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’

Abstract

Balancing selection can maintain immunogenetic variation within host populations, but detecting its signal in a postbottlenecked population is challenging due to the potentially overriding effects of drift. Toll-like receptor genes (TLRs) play a fundamental role in vertebrate immune defence and are predicted to be under balancing selection. We previously characterized variation at TLR loci in the Seychelles warbler (Acrocephalus sechellensis), an endemic passerine that has undergone a historical bottleneck. Five of seven TLR loci were polymorphic, which is in sharp contrast to the low genomewide variation observed. However, standard population genetic statistical methods failed to detect a contemporary signature of selection at any TLR locus. We examined whether the observed TLR polymorphism could be explained by neutral evolution, simulating the population's demography in the software DIYABC. This showed that the posterior distributions of mutation rates had to be unrealistically high to explain the observed genetic variation. We then conducted simulations with an agent-based model using typical values for the mutation rate, which indicated that weak balancing selection has acted on the three TLR genes. The model was able to detect evidence of past selection elevating TLR polymorphism in the prebottleneck populations, but was unable to discern any effects of balancing selection in the contemporary population. Our results show drift is the overriding evolutionary force that has shaped TLR variation in the contemporary Seychelles warbler population, and the observed TLR polymorphisms might be merely the 'ghost of selection past'. Forecast models predict immunogenetic variation in this species will continue to be eroded in the absence of contemporary balancing selection. Such 'drift debt' occurs when a gene pool has not yet reached its new equilibrium level of polymorphism, and this loss could be an important threat to many recently bottlenecked populations.

Too much of a good thing? Finding the most informative genetic data set to answer conservation questions

“…Evidence from a comprehensive meta‐analysis showed that for populations undergoing intensive genetic drift or bottlenecking events, selection was not powerful enough to maintain MHC diversity (Sutton et al, ). It appears that for small populations, genome‐wide effects of neutral processes, such as inbreeding, have the potential to outweigh selection (Gilroy et al, ). However, because there were generally poor correlations across data sets in our study, it is also reasonable to presume that the various data sets also contain local information across the genome.…”

“…With the growing availability of various data sets in molecular ecology, we are increasingly able to ask questions about the extent to which neutral vs. adaptive processes shape patterns of diversity in natural populations (Grueber et al, 2013;Pearson, Bull, & Gardner, 2018;Sutton, Nakagawa, Robertson, & Jamieson, 2011). This is particularly relevant in small populations, which experience significant genetic drift and are under threat from novel environmental and ecological pressures (Gilroy, Phillips, Richardson, & van Oosterhout, 2017). For example, studies of large populations have revealed strong adaptive processes that shape MHC diversity (Gillingham et al, 2017;Schwensow et al, 2016), but are these strong enough to overcome "systemic" effects of inbreeding across the whole genome?…”

Urban colonization through multiple genetic lenses: The city‐fox phenomenon revisited

“…For example, we detected possible balancing selection at MHC Class I and II loci, compared to possible directional selection acting on MHC Class III loci. Interpretations must currently remain conservative, as it is difficult to parse contemporary from historical signatures of selection in recently bottlenecked populations (Gilroy, Phillips, Richardson, & Oosterhout, ).…”

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

“…2015, 2018), bank voles (Kloch et al. 2018), and birds (Alcaide and Edwards 2011; Gilroy et al. 2017; Velová et al.…”