offspring lifetime fitness) for offspring of good and poor mothers. This offspring lifetime fitness rule indicates that empirical research on conditional sex ratios should consider all three components of offspring Ro (juvenile survival, adult life span, and fertility).