Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

Associations between adversity in the family of origin and hair cortisol concentration in adulthood.

The current study examined associations between parental adversities as experienced in adolescence and hair cortisol concentration (HCC) 26 years later (n = 47). Specifically, bivariate correlations and linear regressions were used to examine harsh parenting as well as parental economic pressure, emotional distress, and body mass index (BMI) when their adolescent was between 15 and 16 years old (parent average age 43). HCC was measured when the adolescent was an adult (average 42 years old), at a similar age to when their parent(s) first participated in the study. We also assessed their economic pressure, emotional distress, obesity, and perceived stress in adulthood. For results across generations, parental economic pressure experienced during adolescence was significantly related to HCC when these adolescents were adults. None of the adult economic pressure, emotional distress, BMI, and perceived stress variables were associated with their HCC. Interestingly, there were significant associations among adult perceived stress, economic pressure, emotional distress, and obesity. Thus, the association between parental economic pressure and adult HCC is independent of adult adversities. Results highlight early economic adversity as a possible childhood stressor that has implications throughout the life course.

Transgenerational effects of maternal corticosterone across early life in a viviparous snake.

Glucocorticoids (GCs) are central mediators of vertebrate responses to intrinsic and extrinsic stimuli. Among the sources of variation in circulating GCs are transgenerational effects mediated by mothers. Here we studied potential maternal effects mediated by GCs on offspring phenotype in a live-bearing reptile, the western terrestrial garter snake (Thamnophis elegans). We evaluated the association between baseline corticosterone (CORT) levels during gestation (i.e., preparturition) in field-captured mothers and 1) reproductive success and offspring sex ratios, 2) birth phenotypic traits of offspring born under common-garden laboratory conditions, and 3) neonate (age 3 months) and juvenile (age 12 months) traits of offspring raised under two thermal regimes ('warm' and 'cool') during their first year of life. Reproductive success and offspring sex ratios were not associated with preparturition maternal CORT, but pregnant snakes with higher CORT levels gave birth to smaller, lighter offspring, which tended to grow faster to age three months. Neonate baseline CORT varied with preparturition maternal CORT in a sex-specific manner (positive trend for females, negative for males). Maternal CORT effects on offspring phenotype were no longer detectable in juveniles at age one year. Instead, juvenile phenotypes were most influenced by rearing environment, with offspring raised under the cool regime showing higher baseline CORT and slower growth than those raised under warmer conditions. Our findings support the notion that offspring phenotype might be continuously adjusted in response to environmental cues -both pre- and post-natal- and that the strength of maternal CORT effects declines as offspring develop and experience unique environmental challenges. Our results contribute to a growing literature on transgenerational effects of hormones and help to fill a gap in our knowledge of these effects in ectothermic amniotes.

Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae).

BACKGROUND: The progressive deregulation of the immune system with age, termed immunosenescence, has been well studied in mammalian systems, but studies of immune function in long-lived, wild, non-mammalian populations are scarce. In this study we leverage a 38-year mark-recapture study to quantify the relationships among age, sex, survival, reproductive output and the innate immune system in a long-lived reptile, yellow mud turtles (Kinosternon flavescens; Testudines; Kinosternidae). METHODS: We estimated rates of survival and age-specific mortality by sex based on mark-recapture data for 1530 adult females and 860 adult males over 38 years of captures. We analyzed bactericidal competence (BC), and two immune responses to foreign red blood cells - natural antibody-mediated haemagglutination (NAbs), and complement-mediated haemolysis ability (Lys) - in 200 adults (102 females; 98 males) that ranged from 7 to 58 years of age captured in May 2018 during their emergence from brumation, and for which reproductive output and long-term mark-recapture data were available. RESULTS: We found that females are smaller and live longer than males in this population, but the rate of accelerating mortality across adulthood is the same for both sexes. In contrast, males exhibited higher innate immunity than females for all three immune variables we measured. All immune responses also varied inversely with age, indicating immunosenescence. For females that reproduced in the preceding reproductive season, egg mass (and therefore total clutch mass) increased with age,. In addition to immunosenescence of bactericidal competence, females that produced smaller clutches also had lower bactericidal competence. CONCLUSIONS: Contrary to the general vertebrate pattern of lower immune responses in males than females (possibly reflecting the suppressive effects of androgens), we found higher levels of all three immune variables in males. In addition, contrary to previous work that found no evidence of immunosenescence in painted turtles or red-eared slider turtles, we found a decrease in bactericidal competence, lysis ability, and natural antibodies with age in yellow mud turtles.

