Biosocial Interactions

Jeanne Altmann • Dalton Conley • Noreen Goldman • Tod G. Hamilton • C. Jessica E. Metcalf

Jeanne Altmann’s research deals with life history approaches to behavioral ecology and with non-experimental research design. Most of her empirical work has been carried out on the baboons of Amboseli National Park, Kenya, for which longitudinal studies have been conducted since 1971. Altman and her team of researchers emphasize an integrated, holistic approach by carrying out concurrent studies of behavior, ecology, demography, genetics, and physiology at the level of individuals, social groups, and populations.

Altmann’s current research centers on the magnitude and sources of variability in primate life histories, parental care, and behavioral ontogeny. For baboons, she and her researchers are analyzing sources of variability within groups and examining patterns in their stability among groups and populations and across time. In one series of studies, the researchers are interested in the extent to which various life-history and developmental parameters are food-limited. In others, they are examining empirically and theoretically the effects of social structure within groups on demographic processes within and among groups and across generations. Recently, Altmann and her collaborators have been conducting studies that relate endocrine and genetic data to demographic and behavioral information for the same individuals in the Amboseli baboon population.

Jeanne Altmann co-directs the Amboseli Baboon Research Project (ABRP) with Susan Albets (Duke University). ABRP is one of the longest-running studies of wild primates in the world. Focused on the savannah baboon, Papio cynocephalus, ABRP is located in the Amboseli ecosystem of East Africa, north of Mt. Kilimanjaro. They track hundreds of known individuals in several social groups over the course of their entire lives. They currently monitor around 300 animals, but over the last four decades have accumulated life history information on over 1,500 animals. Research at ABRP has long centered on processes at the individual, group, and population levels, and in recent years has also included other aspects of baboon biology, such as genetics, hormones, nutrition, hybridization, parasitology, and relations with other species.

Jeanne Altmann collaborated with Colchero, F. (University of Southern Denmark; Max Planck Institute for Demographic Research) et al. on “The Emergence of Longevous Populations,” published in Proceedings of the National Academy of Sciences. This paper is significant due to burgeoning public interest in social and economic equality. The authors examine a related phenomenon, lifespan equality, using data from charismatic primate populations and diverse human populations. The study reveals three key findings. First, lifespan equality rises in lockstep with life expectancy, across primate species separated by millions of years of evolution and over hundreds of years of human social progress. Second, industrial humans differ more from nonindustrial humans in these measures than nonindustrial humans do from other primates. Third, in spite of the astonishing progress humans have made in lengthening the lifespan, a male disadvantage in lifespan measures has remained substantial—a result that will resonate with enduring public interest in male–female differences in many facets of life.

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 they 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. Their findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Dalton Conley and Malaspina, D. (New York University) published “Socio-Genomics and Structural Competency,” in Journal of Bioethical Inquiry. Adverse developmental exposures and pathologies of the social environment make vastly greater contributions to the leading health burdens in society than currently known genotypic information. Yet, while patients now commonly bring information on single alleles to the attention of their healthcare team, the former conditions are only rarely considered with respect to future health outcomes. This manuscript aims to integrate social environmental influences in genetic predictive models of disease risk. Healthcare providers must be educated to better understand genetic risks for complex diseases and the specific health consequences of societal adversities, to facilitate patient education, disease prevention, and the optimal care in order to achieve positive health outcomes for those with early trauma or other social disadvantage.

Dalton Conley published “Socio-Genomic Research Using Genome-Wide Molecular Data,” in Annual Review of Sociology. Recent advances in molecular genetics have provided social scientists with new tools with which to explore human behavior. By deploying genomic analysis, we can now explore long-term patterns of human migration and mating, explore the biological aspects of important sociological outcomes such as educational attainment, and, most importantly, model gene-by-environment interaction effects. The intuition motivating much sociogenomic research is that to have a more complete understanding of social life, scholars must take into consideration both nature and nurture as well as their interplay. Most promising is gene-by-environment research that deploys polygenic measures of genotype as a prism through which to refract and detect heterogenous treatment effects of plausibly exogenous environmental influences. This article reviews much recent work in this vein and argues for a broader integration of genomic data into social inquiry.

“Cohort Effects in the Genetic Influence on Smoking,” written by Dalton Conley, Domingue, B. (Stanford University), Fletcher, J. (University of Wisconsin, Madison), and Boardman, J. (University of Colorado) was published in Behavior Genetics. The authors examine the hypothesis that the heritability of smoking has varied over the course of recent history as a function of associated changes in the composition of the smoking and non-smoking populations. Classical twin-based heritability analysis has suggested that genetic basis of smoking has increased as the information about the harms of tobacco has become more prevalent—particularly after the issuance of the 1964 Surgeon General’s Report. In the present paper, they deploy alternative methods to test this claim. They use data from the Health and Retirement Study to estimate cohort differences in the genetic influence on smoking using both genomic-relatedness-matrix restricted maximum likelihood and a modified DeFries–Fulker approach. They perform a similar exercise deploying a polygenic score for smoking using results generated by the Tobacco and Genetics consortium. The results support earlier claims that the genetic influence in smoking behavior has increased over time. Emphasizing historical periods and birth cohorts as environmental factors has benefits over existing GxE research. Their results provide additional support for the idea that anti-smoking policies of the 1980s may not be as effective because of the increasingly important role of genotype as a determinant of smoking status.

