Resistance to gapeworm parasite has both additive and dominant genetic components in house sparrows, with evolutionary consequences for ability to respond to parasite challenge

Lundregan, Sarah; Niskanen, Alina K.; Muff, Stefanie; Holand, Håkon; Kvalnes, Thomas; Ringsby, Thor‐Harald; Husby, Arild; Jensen, Henrik

doi:10.1111/mec.15491

Molecular Ecology

2020

DOI: 10.1111/mec.15491

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Resistance to gapeworm parasite has both additive and dominant genetic components in house sparrows, with evolutionary consequences for ability to respond to parasite challenge

Sarah Lundregan

Alina K. Niskanen

Stefanie Muff

et al.

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Cited by 5 publications

(16 citation statements)

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“…In natural populations, long‐term studies offer a unique opportunity to dissect the genetic architecture of complex traits such as host resistance and reveal the evolutionary potential of populations. The study of Lundregan et al (2020) is the perfect example. Using long‐term data of an insular house sparrow ( Passer domesticus ) metapopulation, they are able to reveal the genetic basis of host resistance to gapeworm ( Syngamus trachea ) and provide insight into the evolutionary potential of this population.…”

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“…Lundregan et al (2020) first quantify the evolutionary potential of this population to respond to gapeworm infection by analysing if the variation in different infection parameters has a heritable genetic component. Using Bayesian animal models, they explore for each parasite resistance trait the proportion of phenotypic variance that is additive genetic variance, dominance variance or environmental variance.…”

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confidence: 99%

“…The trait with stronger genetic basis is the infection intensity, confirming previous results found in farmed animals, where faecal egg count was also shown to be heritable and a trait that could be subject to selection (Hollema, Bijma, & van der Werf, 2018). But most importantly, Lundregan et al (2020) study is one of the first studies to estimate dominance variance in natural populations, showing that additive genetic variance contribution may be overestimated when any extant dominance variance is not accounted for. Studies estimating nonadditive genetic variance in natural systems are scarce and often have low power.…”

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confidence: 99%

“…In addition, ignoring dominance variance did not strongly inflate estimates of additive genetic variance and heritability. Lundregan et al (2020) show that although the need to consider nonadditive genetic effects may not be applicable to all traits, it may be especially important for fitness‐related traits like disease resistance that are expected to display dominance variance. This is critical, because the evolutionary response to selection depends on the additive genetic variance and not accounting for dominance variance may lead to overestimating the evolutionary potential of populations.…”

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confidence: 99%

“…After estimating the heritability, Lundregan et al (2020) analyse the genetic architecture of resistance to gapeworm infection (i.e. number, effect size and genomic distribution of loci associated with resistance).…”

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Genomic architecture of gapeworm resistance in a natural bird population

Ruiz‐López

2020

Molecular Ecology

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Parasites are recognized to be some of the strongest agents of natural selection, sometimes causing major changes in the phenotypes of their hosts. Understanding the genomic determinants leading to these adaptive processes is key to understand host–parasite interactions. However, dissecting the genetic architecture of host resistance in natural systems is difficult because of the multiple factors affecting these complex traits in the wild. In this issue of Molecular Ecology, Lundregan et al. (2020) use an impressive long‐term data set to analyse the genomic architecture of host resistance to gapeworm in a metapopulation of house sparrows. The authors elegantly combine different approaches (variance component analyses, genome partitioning and genome‐wide associations) to reveal that resistance to gapeworm is under polygenic control and can have both a significant additive genetic and dominance variance. This study is one of the first to simultaneously determine genomic architecture and assess additive genetic and dominance genetic variance in parasite resistance in natural populations.

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Genomic architecture of gapeworm resistance in a natural bird population

Ruiz‐López

2020

Molecular Ecology

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Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow

Lundregan

Mäkinen

Buer

et al. 2022

Ecology and Evolution

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Parasites can exert strong selective pressures on their hosts and influence the evolution of host immunity. While several studies have examined the genetic basis for parasite resistance, the role of epigenetics in the immune response to parasites is less understood. Yet, epigenetic modifications, such as changes in DNA methylation, may allow species to respond rapidly to parasite prevalence or virulence. To test the role of DNA methylation in relation to parasite infection, we examined genome‐wide DNA methylation before and during infection by a parasitic nematode, Syngamus trachea , in a natural population of house sparrows ( Passer domesticus ) using reduced representation bisulfite sequencing (RRBS). We found that DNA methylation levels were slightly lower in infected house sparrows, and we identified candidate genes relating to the initial immune response, activation of innate and adaptive immunity, and mucus membrane functional integrity that were differentially methylated between infected and control birds. Subsequently, we used methylation‐sensitive high‐resolution melting (MS‐HRM) analyses to verify the relationship between methylation proportion and S. trachea infection status at two candidate genes in a larger sample dataset. We found that methylation level at NR1D1 , but not CLDN22 , remained related to infection status and that juvenile recruitment probability was positively related to methylation level at NR1D1 . This underscores the importance of performing follow‐up studies on candidate genes. Our findings demonstrate that plasticity in the immune response to parasites can be epigenetically mediated and highlight the potential for epigenetic studies in natural populations to provide further mechanistic insight into host–parasite interactions.

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Redundancy analysis, genome‐wide association studies and the pigmentation of brown trout (Salmo trutta L.)

Valette

Leitwein

Lascaux³

et al. 2022

Journal of Fish Biology

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The association of molecular variants with phenotypic variation is a main issue in biology, often tackled with genome-wide association studies (GWAS). GWAS are challenging, with increasing, but still limited, use in evolutionary biology. We used redundancy analysis (RDA) as a complimentary ordination approach to single-and multitrait GWAS to explore the molecular basis of pigmentation variation in brown trout (Salmo trutta) belonging to wild populations impacted by hatchery fish. Based on 75,684 single nucleotide polymorphic (SNP) markers, RDA, single-and multitrait GWAS allowed the extraction of 337 independent colour patterning loci (CPLs) associated with trout pigmentation traits, such as the number of red and black spots on flanks. Collectively, these CPLs (i) mapped onto 35 out of 40 brown trout linkage groups indicating a polygenic genomic architecture of pigmentation, (ii) were found to be associated with 218 candidate genes, including 197 genes formerly mentioned in the literature associated to skin pigmentation, skin patterning, differentiation or structure notably in a close relative, the rainbow trout (Onchorhynchus mykiss), and (iii) related to functions relevant to pigmentation variation (e.g., calcium-and ionbinding, cell adhesion). Annotated CPLs include genes with well-known pigmentation effects (e.g., PMEL, SLC45A2, SOX10), but also markers associated with genes formerly found expressed in rainbow or brown trout skins. RDA was also shown to be useful to investigate management issues, especially the dynamics of trout pigmentation submitted to several generations of hatchery introgression.

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Resistance to gapeworm parasite has both additive and dominant genetic components in house sparrows, with evolutionary consequences for ability to respond to parasite challenge

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 5 publications

References 138 publications

Genomic architecture of gapeworm resistance in a natural bird population

Genomic architecture of gapeworm resistance in a natural bird population

Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow

Redundancy analysis, genome‐wide association studies and the pigmentation of brown trout (Salmo trutta L.)

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