Over a decade of field physiology reveals life-history specific strategies to drought in garter snakes (Thamnophis legans).

Changing climates and severe weather events can affect population viability. Individuals need to buffer such negative fitness consequences through physiological plasticity. Whether certain life-history strategies are more conducive to surviving changing climates is unknown, but theory predicts that strategies prioritizing maintenance and survival over current reproduction should be better able to withstand such change. We tested this hypothesis in a meta-population of garter snakes having naturally occurring variation in life-history strategies. We tested whether slow pace-of-life (POL) animals, that prioritize survival over reproduction, are more resilient than fast POL animals as measured by several physiological biomarkers. From 2006 to 2019, which included two multi-year droughts, baseline and stress-induced reactivity of plasma corticosterone and glucose varied annually with directionalities consistent with life-history theory. Slow POL animals exhibited higher baseline corticosterone and lower baseline glucose, relative to fast POL animals. These patterns were also observed in stress-induced measures; thus, reactivity was equivalent between ecotypes. However, in drought years, measures of corticosterone did not differ between different life histories. Immune cell distribution showed annual variation independent of drought or life history. These persistent physiological patterns form a backdrop to several extirpations of fast POL populations, suggesting a limited physiological toolkit to surviving periods of extreme drought.

Multiple Paternity in Garter Snakes With Evolutionarily Divergent Life Histories.

Many animal species exhibit multiple paternity, defined as multiple males genetically contributing to a single female reproductive event, such as a clutch or litter. Although this phenomenon is well documented across a broad range of taxa, the underlying causes and consequences remain poorly understood. For example, it is unclear how multiple paternity correlates with life-history strategies. Furthermore, males and females may differ in mating strategies and these patterns may shift with ecological context and life-history variation. Here, we take advantage of natural life-history variation in garter snakes (Thamnophis elegans) to address these questions in a robust field setting where populations have diverged along a slow-to-fast life-history continuum. We determine both female (observed) and male (using molecular markers) reproductive success in replicate populations of 2 life-history strategies. We find that despite dramatic differences in annual female reproductive output: 1) females of both life-history ecotypes average 1.5 sires per litter and equivalent proportions of multiply-sired litters, whereas 2) males from the slow-living ecotype experience greater reproductive skew and greater variance in reproductive success relative to males from the fast-living ecotype males despite having equivalent average reproductive success. Together, these results indicate strong intrasexual competition among males, particularly in the fast-paced life-history ecotype. We discuss these results in the context of competing hypotheses for multiple paternity related to population density, resource variability, and life-history strategy.

Surviving winter: Physiological regulation of energy balance in a temperate ectotherm entering and exiting brumation.

Characterizing the physiological response to prolonged cold exposure is essential for understanding the maintenance of long-term energy balance. As part of their natural life cycle, temperate ectotherms are often exposed to seasonal variation in temperatures, including extended periods of cold well below their activity range. Relatively little is known about variation in physiological responses as vertebrate ectotherms enter and exit brumation in response to sustained cold temperatures. We tested the influence of temperature on physiology before, during, and after a simulated brumation in the checkered garter snake (Thamnophis marcianus), a widespread ectothermic vertebrate. We tested for the relative effect of immediate temperature and physiological context (entering or exiting brumation) on hormones regulating energy balance, indicators of energy availability, and resting metabolic rate (V̇O2). Plasma corticosterone, glucose, and insulin, as well as immune cell heterophil: lymphocyte ratios responded to temperature, though they did so with different thermal response curves. Thermal sensitivity varied both among and within physiological measures depending on whether animals were going into or coming out of brumation. Additionally, V̇O2 was regulated beyond simple temperature-dependence, whereby post-brumation measures were depressed relative to pre-brumation measures at the same temperature. This pattern was characterized by a change in the temperature coefficient (Q10), with a larger pre-brumation Q10, suggesting reduced thermal sensitivity of metabolic rate following a period of extended cold exposure. The integrated physiological response presented here demonstrates not only temperature dependence across physiological axes, but seasonal variation in thermal responsiveness. Our results suggest that energy allocation decisions and hormonal regulation of underlying processes promote differing levels of thermal sensitivity when entering or exiting brumation.

Immunosenescence and its influence on reproduction in a long-lived vertebrate.