Noreen Goldman and Cornman, J. et al. published “Cohort Profile: The Social Environment and Biomarkers of Aging Study (SEBAS) in Taiwan,” in International Journal of Epidemiology. The Social Environment and Biomarkers of Aging Study (SEBAS) is a nationally representative longitudinal survey of Taiwanese middle-aged and older adults. It adds the collection of biomarkers and performance assessments to the Taiwan Longitudinal Study of Aging (TLSA), a nationally representative study of adults aged 60 and over, including the institutionalized population. The TLSA began in 1989, with follow-ups approximately every 3 years; younger refresher cohorts were added in 1996 and 2003. The first wave of SEBAS, based on a sub-sample of respondents from the 1999 TLSA, was conducted in 2000. A total of 1023 respondents completed both a face-to-face home interview and, several weeks later, a hospital-based physical examination. In addition to a 12-h (7?pm–7?am) urine specimen collected the night before and a fasting blood specimen collected during the examination, trained staff measured blood pressure, height, weight and waist and hip circumferences. A second wave of SEBAS was conducted in 2006 using a similar protocol to SEBAS 2000, but with the addition of performance assessments conducted by the interviewers at the end of the home interview. Both waves of SEBAS also included measures of health status (physical, emotional, cognitive), health behaviors, social relationships and exposure to stressors. The SEBAS data, which are publicly available at [], allow researchers to explore the relationships among life challenges, the social environment and health and to examine the antecedents, correlates and consequences of change in biological measures and health.

C. Jessica Metcalf, Meaden, S. (University of Exeter, UK), and Koskella, B. published “The Effects of Host Age and Spatial Location on Bacterial Community Composition in the English Oak Tree (Quercus Robur),” in Environmental Microbiology Reports. Drivers of bacterial community assemblages associated with plants are diverse and include biotic factors, such as competitors and host traits, and abiotic factors, including environmental conditions and dispersal mechanisms. They examine the roles of spatial distribution and host size, as an approximation for age, in shaping the microbiome associated with Quercus robur woody tissue using culture-independent 16S rRNA gene amplicon sequencing. In addition to providing a baseline survey of the Q. robur microbiome, they screened for the pathogen of acute oak decline. Our results suggest that age is a predictor of bacterial community composition, demonstrating a surprising negative correlation between tree age and alpha diversity. They find no signature of dispersal limitation within the Wytham Woods plot sampled. Together, these results provide evidence for niche-based hypotheses of community assembly and the importance of tree age in bacterial community structure, as well as highlighting that caution must be applied when diagnosing dysbiosis in a long-lived plant host.

C. Jessica Metcalf, and Fournier-Level, A. (The University of Melbourne, Parkville) et al. contributed to “Predicting the Evolutionary Dynamics of Seasonal Adaptation to Novel Climates in Arabidopsis thaliana,” published in Proceedings of the National Academy of Sciences. Predicting whether and how populations will adapt to rapid climate change is a critical goal for evolutionary biology. To examine the genetic basis of fitness and predict adaptive evolution in novel climates with seasonal variation, the authors grew a diverse panel of the annual plant Arabidopsis thaliana (multi parent advanced generation intercross lines) in controlled conditions simulating four climates: a present-day reference climate, an increased-temperature climate, a winter-warming only climate, and a poleward-migration climate with increased photoperiod amplitude. In each climate, four successive seasonal cohorts experienced dynamic daily temperature and photoperiod variation over a year. They measured 12 traits and developed a genomic prediction model for fitness evolution in each seasonal environment. This model was used to simulate evolutionary trajectories of the base population over 50 y in each climate, as well as 100-y scenarios of gradual climate change following adaptation to a reference climate. Patterns of plastic and evolutionary fitness response varied across seasons and climates. The increased-temperature climate promoted genetic divergence of subpopulations across seasons, whereas in the winter-warming and poleward-migration climates, seasonal genetic differentiation was reduced. In silico "resurrection experiments" showed limited evolutionary rescue compared with the plastic response of fitness to seasonal climate change. The genetic basis of adaptation and, consequently, the dynamics of evolutionary change differed qualitatively among scenarios. Populations with fewer founding genotypes and populations with genetic diversity reduced by prior selection adapted less well to novel conditions, demonstrating that adaptation to rapid climate change requires the maintenance of sufficient standing variation.

Tod Hamilton and Rosenblum, A. (Duke University), Darity Jr., W. (Duke University), and Harris, A. (Duke University) published “Looking Through the Shades: The Effect of Skin Color on Earnings by Region of Birth and Race for Immigrants to the United States,” in Sociology of Race & Ethnicity. The purpose of their study was to determine whether a labor market penalty exists for members of immigrant groups as a result of being phenotypically different from white Americans. Specifically, the authors examine the link between skin shade, perhaps the most noticeable phenotypical characteristic, and wages for immigrants from five regions: (1) Europe and Central Asia; (2) China, East Asia, South Asia, and the Pacific; (3) Latin America and the Caribbean; (4) Sub-Saharan Africa; and (5) the Middle East and North Africa. Using data from the New Immigrant Survey, a nationally representative multi-cohort longitudinal study of new legal immigrants to the United States, the authors found a skin shade penalty in wages for darker immigrants. However, disaggregating by region of origin shows that this finding is driven exclusively by the experience of immigrants from Latin America; the wage penalty for skin tone is substantial for self-reported nonblack Latin American immigrants. The effects of colorism are much less pronounced or nonexistent among other national-origin populations. Furthermore, although a skin shade penalty is not discernible among African immigrants, findings show that African immigrants experience a racial wage penalty.