Differential effects of early life adversity on male and female rhesus macaque lifespan.

Early life adversity predicts shorter adult lifespan in several animal taxa. Yet, work on long-lived primate populations suggests the evolution of mechanisms that contribute to resiliency and long lives despite early life insults. Here, we tested associations between individual and cumulative early life adversity and lifespan on rhesus macaques at the Cayo Santiago Biological Field Station using 50 years of demographic data. We performed sex-specific survival analyses at different life stages to contrast short-term effects of adversity (i.e., infant survival) with long-term effects (i.e., adult survival). Female infants showed vulnerability to multiple adversities at birth, but affected females who survived to adulthood experienced a reduced risk later in life. In contrast, male infants showed vulnerability to a lower number of adversities at birth, but those who survived to adulthood were negatively affected by both early life individual and cumulative adversity. Our study shows profound immediate effects of insults  on female infant cohorts and suggests that affected female adults are more robust. In contrast, adult males who experienced harsh conditions early in life showed an increased mortality risk at older ages as expected from hypotheses within the life course perspective. Our analysis suggests sex-specific selection pressures on life histories and highlights the need for studies addressing the effects of early life adversity across multiple life stages.

Advancing methods for the biodemography of aging within social contexts.

Several social dimensions including social integration, status, early-life adversity, and their interactions across the life course can predict health, reproduction, and mortality in humans. Accordingly, the social environment plays a fundamental role in the emergence of phenotypes driving the evolution of aging. Recent work placing human social gradients on a biological continuum with other species provides a useful evolutionary context for aging questions, but there is still a need for a unified evolutionary framework linking health and aging within social contexts. Here, we summarize current challenges to understand the role of the social environment in human life courses. Next, we review recent advances in comparative biodemography and propose a biodemographic perspective to address socially driven health phenotype distributions and their evolutionary consequences using a nonhuman primate population. This new comparative approach uses evolutionary demography to address the joint dynamics of populations, social dimensions, phenotypes, and life history parameters. The long-term goal is to advance our understanding of the link between individual social environments, population-level outcomes, and the evolution of aging.

Hurricanes affect diversification among individual life courses of a primate population.

Extreme climatic events may influence individual-level variability in phenotypes, survival and reproduction, and thereby drive the pace of evolution. Climate models predict increases in the frequency of intense hurricanes, but no study has measured their impact on individual life courses within animal populations. We used 45 years of demographic data of rhesus macaques to quantify the influence of major hurricanes on reproductive life courses using multiple metrics of dynamic heterogeneity accounting for life course variability and life-history trait variances. To reduce intraspecific competition, individuals may explore new reproductive stages during years of major hurricanes, resulting in higher temporal variation in reproductive trajectories. Alternatively, individuals may opt for a single optimal life-history strategy due to trade-offs between survival and reproduction. Our results show that heterogeneity in reproductive life courses increased by 4% during years of major hurricanes, despite a 2% reduction in the asymptotic growth rate due to an average decrease in mean fertility and survival by that is, shortened life courses and reduced reproductive output. In agreement with this, the population is expected to achieve stable population dynamics faster after being perturbed by a hurricane ( ρ = 1.512 ; 95% CI: 1.488, 1.538), relative to ordinary years ρ = 1.482 ; 1.475 , 1.490 . Our work suggests that natural disasters force individuals into new demographic roles to potentially reduce competition during unfavourable environments where mean reproduction and survival are compromised. Variance in lifetime reproductive success and longevity are differently affected by hurricanes, and such variability is mostly driven by survival.

Rhesus macaques compensate for reproductive delay following ecological adversity early in life.