Immunosenescence is a well-known phenomenon in mammal systems, but its relevance in other long-lived vertebrates is less understood. Further, the influence of age and reproductive effort on immune function in long-lived species can be challenging to assess, as long-term data are scarce and it is often difficult to sample the oldest age classes. We used the painted turtle (Chrysemys picta) to test hypotheses of immunosenescence and a trade-off between reproductive output and immune function in a population of a long-lived vertebrate that has been monitored for over 30 years. These long-term data were utilized to employ a unique approach of aging turtles with mark-recapture data and population-specific growth modeling to obtain more accurate estimates of age. We analyzed natural antibodies, lysis ability and bactericidal competence in 126 individuals from 1 to 33 years of age captured during May and June 2011. Older turtles exhibited greater natural antibody levels than young individuals. Young females with large clutches exhibited greater lysis ability, while older females with large clutches had decreased lysis ability, suggesting a trade-off between reproductive output and immune function conditional upon age. However, bactericidal competence increased later in the nesting season for older females. Our study rejects the hypothesis of immunosenescence in a long-lived turtle, despite evidence of actuarial and reproductive senescence in this population. Additionally, we detected mixed evidence for a trade-off between reproduction and immune health.

Genetic background and thermal environment differentially influence the ontogeny of immune components during early life in an ectothermic vertebrate.

An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G) and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alterations in temperature regimes have been implicated in emergent disease outbreaks, making it a critical environmental factor to study in the context of immune phenotype determinants of wild animals. We assessed the relative influences of environmental temperature, genetic background and their interaction on first-year development of innate and adaptive immune defences of captive-born garter snakes Thamnophis elegans using a reciprocal transplant laboratory experiment. We used a full-factorial design with snakes from two divergent life-history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime-that is, warmer and cooler-of each habitat. Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune-component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast- and the slow-paced life-history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development. Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune-component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

Effects of early nutritional stress on physiology, life histories and their trade-offs in a model ectothermic vertebrate.

Early-life experiences can have far-reaching consequences for phenotypes into adulthood. The effect of early-life experiences on fitness, particularly under adverse conditions, is mediated by resource allocation to particular life-history traits. Reptiles exhibit great variation in life histories (e.g. indeterminate growth), thus selective pressures often mitigate the effects of early-life stress, particularly on growth and maturation. We examined the effects of early-life food restriction on growth, adult body size, physiology and reproduction in the checkered garter snake. Animals were placed on one of two early-life diet treatments: normal diet (approximating ad libitum feeding) or low diet (restricted to 20% of body mass in food weekly). At 15 weeks of age, low-diet animals were switched to the normal-diet treatment. Individuals fed a restricted diet showed reduced growth rates, depressed immunocompetence and a heightened glucocorticoid response. Once food restriction was lifted, animals experiencing nutritional stress early in life (low diet) caught up with the normal-diet group by increasing their growth, and were able to recover from the negative effects of nutritional stress on immune function and physiology. Growth restriction and the subsequent allocation of resources into increasing growth rates, however, had a negative effect on fitness. Mating success was reduced in low-diet males, while low-diet females gave birth to smaller offspring. In addition, although not a direct goal of our study, we found a sex-specific effect of early-life nutritional stress on median age of survival. Our study demonstrates both immediate and long-term effects of nutritional stress on physiology and growth, reproduction, and trade-offs among them.

Decades of field data reveal that turtles senesce in the wild.

Lifespan and aging rates vary considerably across taxa; thus, understanding the factors that lead to this variation is a primary goal in biology and has ramifications for understanding constraints and flexibility in human aging. Theory predicts that senescence-declining reproduction and increasing mortality with advancing age-evolves when selection against harmful mutations is weaker at old ages relative to young ages or when selection favors pleiotropic alleles with beneficial effects early in life despite late-life costs. However, in many long-lived ectotherms, selection is expected to remain strong at old ages because reproductive output typically increases with age, which may lead to the evolution of slow or even negligible senescence. We show that, contrary to current thinking, both reproduction and survival decline with adult age in the painted turtle, Chrysemys picta, based on data spanning >20 y from a wild population. Older females, despite relatively high reproductive output, produced eggs with reduced hatching success. Additionally, age-specific mark-recapture analyses revealed increasing mortality with advancing adult age. These findings of reproductive and mortality senescence challenge the contention that chelonians do not age and more generally provide evidence of reduced fitness at old ages in nonmammalian species that exhibit long chronological lifespans.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Sex-specific growth, shape, and their impacts on the life history of a long-lived vertebrate.

