Toll-like receptor variation in the bottlenecked population of the endangered Seychelles warbler

D L Gilroy,D S Richardson,C Van Oosterhout,J Komdeur

doi:10.1111/acv.12307

D L Gilroy, D S Richardson + Show 2 more

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https://doi.org/10.1111/acv.12307

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Abstract

In small populations, drift results in a loss of genetic variation, which reduces adaptive evolutionary potential. Furthermore, the probability of consanguineous mating increases which may result in inbreeding depression. Under certain circumstances, balancing selection can counteract drift and maintain variation at key loci. Identifying such loci is important from a conservation perspective and may provide insight into how different evolutionary forces interact in small populations. Toll-like receptor (TLR) genes play a pivotal role in vertebrate innate immune defence by recognizing invading pathogens. We characterize TLR variation in the Seychelles warbler (SW) Acrocephalus sechellensis, an endangered passerine that recently suffered a population bottleneck. Five of seven TLR loci were polymorphic, with one locus (TLR15) containing four functional variants and showing an excess of heterozygotes. Haplotype-level tests failed to detect selection at these loci, but site-specific tests detected signatures of positive selection within TLR3 and TLR15. After characterizing variation (excluding TLR15) in 5–6 other Acrocephalus species, we found that TLR variation was positively correlated with population size across species and followed the pattern observed at neutral microsatellite loci. The depauperate TLR variation observed suggests that even at important immunity-related loci, balancing selection may only attenuate the overriding effects of drift. However, in the SW, TLR15 appears to be an outlier and warrants further investigation. The low levels of TLR variation may be disadvantageous for the long-term viability of the SW and conservation measures that maximize the retention of the variation should be considered.

Highlights

Analysis of genetic variation within and among populations can provide important insight into the evolutionary and demographic history of a species (Garrigan & Hedrick, 2003; Piertney & Webster, 2010; Sutton et al, 2011)
In the Seychelles warbler (SW), three loci deviated from Hardy–Weinberg proportions: TLR1LB and TLR3 had a deficiency of heterozygotes (TLR1LB: FIS = 0.372, P = 0.002; TLR3: FIS = 0.186, P = 0.031) and TLR15 had a heterozygote excess (FIS = À0.061, P = 0.017) (Supporting Information Fig. S1)
Across the Tolllike receptor (TLR) loci levels of variation were, on average, as low as levels of variation observed at neutral loci (Hansson & Richardson, 2005)

Summary

Introduction

Analysis of genetic variation within and among populations can provide important insight into the evolutionary and demographic history of a species (Garrigan & Hedrick, 2003; Piertney & Webster, 2010; Sutton et al, 2011). Studies that determine the level of functional variation at key loci in populations can elucidate where within and among individual polymorphism is important (such as those involved in the immune response). It can identify where lack of polymorphism may underlie potential vulnerability to future stresses, such as hindering adaptation to novel pathogen infections (Frankel, 1974; Hedrick, 2001). The results from these studies can feed into policy-making decisions when assessing the long-term viability of fragmented and bottlenecked populations. Where evidence of unusually low levels of variation at immune genes is found, genetic augmentation from other populations may be considered (e.g. Franklin et al, 2009)

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