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and life span. However, long-lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter life spans. Here, we quantify the effects of major hurricanes and density dependence as sources of early-life ecological adversity on Cayo Santiago rhesus macaque female reproduction and decompose their effects onto the mean age-specific fertility, reproductive pace, and lifetime reproductive success (LRS). Females experiencing major hurricanes exhibit a delayed reproductive debut but maintain the pace of reproduction past debut and show a higher mean fertility during prime reproductive ages, relative to unaffected females. Increasing density at birth is associated to a decrease in mean fertility and reproductive pace, but such association is absent at intermediate densities. When combined, our study reveals that hurricanes early in life predict a delay-overshoot pattern in mean age-specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, this long-lived population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no major negative fitness outcomes. Density presents a more complex relation with reproduction that suggests females experiencing a population regulated at intermediate densities early in life will escape density dependence and show optimized reproductive schedules. Our results support hypotheses about life history trade-offs in which adversity-affected females ensure their future reproductive potential by allocating more energy to growth or maintenance processes at younger adult ages.

Demographic consequences of changing body size in a terrestrial salamander.

Changes in climate can alter individual body size, and the resulting shifts in reproduction and survival are expected to impact population dynamics and viability. However, appropriate methods to account for size-dependent demographic changes are needed, especially in understudied yet threatened groups such as amphibians. We investigated individual- and population-level demographic effects of changes in body size for a terrestrial salamander using capture-mark-recapture data. For our analysis, we implemented an integral projection model parameterized with capture-recapture likelihood estimates from a Bayesian framework. Our study combines survival and growth data from a single dataset to quantify the influence of size on survival while including different sources of uncertainty around these parameters, demonstrating how selective forces can be studied in populations with limited data and incomplete recaptures. We found a strong dependency of the population growth rate on changes in individual size, mediated by potential changes in selection on mean body size and on maximum body size. Our approach of simultaneous parameter estimation can be extended across taxa to identify eco-evolutionary mechanisms acting on size-specific vital rates, and thus shaping population dynamics and viability.

Hurricane-induced demographic changes in a non-human primate population.

Major disturbance events can have large impacts on the demography and dynamics of animal populations. Hurricanes are one example of an extreme climatic event, predicted to increase in frequency due to climate change, and thus expected to be a considerable threat to population viability. However, little is understood about the underlying demographic mechanisms shaping population response following these extreme disturbances. Here, we analyse 45 years of the most comprehensive free-ranging non-human primate demographic dataset to determine the effects of major hurricanes on the variability and maintenance of long-term population fitness. For this, we use individual-level data to build matrix population models and perform perturbation analyses. Despite reductions in population growth rate mediated through reduced fertility, our study reveals a demographic buffering during hurricane years. As long as survival does not decrease, our study shows that hurricanes do not result in detrimental effects at the population level, demonstrating the unbalanced contribution of survival and fertility to population fitness in long-lived animal populations.

Unexpected spatial population ecology of a widespread terrestrial salamander near its southern range edge.

Under the current amphibian biodiversity crisis, common species provide an opportunity to measure population dynamics across a wide range of environmental conditions while examining the processes that determine abundance and structure geographical ranges. Studying species at their range limits also provides a window for understanding the dynamics expected in future environments under increasing climate change and human modification. We quantified patterns of seasonal activity, density and space use in the eastern red-backed salamander (Plethodon cinereus) near its southern range edge and compare the spatial ecology of this population to previous findings from the core of their range. This southern population shows the expected phenology of surface activity based on temperature limitations in warmer climates, yet maintains unexpectedly high densities and large home ranges during the active season. Our study suggests that ecological factors known to strongly affect amphibian populations (e.g. warm temperature and forest fragmentation) do not necessarily constrain this southern population. Our study highlights the utility of studying a common amphibian as a model system for investigating population processes in environments under strong selective pressure.

Drivers of Diversification in Individual Life Courses.

