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

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. Tolllike 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.

Toll‐like receptor variation in the bottlenecked population of the Seychelles warbler: computer simulations see the ‘ghost of selection past’ and quantify the ‘drift debt’

“…A previous study showed that five of seven TLR loci remained polymorphic in the Seychelles warbler population (Gilroy et al ., ,b). According to our simulations, we can reject neutral evolution for the three most polymorphic loci ( TLR1LB, TLR3 and TLR15; P < 0.001 for all), but not for the two less diverse loci ( TLR1LA and TLR5; P = 0.991, 0.964, respectively; Tables and ).…”

“…The following TLR loci were amplified: TLR1LA, TLR1LB, TLR3, TLR4, TLR5, TLR15 and TLR21, in 22‐30 individuals, as detailed in Gilroy et al . (,b).…”

“…We assume there is no recombination and that variation is solely introduced by mutation. This was based on previous tests using genetic algorithm recombination detection (GARD) analyses (Pond et al ., ) on sequences for all TLR loci in the Seychelles warbler, which failed to detect any evidence of recombination using site‐by‐site analysis (Gilroy et al ., ,b).…”

“…Individuals were diploid, and the fitness ( w ) of an individual with a homozygous locus was given by w = 1 − S , with S being the selection coefficient. Based on preliminary findings (Gilroy et al ., ,b), we explored the parameter space across selection coefficients 0.0 ≤ S ≤ 0.1. The fitness of heterozygote individuals was equal to unity.…”

“…The Seychelles warbler, Acrocephalus sechellensis , is an island endemic passerine species that went through a population bottleneck of less than 30 individuals on a single island during the last century (Collar & Stuart, ). In a previous study, we characterized variation at TLR genes in this population (Gilroy et al ., ,b). We found that despite the considerable losses of genomewide variation due to the bottleneck (Spurgin et al ., ), considerable polymorphism remained at five different TLR loci ( TLR1LA, TLR1LB, TLR3, TLR5 and TLR15 ), while two loci were monomorphic ( TLR4 and TLR21 ).…”