Host heterozygosity and genotype rarity affect viral dynamics in an avian subspecies complex

Abstract

Genetic diversity at community, population and individual levels is thought to influence the spread of infectious disease. At the individual level, inbreeding and heterozygosity are associated with increased risk of infection and disease severity. Host genotype rarity may also reduce infection risk if pathogens are co-adapted to common or local hosts, but to date, no studies have investigated the relative importance of genotype rarity and heterozygosity for infection in a wild, sexually reproducing vertebrate. With beak and feather disease virus (BFDV) infection in a wild parrot (Platycercus elegans), we show that both heterozygosity and genotype rarity of individual hosts predicted infection, but in contrasting ways. Heterozygosity was negatively associated with probability of infection, but not with infection load. In contrast, increased host genotype rarity was associated with lower viral load in infected individuals, but did not predict infection probability. These effects were largely consistent across subspecies, but were not evident at the population level. Subspecies and age were also strongly associated with infection. Our study provides novel insights into infection dynamics by quantifying rarity and diversity simultaneously. We elucidate roles that host genetic diversity can play in infection dynamics, with implications for understanding population divergence, intraspecific diversity and conservation.Pathogens by definition have negative health consequences for their host and often reduce host likelihood of survival or reproduction 1 . Therefore, pathogens have long been considered a strong selective force against susceptible host individuals 2-4 . Genetic diversity is hypothesised to influence the susceptibility of hosts to infection directly, and it is generally accepted that lower genetic diversity increases susceptibility 1 . In natural populations, individuals that are more homozygous tend to exhibit higher infection probabilities 5-9 and pathogen loads 7,8,10,11 . A possible mechanism explaining this phenomenon could relate to the reduced capability of individuals with reduced allelic diversity at loci associated with immunity (e.g. major histocompatibility complex or Toll-like receptors) to defend themselves against pathogens 12-14 , or indirectly through negative effects associated with inbreeding (e.g. expression of deleterious recessive alleles) 15,16 . In addition, individual susceptibility may also be related to the co-adaptation of the pathogen with common genotypes, which gives rise to a selective advantage for rare genotypes [17][18][19] . Whilst selection against homozygotes results in greater overall population heterozygosity 2 , rare genotype advantage due to selection against common genotypes, results in negative frequency-dependent selection on genotypes 20,21 . Hence pathogens have considerable potential to contribute to the maintenance of genetic diversity and subsequently hinder or promote host divergence between wild populations 22,23 . Although studies have separately investi...

Low heterozygosity is associated with vector‐borne disease in crows

“…In the current study, we found that low multilocus heterozygosity-which previous work has shown to correlate with inbreeding in crows (Townsend et al 2009a(Townsend et al , 2010b)-was associated with two vector-borne infectious diseases: an emerging epidemic pathogen (WNV) and an endemic, common one (Plasmodium spp). Overall, our results support the widely held hypothesis that inbred individuals may be more susceptible to certain infections than outbred individuals (Altizer et al 2003, Spielman et al 2004, Eastwood et al 2017, and provides empirical data-rare in wild, free-living populations-on how this susceptibility varies among specific pathogens. We found no associations between heterozygosity and infection by Campylobacter jejuni, a common and widespread bacterial pathogen with a fecal-oral transmission route.…”

“…We found no associations between heterozygosity and infection by Campylobacter jejuni, a common and widespread bacterial pathogen with a fecal-oral transmission route. Overall, our results support the widely held hypothesis that inbred individuals may be more susceptible to certain infections than outbred individuals (Altizer et al 2003, Spielman et al 2004, Eastwood et al 2017, and provides empirical data-rare in wild, free-living populations-on how this susceptibility varies among specific pathogens.…”

“…Inbreeding depression-the decline in fitness of inbred progeny relative to outbred progenymay be driven, in part, by increased susceptibility of inbred individuals to infectious disease (Spielman et al 2004, Eastwood et al 2017. In theory, inbreeding could elevate infection risk if individuals with low heterozygosity at loci associated with immune responses are able to recognize fewer pathogens than more heterozygous individuals (heterozygote advantage; Radwan et al 2010, Spurgin andRichardson 2010).…”

Maize responsiveness to <i>Azospirillum brasilense</i>: insights into genetic control and genomic prediction

“…Relations between genomic heterozygosity and plant fitness have been explored in several species, and, when studied at the individual level, these relations serve as a measure of individual genetic diversity (Arct et al, 2017;Eastwood et al, 2017). Our analysis revealed modest negative correlations between heterozygosity and RDM and RV under N stress plus A. brasilense treatment.…”

“…Hence, the competition between A. brasilense and a wide range of other microorganisms that have little or no effect on the plant could have resulted in a lower benefit due to inoculation. In addition, regarding host-pathogen systems, the lower individual genetic diversity can increase the susceptibility to infection (Govindaraj et al, 2015;Eastwood et al, 2017). Similarly, this could happen with A. brasilense, where the allelic diversity among specific loci associated with plant immunity would actively control the extent of colonization by the bacteria and, consequently, the degree of beneficial results.…”