Balancing Selection Drives the Maintenance of Genetic Variation in Drosophila Antimicrobial Peptides

Chapman, J. R.; Hill, Tom; Unckless, Robert L.

doi:10.1093/gbe/evz191

Cited by 38 publications

(58 citation statements)

References 108 publications

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“…Knocking down the other three Bom genes had no significant effect on survival (Table 2). Using Tajima's D values for the DGRP calculated in Chapman et al [40], we found that We have previously calculated Tajima's D for all genes in the DGRP [40]. We ranked all DGRP genes from most negative to most positive and calculated the percentile ranking for each GOI and neighbor gene (Table S2).…”

Section: Role Of Bomanin Genes On E Faecalis Survivalmentioning

confidence: 99%

The Genetic Basis of Natural Variation in Drosophila melanogaster Immune Defense against Enterococcus faecalis

Chapman

Dowell

Chan

et al. 2020

Genes

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Dissecting the genetic basis of natural variation in disease response in hosts provides insights into the coevolutionary dynamics of host-pathogen interactions. Here, a genome-wide association study of Drosophila melanogaster survival after infection with the Gram-positive entomopathogenic bacterium Enterococcus faecalis is reported. There was considerable variation in defense against E. faecalis infection among inbred lines of the Drosophila Genetics Reference Panel. We identified single nucleotide polymorphisms associated with six genes with a significant (p < 10−08, corresponding to a false discovery rate of 2.4%) association with survival, none of which were canonical immune genes. To validate the role of these genes in immune defense, their expression was knocked-down using RNAi and survival of infected hosts was followed, which confirmed a role for the genes krishah and S6k in immune defense. We further identified a putative role for the Bomanin gene BomBc1 (also known as IM23), in E. faecalis infection response. This study adds to the growing set of association studies for infection in Drosophila melanogaster and suggests that the genetic causes of variation in immune defense differ for different pathogens.

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Section: Role Of Bomanin Genes On E Faecalis Survivalmentioning

confidence: 99%

The Genetic Basis of Natural Variation in Drosophila melanogaster Immune Defense against Enterococcus faecalis

Chapman

Dowell

Chan

et al. 2020

Genes

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“…Temporin alleles in R. arvalis (Raar_Temp* 23,24,11,25,27,22,19,18,16,17,30) were grouped in two distinct clades, supporting a recent genetic duplication of Raar_ Temp*23,24,11,25 in R. arvalis after the two species diverged. Rest of the alleles (Raar_Temp *27,22,19,18,16,17, 30) awere more similar to Brevinin than Temporin alleles.…”

Section: Copy Number and Trans-species Polymorphism Variationmentioning

confidence: 90%

“…They have been implicated as a defense against the lethal fungus Batrachochytrium dendrobatidis (Bd) causing global amphibian population declines (e.g., [19][20][21]). It has been firmly established that AMPs may be encoded by duplicated genes [17,22]. A high number of amphibian AMPs has been characterized with the aim to develop peptide-based therapeutic agents [23,24].…”

Section: Introductionmentioning

confidence: 99%

“…However, most of the AMP studies have focused on the antimicrobial peptide variation between amphibian species, and the genetic variation at the population level has received less consideration. Indeed, while there is evidence of geographic variation in effectiveness of antimicrobial defenses in various organism groups [22,[25][26][27][28][29], populationlevel variation in peptide profiles [27,29] and positive selection acting on the Mature Peptide domain [6,7,16], little attention has been directed towards understanding the evolutionary forces acting on the genes coding for AMPs [17,22,30,31]. This is especially the case for the role of selection acting upon sequence variation in AMP genes, and how this variation is distributed within populations as well as at larger geographical scales.…”

Section: Introductionmentioning

confidence: 99%

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Antimicrobial peptide and sequence variation along a latitudinal gradient in two anurans

et al. 2020

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Background: While there is evidence of both purifying and balancing selection in immune defense genes, largescale genetic diversity in antimicrobial peptides (AMPs), an important part of the innate immune system released from dermal glands in the skin, has remained uninvestigated. Here we describe genetic diversity at three AMP loci (Temporin, Brevinin and Palustrin) in two ranid frogs (Rana arvalis and R. temporaria) along a 2000 km latitudinal gradient. We amplified and sequenced part of the Acidic Propiece domain and the hypervariable Mature Peptide domain (~150-200 bp) in the three genes using Illumina Miseq and expected to find decreased AMP genetic variation towards the northern distribution limit of the species similarly to studies on MHC genetic patterns. Results: We found multiple loci for each AMP and relatively high gene diversity, but no clear pattern of geographic genetic structure along the latitudinal gradient. We found evidence of trans-specific polymorphism in the two species, indicating a common evolutionary origin of the alleles. Temporin and Brevinin did not form monophyletic clades suggesting that they belong to the same gene family. By implementing codon evolution models we found evidence of strong positive selection acting on the Mature Peptide. We also found evidence of diversifying selection as indicated by divergent allele frequencies among populations and high Theta k values. Conclusion: Our results suggest that AMPs are an important source of adaptive diversity, minimizing the chance of microorganisms developing resistance to individual peptides.

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“…Following Haldane's initial hypotheses, balancing selection as a result of coevolution in the form of NFDS and/or overdominance was suggested as a mechanism behind the extraordinary genetic diversity found at mammalian Major Histocompatibility Complex (MHC) loci (Bodmer, 1972). These same arguments have 15 been used recently to explain the diversity of anti-microbial peptides in Drosophila (Unckless et al, 2016;Chapman et al, 2019). MHC loci, and other immune defence genes, are notable not only for their high levels of heterozygosity (> 200 alleles across three loci Klein and Figueroa, 1986;Zimmer and Emlen, 2013) but also for the long-term trans-specific persistence of these polymorphisms (Lawlor et al, 1988;Klein, 1987).…”

Section: Introductionmentioning

confidence: 95%

Coevolution does not slow the rate of loss of heterozygosity in a stochastic host-parasite model with constant population size

MacPherson¹,

Keeling

Otto³

2020

Preprint

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Coevolutionary negative frequency dependent selection has been hypothesized to maintain genetic variation in host and parasites. Despite the extensive literature pertaining to host-parasite coevolution, the effect of matching-alleles (MAM) coevolution on the maintenance of genetic variation has not been explicitly modelled in a finite population. The dynamics of the MAM in an infinite population, in fact, suggests that genetic variation in these coevolving populations behaves neutrally. We find that while this is largely true in finite populations two additional phenomena arise. The first of these effects is that of coevolutionary natural selection on stochastic perturbations in host and pathogen allele frequencies. While this may increase or decrease genetic variation, depending on the parameter conditions, the net effect is small relative to that of the second phenomena. Following fixation in the pathogen, the MAM becomes one of directional selection, which in turn rapidly erodes genetic variation in the host. Hence, rather than maintain it, we find that, on average, matching-alleles coevolution depletes genetic variation.

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Balancing Selection Drives the Maintenance of Genetic Variation in Drosophila Antimicrobial Peptides

Cited by 38 publications

References 108 publications

The Genetic Basis of Natural Variation in Drosophila melanogaster Immune Defense against Enterococcus faecalis

The Genetic Basis of Natural Variation in Drosophila melanogaster Immune Defense against Enterococcus faecalis

Antimicrobial peptide and sequence variation along a latitudinal gradient in two anurans

Coevolution does not slow the rate of loss of heterozygosity in a stochastic host-parasite model with constant population size

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