Heterogeneity in life courses among individuals of a population influences the speed of adaptive evolutionary processes, but it is less clear how biotic and abiotic environmental fluctuations influence such heterogeneity. We investigate principal drivers of variability in sequence of stages during an individual's life in a stage-structured population. We quantify heterogeneity by measuring population entropy of a Markov chain, which computes the rate of diversification of individual life courses. Using individual data of a primate population, we show that density regulates the stage composition of the population but that its entropy and the generating moments of heterogeneity are independent of density. This lack of influence of density on heterogeneity is due to neither low year-to-year variation in entropy nor differences in survival among stages but is rather due to differences in stage transitions. Our analysis thus shows that well-known classical ecological selective forces, such as density regulation, are not linked to potential selective forces governing heterogeneity through underlying stage dynamics. Despite evolution acting heavily on individual variability in fitness components, our understanding is poor whether observed heterogeneity is adaptive and how it evolves and is maintained. Our analysis illustrates how entropy represents a more integrated measure of diversity compared to the population structural composition, giving us new insights about the underlying drivers of individual heterogeneity within populations and potential evolutionary mechanisms.

The Population Genetic Composition of Conventional and SPF Colonies of Rhesus Macaques (Macaca mulatta) at the Caribbean Primate Research Center.

The SPF breeding program at the Caribbean Primate Research Center supplies Indian-origin rhesus macaques of known genetic and virologic background for biomedical research. In this study, population genetic analyses using 14 short tandem-repeat sequences showed that the SPF colony has remained genetically homogenous over time, with sufficient amounts of heterozygosity and minimal stratification from its founders. Intergenerational studies indicated that an average of 7 alleles have been retained, inbreeding levels have remained low, and the degree of Indian ancestry is one of the highest among several national primate research centers. The relative low genetic diversity in the free-ranging population as well as in the captive SPF and conventional colonies when compared with that of other primate centers indicates that the free-ranging population, from which the captive-colony animals were derived, has experienced significant founder effects and genetic drift during the years after its establishment. This study supports the historical origin of the free-ranging population and confirms the high value of this resource for biomedical research. Current genetic diversity levels within the SPF colony can be ensured with the practice of colony management approaches such as equalizing male:female ratios in each SPF breeding group and increasing breeding group sizes. Introducing new Indian-origin macaques from other captive colonies might help to maximize the genetic diversity of the breeding stock. Furthermore, genetic estimates must be used to rank breeders according to their genetic value or their genome uniqueness to increase founder-genome representation and curb future genetic bottlenecks and allele loss.

Managing the Cayo Santiago rhesus macaque population: The role of density.

Cayo Santiago is the oldest continuously operating free-ranging rhesus monkey colony in the world. Population control of this colony has historically been carried out by periodic live capture and removal of animals. However, the effect of such a strategy on the size, growth rate, age structure, and sex ratio of the population has not been analyzed. This study reviews past removal data and uses a population projection model to simulate the effects of different removal schemes based on Cayo Santiago demographic data from 2000-2012. The model incorporates negative density-dependence in female fertility, as well as male and female survival rates, to determine the population-level effects of selective removal by age and sex. Modeling revealed that removal of sexually immature individuals has negligible effects on the population dynamics explaining why with an initial population of 1309 in 2000 and annual removals of immature monkeys a mean annual population growth rate of 12% and a final population size of ∼1,435 individuals by 2012 (∼0.009 animal/m(2) ) was observed. With no removals, the population is expected to exhibit dampened oscillations until reaching equilibrium at ∼1,690 individuals (∼0.0111 animal/m(2) ) in 2,100. In contrast, removal of adult females (≥4 yrs) would significantly reduce the population size, but would also promote an increase in population growth rate due to density feedback. A maximum annual production of 275 births is expected when 550 adult females are present in the population. Sensitivity analyses showed that removing females, in contrast to controlling their fertility through invasive treatments would contribute the most to changes in population growth rate. Given the density compensation on fertility, stabilizing the population would require removing ∼80% of the current population of adult females. This study highlights the importance of addressing the population-level density effects, as well as sensitivity analyses, to optimize management strategies.

Discovery of a secular trend in Cayo Santiago macaque reproduction.

