Abstract

Host-parasite relationships are likely to change over the coming decades in response to climate change and increased anthropogenic stressors. Understanding the genetic architecture of parasite resistance will aid prediction of species' responses to intensified parasite challenge. The gapeworm "Syngamus trachea" is prevalent in natural bird populations and causes symptomatic infections ranging from mild to severe. The parasite may affect ecological processes by curtailing bird populations and is important due to its propensity to spread to commercially farmed birds. Our large-scale data set on an insular house sparrow metapopulation in northern Norway includes information on gapeworm prevalence and infection intensity, allowing assessment of the genetics of parasite resistance in a natural system. To determine whether parasite resistance has a heritable genetic component, we performed variance component analyses using animal models. Resistance to gapeworm had substantial additive genetic and dominance variance, and genome-wide association studies to identify single nucleotide polymorphisms associated with gapeworm resistance yielded multiple loci linked to immune function. Together with genome partitioning results, this indicates that resistance to gapeworm is under polygenic control in the house sparrow, and probably in other bird species. Hence, our results provide the foundation needed to study any eco-evolutionary processes related to gapeworm infection, and show that it is necessary to use methods suitable for polygenic and nonadditive genetic effects on the phenotype.

Highlights

  • Parasite prevalence and virulence are major drivers of ecological and evolutionary processes in natural populations, and are expected to shift over the coming decades in response to climate change (Altizer, Ostfeld, Johnson, Kutz, & Harvell, 2013; Harvell, Altizer, Cattadori, Harrington, & Weil, 2009)

  • We provide evidence that S. trachea infection status and infection intensity (FEC and faecal egg count (FEC) in the infected subset of individuals) have substantial additive genetic variance leading to moderate heritability estimates (Table 3; h2liab = 0.124, 0.239 and 0.351 respectively) that are in line with those from previous studies

  • A genetic basis for parasite infection intensity has previously been established in commercially farmed animals, with heritability estimates for faecal egg count in the region of 0.30 for cattle and pig (Gasbarre, Leighton, & Davies, 1990; Leighton, Murrell, & Gasbarre, 1989; Nejsum et al, 2009), 0.15–0.40 for sheep (Gauly, Kraus, Vervelde, Van Leeuwen, & Erhardt, 2002; Stear et al, 2007; Woolastont & Windon, 2001) and 0.35–0.41 for chicken (Psifidi et al, 2016)

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Summary

| INTRODUCTION

Parasite prevalence and virulence are major drivers of ecological and evolutionary processes in natural populations, and are expected to shift over the coming decades in response to climate change (Altizer, Ostfeld, Johnson, Kutz, & Harvell, 2013; Harvell, Altizer, Cattadori, Harrington, & Weil, 2009). Limitations apply to the GWAS approach when it is used to map pathogen resistance genes: success is more likely where resistance is due to common, large-effect variants, and resistance genes identified in a given population may depend on the genetic makeup of the pathogen community (MacPherson, Otto, & Nuismer, 2018) Despite these drawbacks, numerous genes relating to parasite resistance have been identified in livestock, including sheep (Benavides, Sonstegard, & Van Tassell, 2016; Berton et al, 2017; Periasamy et al, 2014; Pickering, Auvray, Dodds, & McEwan, 2015), cattle (May et al, 2019), goat (Silva et al, 2018; Zvinorova et al, 2016) and chicken (Boulton et al, 2018). Additive and dominance effect sizes of markers on our custom house sparrow genome-wide 200k single nucleotide polymorphism (SNP) array (Lundregan et al, 2018) were estimated using GWAS, to identify genomic regions related to parasite resistance in the house sparrow and provide mechanistic insight into its evolutionary potential

| METHODS
Findings
| DISCUSSION
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