The immunogenetic impact of European colonization in the Americas

Evelyn Jane Collen; Angad Singh Johar; João C Teixeira; Bastien Llamas

doi:10.3389/fgene.2022.918227

The immunogenetic impact of European colonization in the Americas

Front Genet. 2022 Aug 5:13:918227. doi: 10.3389/fgene.2022.918227. eCollection 2022.

Authors

Evelyn Jane Collen¹, Angad Singh Johar^{1

2}, João C Teixeira^{1

3

4}, Bastien Llamas^{1

4

5

6}

Affiliations

¹ Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, SA, Australia.
² School of Mathematics and Statistics, The University of Melbourne, Parkville, VIC, Australia.
³ School of Culture History and Language, The Australian National University, Canberra, ACT, Australia.
⁴ Centre of Excellence for Australian Biodiversity and Heritage (CABAH), School of Biological Sciences, University of Adelaide, Adelaide, SA, Australia.
⁵ National Centre for Indigenous Genomics, Australian National University, Canberra, ACT, Australia.
⁶ Telethon Kids Institute, Indigenous Genomics Research Group, Adelaide, SA, Australia.

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.

Keywords: Indigenous peoples of America; Native Americans; Virgin Soil; colonization; host-pathogen coevolution; immunity; immunogenetic adaptation; infectious disease.

Publication types

Review