Genetic drift outweighs natural selection at toll‐like receptor (TLR) immunity loci in a re‐introduced population of a threatened species

Abstract

During population establishment, genetic drift can be the key driver of changes in genetic diversity, particularly while the population is small. However, natural selection can also play a role in shaping diversity at functionally important loci. We used a well-studied, re-introduced population of the threatened Stewart Island robin (N = 722 pedigreed individuals) to determine whether selection shaped genetic diversity at innate immunity toll-like receptor (TLR) genes, over a 9-year period of population growth following establishment with 12 genetic founders. We found no evidence for selection operating with respect to TLR diversity on first-year overwinter survival for the majority of loci, genotypes and alleles studied. However, survival of individuals with TLR4BE genotype was significantly improved: these birds were less than half as likely to die prior to maturity compared with all other TLR4 genotypes. Furthermore, the population frequency of this genotype, at a two-fold excess over Hardy-Weinberg expectation, was increased by nonrandom mating. Near-complete sampling and full pedigree and reproductive data enabled us to eliminate other potential causes of these patterns including inbreeding, year effects, density dependence, selection on animals at earlier life history stages or genome-level association of the TLR4E allele with 'good genes'. However, comparison of observed levels of gene diversity to predictions under simulated genetic drift revealed results consistent with neutral expectations for all loci, including TLR4. Although selection favoured TLR4BE heterozygotes in this population, these effects were insufficient to outweigh genetic drift. This is the first empirical study to show that genetic drift can overwhelm natural selection in a wild population immediately following establishment.

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

“…Across birds, extensive evidence for episodic positive selection on TLR-4 leucine-rich repeat regions has been observed (Grueber et al, 2014). On a scale more comparable to our study, a genetic bottleneck at the time of introduction influenced variation in the TLR-4 exon sequence in a passerine introduced to New Zealand (Grueber et al, 2013). The only study so far to consider selection on drivers of gene expression in wild animals involved the mannan-binding lectin promoter in roe deer (Capreolus capreolus) (Quéméré et al, 2015).…”

Avian β-defensin variation in bottlenecked populations: the Seychelles warbler and other congeners

“…Drift is the predominant evolutionary force shaping genetic variation in small populations Miller and Lambert 2004;Jensen et al 2013), and its effects on genetic variation often outweigh the influence of selection (Miller and Lambert 2004;Alcaide 2010;Grueber et al 2013). Nevertheless, various studies have shown that within small natural populations, variation at specific key loci can be elevated above that of the genome-wide average, and be maintained across bottleneck events as a result of balancing selection (Aguilar et al 2004;Tompkins 2007;van Oosterhout et al 2006).…”

Gene dynamics of toll-like receptor 4 through a population bottleneck in an insular population of water voles (Arvicola amphibius)

“…This may have potential consequences for survival, fitness, fecundity and reproductive success of water voles and consequently population viability and persistence. As such, it is an ecologically meaningful locus and understanding its dynamics in populations is useful in a conservation context (Hedrick 2001;Seddon 2010;Thomas 2011;Oliver and Piertney 2012;Grueber et al 2013). This reinforces the point made by Acevedo-Whitehouse and Cunningham (2006) that the MHC is not the only region of the immunogenome that is important and should be characterised in an ecological context.…”

“…TLRs are an essential family of type 1 transmembrane glycoproteins that act as pattern recognition receptors (PRRs) and play an important role in the innate immune response (Akira et al 2001;Brownlie and Allan 2011;Grueber et al 2013;Fornusková et al 2013). They are involved in the initial recognition of invading infectious agents (Tschirren et al 2013) and act as a host's front-line defence against a wide range of pathogens (Uematsu and Akira 2008;Iwasaki and Medzhitov 2010;Alcaide and Edwards 2011).…”