Genotype-environment associations reveal genes potentially linked to
avian malaria infection in populations of an endemic island bird
Abstract
Patterns of pathogen prevalence are, at least partially, the result of
coevolutionary host-pathogen interactions. Thus, exploring the
distribution of host genetic variation in relation to infection by a
pathogen within and across populations can provide important insights
into mechanisms of host defence and adaptation. Here we use a landscape
genomics approach (Bayenv) in conjunction with genome-wide data
(ddRADseq) to test for associations between avian malaria (Plasmodium)
prevalence and host genetic variation across 13 populations of the
island endemic Berthelot’s pipit (Anthus berthelotii). Considerable and
consistent spatial heterogeneity in malaria prevalence was observed
among populations over a period of 15 years. The prevalence of malaria
infection was also strongly positively correlated with pox (Avipoxvirus)
prevalence. Multiple host loci showed significant associations with
malaria prevalence after controlling for genome-wide neutral genetic
structure. These sites were located near to or within genes linked to
metabolism, stress response, transcriptional regulation, complement
activity and the inflammatory response, many previously implicated in
vertebrate responses to malarial infection. Our findings identify
diverse genes - not just limited to the immune system - that may be
involved in host protection against malaria and suggests that spatially
variable pathogen pressure may be an important evolutionary driver of
genetic divergence among wild animal populations, such as Berthelot’s
pipit. Further, our data indicate that spatio-temporal variation in
multiple different pathogens (e.g., malaria and pox in this case) may
have to be studied together to develop a more holistic understanding of
host pathogen-mediated evolution.