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’

Gilroy, DL; Phillips, KP; Richardson, DS; van Oosterhout, C

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.

Citation

Gilroy, D., Phillips, K., Richardson, D., & van Oosterhout, C. (2017). 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’. Journal of Evolutionary Biology, 30(7), 1276-1287. https://doi.org/10.1111/jeb.13077

• Journal Article Type: Article
• Acceptance Date: Mar 21, 2017
• Online Publication Date: Mar 28, 2017
• Publication Date: Jul 11, 2017
• Deposit Date: Sep 29, 2021
• Journal: Journal of Evolutionary Biology
• Print ISSN: 1010-061X
• Electronic ISSN: 1420-9101
• Publisher: Wiley
• Volume: 30
• Issue: 7
• Pages: 1276-1287
• DOI: https://doi.org/10.1111/jeb.13077
• Publisher URL: http://dx.doi.org/10.1111/jeb.13077
• Related Public URLs: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1420-9101/
• Additional Information: Access Information : This article is available to read for free using the link above.; Funders : Natural Environment Research Council (NERC);Earth and Life Systems Alliance (ELSA); Projects : Transgenerational impacts on senescence: quantitative genetics of cellular and organismal ageing in the wild; Grant Number: NE/K005502/1; Grant Number: NER/I/S/2002/00712