BACKGROUND: Individual growth rates both comprise and determine life-history phenotypes. Despite decades of interest in understanding the relationship between individual growth and life history, chelonian longevity has limited our ability to robustly estimate individual growth curves that span the life of both sexes. QUESTIONS: (1) Do patterns of growth in size and shape differ between the sexes of the painted turtle, Chrysemys picta? (2) Does individual variation in size and shape affect female reproductive effort? METHODS: Using 30 years of field data on shell morphology of a single population of painted turtles, we used principal components analysis to summarize multivariate size and shape. We assessed the ability of three non-linear growth models - the logistic, Gompertz, and von Bertalanffy - to predict size-at-age and used model comparison to justify sex-specific model fits. We correlated age-specific size and shape of females with their reproductive efforts. RESULTS: Model comparison supported separate fits of the von Bertalanffy growth function for each sex; non-overlapping confidence intervals imply differences in sex-specific asymptotic size, but not growth rate. Higher-order axes of variation in shell morphology described significant sexual dimorphism in shell shape related to the sphericity and curviness of the shell. Shell sphericity of females covaried with clutch size, mean egg mass, and total clutch mass. Irrespective of shell morphology, we found evidence of an egg number versus egg mass trade-off. Yet, females who matured at a larger size produced greater reproductive efforts.

Rapid molecular evolution across amniotes of the IIS/TOR network.

The insulin/insulin-like signaling and target of rapamycin (IIS/TOR) network regulates lifespan and reproduction, as well as metabolic diseases, cancer, and aging. Despite its vital role in health, comparative analyses of IIS/TOR have been limited to invertebrates and mammals. We conducted an extensive evolutionary analysis of the IIS/TOR network across 66 amniotes with 18 newly generated transcriptomes from nonavian reptiles and additional available genomes/transcriptomes. We uncovered rapid and extensive molecular evolution between reptiles (including birds) and mammals: (i) the IIS/TOR network, including the critical nodes insulin receptor substrate (IRS) and phosphatidylinositol 3-kinase (PI3K), exhibit divergent evolutionary rates between reptiles and mammals; (ii) compared with a proxy for the rest of the genome, genes of the IIS/TOR extracellular network exhibit exceptionally fast evolutionary rates; and (iii) signatures of positive selection and coevolution of the extracellular network suggest reptile- and mammal-specific interactions between members of the network. In reptiles, positively selected sites cluster on the binding surfaces of insulin-like growth factor 1 (IGF1), IGF1 receptor (IGF1R), and insulin receptor (INSR); whereas in mammals, positively selected sites clustered on the IGF2 binding surface, suggesting that these hormone-receptor binding affinities are targets of positive selection. Further, contrary to reports that IGF2R binds IGF2 only in marsupial and placental mammals, we found positively selected sites clustered on the hormone binding surface of reptile IGF2R that suggest that IGF2R binds to IGF hormones in diverse taxa and may have evolved in reptiles. These data suggest that key IIS/TOR paralogs have sub- or neofunctionalized between mammals and reptiles and that this network may underlie fundamental life history and physiological differences between these amniote sister clades.

Physiology at near-critical temperatures, but not critical limits, varies between two lizard species that partition the thermal environment.

The mechanisms that mediate the interaction between the thermal environment and species ranges are generally uncertain. Thermal environments may directly restrict species when environments exceed tolerance limits (i.e. the fundamental niche). However, thermal environments might also differentially affect relative performance among species prior to fundamental tolerances being met (i.e. the realized niche). We examined stress physiology (plasma glucose and corticosterone), mitochondrial performance and the muscle metabolome of congeneric lizards that naturally partition the thermal niche, Elgaria multicarinata (southern alligator lizards; SALs) and Elgaria coerulea (northern alligator lizards; NALs), in response to a thermal challenge to quantify variation in physiological performance and tolerance. Both NAL and SAL displayed physiological stress in response to high temperature, but neither showed signs of irreversible damage. NAL displayed a higher baseline mitochondrial respiration rate than SAL. Moreover, NAL substantially adjusted their physiology in response to thermal challenge, whereas SAL did not. For example, the metabolite profile of NAL shifted with changes in key energetic molecules, whereas these were unaffected in SAL. Our results indicate that near-critical high temperatures should incur greater energetic cost in NAL than SAL via an elevated metabolic rate and changes to the metabolome. Thus, SAL displace NAL in warm environments that are within NAL's fundamental thermal niche, but relatively costly. Our results suggest that subcritical thermal events can contribute to biogeographic patterns via physiological differences that alter the relative costs of living in warm or cool environments.