Reproductive synchrony and the consequent clustering of births are hypothesized to be regulated by seasonal changes in rainfall and food availability. Such climate-related seasonality is, however, questionable in tropical populations occupying temporally invariant habitats year round. Using the long-term data of the Cayo Santiago rhesus macaques from 1973 to 2013, this study distinguishes synchrony (a greater than chance clustering of births) from seasonality (a cluster of births during a period of the year when abiotic conditions are favorable) and shows that females are highly synchronized (>72% of births in a 3-month period) but the effects of environmental zeitgebers on reproduction are overridden by biological factors. Specifically, biotic and abiotic factors including (i) loss of immature offspring; (ii) population density; (iii) age at delivery; (iv) rainfall; and (v) changes in colony management were modeled in relation to the annual onset of births and the median birth date. Females experiencing loss of immature offspring had an interbirth interval of <365 days in average and the proportion of these females increased up to 48% due to changes in colony management overtime, although reproductive synchrony increased with increasing population density. A secular trend in both the onset of births and the median date of birth is documented and the model predicts that the median birth date will advance across all calendar-based seasons by 2050. The secular trend in reproduction appears to be triggered by changes in the age at delivery of females, the absence of physiological constraints from maternal investment due to offspring loss, shorter interbirth interval, and a higher degree of coordination due to increasing population density. This study challenges the reproductive phenology previously described for rhesus macaques highlighting the importance of long-term studies in addressing the ultimate causes of reproductive synchrony.

Long-term effects of tetanus toxoid inoculation on the demography and life expectancy of the Cayo Santiago rhesus macaques.

Tetanus was a major cause of mortality in the free-ranging population of rhesus monkeys on Cayo Santiago prior to 1985 when the entire colony was given its first dose of tetanus toxoid. The immediate reduction in mortality that followed tetanus toxoid inoculation (TTI) has been documented, but the long-term demographic effects of eliminating tetanus infections have not. This study uses the Cayo Santiago demographic database to construct comparative life tables 12 years before, and 12 years after, TTI. Life tables and matrix projection models are used to test for differences in: (i) survival among all individuals as well as among social groups, (ii) long-term fitness of the population, (iii) age distribution, (iv) reproductive value, and (v) life expectancy. A retrospective life table response experiment (LTRE) was performed to determine which life cycle transition contributed most to observed changes in long-term fitness of the population post-TTI. Elimination of clinical tetanus infections through mass inoculation improved the health and well-being of the monkeys. It also profoundly affected the population by increasing survivorship and long-term fitness, decreasing the differences in survival rates among social groups, shifting the population's age distribution towards older individuals, and increasing reproductive value and life expectancy. These findings are significant because they demonstrate the long-term effects of eradicating a major cause of mortality at a single point in time on survival, reproduction, and overall demography of a naturalistic population of primates.

Demographic variability and density-dependent dynamics of a free-ranging rhesus macaque population.

Density-dependence is hypothesized as the major mechanism of population regulation. However, the lack of long-term demographic data has hampered the use of density-dependent models in nonhuman primates. In this study, we make use of the long-term demographic data from Cayo Santiago's rhesus macaques to parameterize and analyze both a density-independent and a density-dependent population matrix model, and compare their projections with the observed population changes. We also employ a retrospective analysis to determine how variance in vital rates, and covariance among them, contributed to the observed variation in long-term fitness across different levels of population density. The population exhibited negative density-dependence in fertility and the model incorporating this relationship accounted for 98% of the observed population dynamics. Variation in survival and fertility of sexually active individuals contributed the most to the variation in long-term fitness, while vital rates displaying high temporal variability exhibited lower sensitivities. Our findings are novel in describing density-dependent dynamics in a provisioned primate population, and in suggesting that selection is acting to lower the variance in the population growth rate by minimizing the variation in adult survival at high density. Because density-dependent mechanisms may become stronger in wild primate populations due to increasing habitat loss and food scarcity, our study demonstrates that it is important to incorporate variation in population size, as well as demographic variability into population viability analyses for a better understanding of the mechanisms regulating the growth of primate populations.