Click here for an overview of research in the Archie lab. Keep reading for updates on our latest research.
Social effects on microbiomes and macroparasites
Social context shapes microbiomes and parasite communities
Social behavior is proposed to have profound effects on microbial transmission. While these effects are well known for pathogenic microbes, social effects on beneficial bacterial communities, such as the vertebrate gut microbiome, have been relatively ignored. In 2015, we tested for social effects on gut microbiome composition via metagenomic shotgun sequencing of fecal-derived DNA from nearly all the adult baboons living in two social groups in the Amboseli ecosystem, Kenya. We found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments.
More recently, we have tested how an individual’s social context affects patterns of macroparasite infection in the Amboseli baboons. We tested how multi-scale factors affect parasite infection in females (Akinyi et al. 2019, J Anim Ecol) and males (Habig et al. 2019, Behav Ecol Sociobiol). We found that social connectedness to females is linked to higher disease risk in males. In contrast, females, social isolation was linked to higher parasitism. These results highlight the different ways social context may shape disease risk.
Other ecological and evolutionary forces shaping microbiomes Recently, our group has been testing the role of the role of vertical versus horizontal (i.e. environmental) transmission in shaping microbiome composition. Classic evolutionary theory predicts that if beneficial microbes improve host fitness, they should be vertically transmitted to offspring. In 2019, postdoc Johannes Bjork tested for for vertical transmission in marine sponges—a system where microbes provide known benefits and there is a strong expectation of vertical transmission (Björk et al. 2019, Nature Ecology and Evolution). Surprisingly, we found that vertical transmission was weak and unfaithful in multiple sponge species; instead sponges acquire beneficial symbionts from their environments. Also in 2019, PhD student Laura Grieneisen tested environmental contributions to baboon microbiomes, comparing gut microbiome composition from 14 baboon populations across southern Kenya (Grieneisen et al. 2019, Proc R Soc). We found that the effects of host environments, especially the soil properties of a given site, were 15 times stronger than host population genetic effects. These findings challenge classic evolutionary and ecological predictions about microbiome community assembly.
Reproductive microbiomes. Our lab also has a strong interest in female reproductive microbiomes, which make key contributions to female health and fitness. In humans, the vaginal microbiome is dominated by bacteria from the genus Lactobacillus that create an acidic environment proposed to protect women against sexually transmitted infections. Surprisingly, this community is unique to humans: lactobacilli comprise 70% of vaginal bacteria in humans, but only 1% in other mammals. In 2016, PhD students Liz Miller tested several leading hypotheses to explain humans’ unique vaginal microbiota using comparative data across mammals (Miller et al. 2016, Front. Microbiol). We found no support for any of the dominant hypotheses, leading us to generate new hypotheses. In 2017, we also tested how baboon vaginal microbiomes change in response to reproductive state, ovarian cycle phase, and sexual behavior. We found an especially unique microbial community during ovulation, which may provide olfactory cues that signal ovulation to males and have implications for disease risk and conception success (Miller et al., 2017, Microbiome).
Social context affects health and fitness.
Social environments, both in early life and adulthood, are among the strongest predictors of health and survival. Work in our lab has highlighted similar effects in baboons, showing that social status affects wound healing in male baboons (Archie et al. 2012, PNAS), and that social affiliation predicts longevity in female baboons, (Archie et al. 2014, Proc R Soc). More recently, our research has expanded to include interactions between social relationships and early life adversity (Tung & Archie et al. 2016, Nat Comm). Two recent studies along these lines are:
Do social relationships mediate the link between early adversity and adult stress responses? In humans and other animals, it is well known that individuals who experience especially harsh conditions in early life (e.g. famine, neglect, war, parental loss) are at higher risk for several diseases and are more vulnerable to chronic stress in adulthood. What we haven’t known is whether social support in adulthood, or a lack thereof, contributes to those effects. For instance, if early life adversity makes it more challenging to form strong, supportive friendships in adulthood, does this social adversity explain the link between early adversity and adult stress? This makes sense, in part because adult social adversity is happening at the same time as the adult stresses, while the early life experiences may have happened many years ago. A postdoc, Stacy Rosenbaum, and I are tackling this question using detailed data from hundreds of baboons on early life conditions, adult social bonds, and adult stress responses. So far, we find that baboons who experience the most early life adversity have higher stress hormone levels as adults. However, these effects are almost entirely explained by harsh early life conditions themselves, not a lack of social support in adulthood. This shows the long-term effects of early life adversity are more powerful than near-term effects of social bonds, even though early adversity may have occurred many years in the past. It also means that to mitigate early life effects, it might be most effective to focus on early life circumstances, and effects of social bonds on adult stress, which are real, are largely independent of early life experiences (at least in baboons).
Another recent goal has been to test the long-standing hypothesis that accelerated reproduction is an adaptive response to early life adversity: if an individual can anticipate an early death, should they also “live fast”? This idea is common in evolutionary medicine, but no studies have tested if accelerating reproduction in response to early life adversity actually increases fitness. Working with PhD student Chelsea Weibel, we are using 48 years of data on early life experiences, reproductive timing, and lifetime reproductive success. Watch this space for more results soon!