Geographic variation and within-individual correlations of physiological stress markers in a widespread reptile, the common garter snake (Thamnophis sirtalis).

Characterizing the baseline and stress-induced hormonal, metabolite, and immune profiles of wild animals is important to assess the impacts of variable environments, including human-induced landscape changes, on organismal health. Additionally, the extent to which these profiles are coordinated across physiological systems within individuals remains an important question in understanding how stressors can differentially affect aspects of an individual's physiology. Here, we present data from wild populations of the common garter snake (Thamnophis sirtalis) on both baseline and stress-induced biomarkers: plasma corticosterone (CORT) concentration, plasma glucose concentration, and whole blood heterophil:lymphocyte ratio. Using a standardized restraint protocol with individuals from populations in disparate portions of this species' range - the Sierra Nevada Mountains of California and the plains of Iowa - we collected blood plasma samples at nine time points over three days. Both CORT and glucose response curves differed between georegions, with Iowa snakes attaining higher glucose concentration and maintaining elevated CORT and glucose levels for a longer duration. Additionally, both the total amount and proportional increases of CORT and glucose were lower in larger and therefore older snakes, suggesting ontogenetic shifts in stress perception or response. Within-individual correlation among the three physiological indicators was significant at the time of capture, absent after 3h in captivity, and partially restored after 3days in captivity, demonstrating the effect of stress on the relationships among these physiological systems. Together, these results provide further evidence for the great physiological flexibility of ectothermic tetrapods in maintaining homeostasis across a range of factors.

Hormonal and metabolic responses to upper temperature extremes in divergent life-history ecotypes of a garter snake.

Extreme temperatures constrain organismal physiology and impose both acute and chronic effects. Additionally, temperature-induced hormone-mediated stress response pathways and energetic trade-offs are important drivers of life-history variation. This study employs an integrative approach to quantify acute physiological responses to high temperatures in divergent life-history ecotypes of the western terrestrial garter snake (Thamnophis elegans). Using wild-caught animals, we measured oxygen consumption rate and physiological markers of hormonal stress response, energy availability and anaerobic respiration in blood plasma across five ecologically relevant temperatures (24, 28, 32, 35 and 38°C; 3 h exposure). Corticosterone, insulin and glucose concentrations all increased with temperature, but with different thermal response curves, suggesting that high temperatures differently affect energy-regulation pathways. Additionally, oxygen consumption rate increased without plateau and lactate concentration did not increase with temperature, challenging the recent hypothesis that oxygen limitation sets upper thermal tolerance limits. Finally, animals had similar physiological thermal responses to high-temperature exposure regardless of genetic background, suggesting that local adaptation has not resulted in fixed differences between ecotypes. Together, these results identify some of the mechanisms by which higher temperatures alter hormonal-mediated energy balance in reptiles and potential limits to the flexibility of this response.

Insulin-like signaling (IIS) responses to temperature, genetic background, and growth variation in garter snakes with divergent life histories.

The insulin/insulin-like signaling pathway (IIS) has been shown to mediate life history trade-offs in mammalian model organisms, but the function of this pathway in wild and non-mammalian organisms is understudied. Populations of western terrestrial garter snakes (Thamnophis elegans) around Eagle Lake, California, have evolved variation in growth and maturation rates, mortality senescence rates, and annual reproductive output that partition into two ecotypes: "fast-living" and "slow-living". Thus, genes associated with the IIS network are good candidates for investigating the mechanisms underlying ecological divergence in this system. We reared neonates from each ecotype for 1.5years under two thermal treatments. We then used qPCR to compare mRNA expression levels in three tissue types (brain, liver, skeletal muscle) for four genes (igf1, igf2, igf1r, igf2r), and we used radioimmunoassay to measure plasma IGF-1 and IGF-2 protein levels. Our results show that, in contrast to most mammalian model systems, igf2 mRNA and protein levels exceed those of igf1 and suggest an important role for igf2 in postnatal growth in reptiles. Thermal rearing treatment and recent growth had greater impacts on IGF levels than genetic background (i.e., ecotype), and the two ecotypes responded similarly. This suggests that observed ecotypic differences in field measures of IGFs may more strongly reflect plastic responses in different environments than evolutionary divergence. Future analyses of additional components of the IIS pathway and sequence divergence between the ecotypes will further illuminate how environmental and genetic factors influence the endocrine system and its role in mediating life history trade-offs.

Reproductive aging patterns in primates reveal that humans are distinct.

Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.