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Petersen, R. M.

Publications and source records attributed to Petersen, R. M..

7 recordsLinked to original sources

Contrasting effects of forest fragmentation on the genetics and microbiomes of an endangered arboreal primate

Landscape fragmentation, one of the leading drivers of biodiversity loss, can reshape both the genetics and microbiomes of wild populations. Although fragmentation is generally expected to limit gene flow and erode genetic diversity, and to disrupt host-associated microbial communities, these responses arise via different pathways and may therefore diverge within the same population. To understand how fragmentation simultaneously shapes population genetics and gut microbiomes, we analyzed fecal-derived host genomic and microbiome data from endangered, arboreal black howler monkeys (Alouatta pigra) across a fragmentation gradient. We then integrated these data with measures of ecological connectivity, habitat quality, and demography to identify the drivers of genetic and microbiome variation and structure. Multivariate analyses indicated that genetic patterns were shaped by both connectivity and habitat quality, whereas microbiome variation was driven mainly by habitat quality. Contrary to expectations under reduced realized connectivity with increasing isolation, monkeys showed the strongest gene flow signal in the most fragmented region, and higher genetic diversity and lower inbreeding than monkeys in continuous forest. Relatedness and isolation-by-distance patterns suggested that fragmentation has sex-specific effects on movement, disrupting the usual pattern of short-range male dispersal in the most fragmented region. Gut microbiomes, however, showed predicted negative responses to fragmentation: individuals in highly fragmented habitat had lower microbial diversity and compositional shifts consistent with lower-quality diets and increased exposure to disturbed environments. These results show contrasting biological responses to fragmentation within a single population, with genetic patterns likely resulting from compensatory behavioral flexibility and microbiome patterns reflecting local habitat degradation. Our findings underscore the need for conservation assessments that integrate multiple dimensions of population health rather than relying on any single indicator of fragmentation impact.

ecology↗

Early life adversity shapes life history trade-offs between growth and reproduction in free-ranging rhesus macaques

Life history theory predicts that organisms allocate resources across physiological processes to maximize fitness. Under this framework, early life adversity (ELA)--which often limits energetic capital--could shape investment in growth and reproduction, as well as trade-offs between them, ultimately contributing to variation in evolutionary fitness. Using long-term demographic, behavioral, and physiological data for 2,100 females from a non-human primate population, we tested whether naturally-occurring ELA influences investment in the competing physiological demands of growth and reproduction. By analyzing ELA, growth, and reproduction in the same individuals, we also assessed whether adversity intensifies trade-offs between life history domains. We found that ELA influenced life history patterns, and was associated with modified growth, delayed reproductive maturity, and small adult body size. Different types of ELA sometimes had distinct reproductive outcomes--e.g., large group size was linked to faster reproductive rates, while low maternal rank predicted slower ones. Adversity also amplified trade-offs between growth and reproduction: small body size was a stronger predictor of delayed and reduced reproductive output in females exposed to ELA, compared to those not exposed. Finally, we examined how traits modified by ELA related to lifetime reproductive success. Across the population, starting reproduction earlier and maintaining a moderate reproductive rate conferred the greatest number of offspring surviving to reproductive maturity. These findings suggest that ELA impacts key life history traits as well as relationships between them, and can constrain individuals from adopting the most optimal reproductive strategy. Significance StatementEarly life adversity (ELA) can have lasting effects on evolutionary fitness (e.g., the number of surviving offspring an animal produces); however, the paths connecting ELA to fitness--for example by influencing growth, reproductive timing or rate, or trade-offs between these processes--remain unclear. Leveraging long-term behavioral, physiological, and demographic data from 2,100 female rhesus macaques, we found that ELA-exposed females exhibited growth and reproductive schedules associated with less-optimal lifetime fitness outcomes. Further, ELA intensified trade-offs between growth and reproduction, suggesting that affected individuals face steeper energetic constraints. Our findings highlight the long-lasting impacts of ELA on traits of evolutionary and biomedical importance in a non-human primate model with relevance to humans.

evolutionary biology↗

Genetically-based sperm discrimination in the vaginal tract of a primate species

Females influence offspring paternity through diverse pre- and post-copulatory mechanisms. Sperm discrimination--the differential physiological response to ejaculates based on male or sperm characteristics--can bias fertilization outcomes, but in vivo evidence of this process in large-bodied mammals is lacking. Here, we tested whether two aspects of female physiology that affect sperm survival-vaginal immune response and pH-are modulated by male genetic makeup in a nonhuman primate. We observed post-copulatory differences in vaginal gene expression and pH, with the strongest immune responses and largest pH decreases, harmful to sperm, exhibited by females mating with genetically similar males. These findings support genetically based post-copulatory mate discrimination in primates, shedding light on the interaction between male gametes and the female reproductive tract and potentially explaining variation in conception probability.

