The immunogenetic impact of European colonization in the Americas

Abstract

The introduction of pathogens originating from Eurasia into the Americas during early European contact has been associated with high mortality rates among Indigenous peoples, likely contributing to their historical and precipitous population decline. However, the biological impacts of imported infectious diseases and resulting epidemics, especially in terms of pathogenic effects on the Indigenous immunity, remain poorly understood and highly contentious to this day. Here, we examine multidisciplinary evidence underpinning colonization-related immune genetic change, providing contextualization from anthropological studies, paleomicrobiological evidence of contrasting host-pathogen coevolutionary histories, and the timings of disease emergence. We further summarize current studies examining genetic signals reflecting post-contact Indigenous population bottlenecks, admixture with European and other populations, and the putative effects of natural selection, with a focus on ancient DNA studies and immunity-related findings. Considering current genetic evidence, together with a population genetics theoretical approach, we show that post-contact Indigenous immune adaptation, possibly influenced by selection exerted by introduced pathogens, is highly complex and likely to be affected by multifactorial causes. Disentangling putative adaptive signals from those of genetic drift thus remains a significant challenge, highlighting the need for the implementation of population genetic approaches that model the short time spans and complex demographic histories under consideration. This review adds to current understandings of post-contact immunity evolution in Indigenous peoples of America, with important implications for bettering our understanding of human adaptation in the face of emerging infectious diseases.

The landscape of ancient human pathogens in Eurasia from the Stone Age to historical times

“…This may have caused significant population declines with depopulated areas repopulated by opportunistic settlers who intermixed with the remaining original population. Such a scenario would mirror the population decline of Indigenous people in the Americas following their exposure to Eurasian diseases introduced by European colonists 57,58 . Our findings also support the interpretation of increased pathogen pressure as a driver of positive selection on immunogenetic variants associated with risk of the autoimmune disease multiple sclerosis in Steppe populations around 5,000 years ago 59 , and genetic adaptations in genes involved in host-pathogen interactions having occurred predominantly after the onset of the Bronze Age in Europe 60 .…”

Indigenous populations of the Pacific and American West

“…There is also an inherent danger in grounding any historical explanation in the supposed immunological differences between Europeans and other peoples. Even if we accept that varying coevolutionary histories with pathogens are likely to have distinguished Europeans from American, Pacific and Australian populations, wide variations in resource production, population density and disease environments across these “new worlds” suggest equal degrees of variation between Indigenous peoples (Collen, Johar, Teixeira, & Llamas, 2022).…”