evolutionary biology↗

Early life environments shape adult cardiometabolic health during rapid lifestyle change

Early life environments can have long-lasting impacts on health and fitness, but the evolutionary significance of these effects remains debated. Two major classes of explanations have been proposed: developmental constraints (DC) explanations posit that early life adversity limits optimal development, leading to long-term costs, while predictive adaptive response (PAR) explanations posit that organisms use early life cues to predict adult conditions, resulting in detriments when adult environments do not match expectations. We tested these hypotheses using anthropological and biomedical data for the Orang Asli--the Indigenous peoples of Peninsular Malaysia--who are undergoing a rapid but heterogenous transition from non-industrial, subsistence-based livelihoods to more industrialized, market-integrated conditions. Using questionnaire data, we show that this shift creates natural variation in the degree of similarity between early life and adult environments. Using anthropometric and health data, we find that, more rural, subsistence-based early life environments are associated with shorter stature but better adult cardiometabolic health. Applying a quadratic regression framework, we find support for DC but not PAR in explaining adult cardiometabolic health, echoing findings and conclusions from other long-lived species. Overall, our results suggest that early life conditions can provide additive protection against common health issues associated with urban, industrialized lifestyle exposure.

evolutionary biology↗

Uncovering methylation-dependent genetic effects on regulatory element function in diverse genomes

A major goal in evolutionary biology and biomedicine is to understand the complex interactions between genetic variants, the epigenome, and gene expression. However, the causal relationships between these factors remain poorly understood. mSTARR-seq, a methylation-sensitive massively parallel reporter assay, is capable of identifying methylation-dependent regulatory activity at many thousands of genomic regions simultaneously, and allows for the testing of causal relationships between DNA methylation and gene expression on a region-by-region basis. Here, we developed a multiplexed mSTARR-seq protocol to assay naturally occurring human genetic variation from 25 individuals sampled from 10 localities in Europe and Africa. We identified 6,957 regulatory elements in either the unmethylated or methylated state, and this set was enriched for enhancer and promoter annotations, as expected. The expression of 58% of these regulatory elements was modulated by methylation, which was generally associated with decreased RNA expression. Within our set of regulatory elements, we used allele-specific expression analyses to identify 8,020 sites with genetic effects on gene regulation; further, we found that 42.3% of these genetic effects varied between methylated and unmethylated states. Sites exhibiting methylation-dependent genetic effects were enriched for GWAS and EWAS annotations, implicating them in human disease. Compared to datasets that assay DNA from a single European individual, our multiplexed assay uncovers dramatically more genetic effects and methylation-dependent genetic effects, highlighting the importance of including diverse individuals in assays which aim to understand gene regulatory processes.

genomics↗

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Exposure to adversity during early life is linked to lasting detrimental effects on evolutionary fitness across many taxa. However, due to the challenges of collecting longitudinal data, especially in species where one sex disperses, direct evidence from long-lived species remains relatively scarce. Here we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques (Macaca mulatta) at Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of ten forms of early life adversity for 6,599 macaques (3,230 male, 3,369 female), with a smaller sample size (N=299) for one form of adversity (maternal social isolation) which required high-resolution behavioral data. We found that individuals who experienced more early life adversity died earlier than those who experienced less adversity. Mortality risk was highest during early life, defined as birth to four years old, suggesting acute survival effects of adversity, but heightened mortality risk was also present in macaques who survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands, female philopatry, and male dispersal. By leveraging data on thousands of macaques collected over decades, our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing, and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities in long-lived species. Significance Statement Exposure to early life adversity, even when conditions subsequently improve, can have profound and persistent consequences for human health. Negative effects of early life adversity appear widespread across the animal kingdom. To date, however, direct evidence from long-lived species is relatively scarce due to the difficulties of collecting data from early life till death. We leverage six decades of observations on thousands of free-ranging male and female rhesus macaques to examine the complex ways early life adversity impacts survival. Our results suggest that the type of adversity and life history factors intersect to impact immediate and downstream survival. By studying early life adversity across environments, cultures, contexts, and species, we can better understand the evolutionary underpinnings of early life sensitivities.

animal behavior and cognition↗

The biology of aging in a social world: insights from free-ranging rhesus macaques

Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individuals life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago Island, which is home to the worlds longest continuously monitored free-ranging population of rhesus macaques. We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.

immunology↗