The type of bottleneck matters: Insights into the deleterious variation landscape of small managed populations

Abstract

Predictions about the consequences of a small population size on genetic and deleterious variation are fundamental to population genetics. As small populations are more affected by genetic drift, purifying selection acting against deleterious alleles is predicted to be less efficient, therefore increasing the risk of inbreeding depression. However, the extent to which small populations are subjected to genetic drift depends on the nature and time frame in which the bottleneck occurs. Domesticated species are an excellent model to investigate the consequences of population bottlenecks on genetic and deleterious variation in small populations. This is because their history is dominated by known bottlenecks associated with domestication, breed formation and intense selective breeding. Here, we use whole-genome sequencing data from 97 chickens representing 39 traditional fancy breeds to directly examine the consequences of two types of bottlenecks for deleterious variation: the severe domestication bottleneck and the recent population decline accompanying breed formation. We find that recently bottlenecked populations have a higher proportion of deleterious variants relative to populations that have been kept at small population sizes since domestication. We also observe that long tracts of homozygous genotypes (runs of homozygosity) are proportionally more enriched in deleterious variants than the rest of the genome. This enrichment is particularly evident in recently bottlenecked populations, suggesting that homozygosity of these variants is likely to occur due to genetic drift and recent inbreeding. Our results indicate that the timing and nature of population bottlenecks can substantially shape the deleterious variation landscape in small populations. K E Y W O R D S deleterious variants, domestication, effective population size, population bottleneck, runs of homozygosity, small population | 331 BORTOLUZZI eT aL.

Prioritizing sequence variants in conserved non-coding elements in the chicken genome using chCADD

“…We used a dataset by Bortoluzzi and colleagues available at the European Nucleotide Archive (http://www.ebi.ac.uk/ena/) under accession number PRJEB34245 [31] and PRJEB36674 [18]. The dataset comprised a total of 169 individuals sampled from 88 traditional chicken breeds of divergent demographic and selection history.…”

Using whole-genome sequencing data for demographic and functional evaluations of small managed populations

“…The hypothesis that the type and time-frame of a population decline have important consequences on a population's genetic variation was more formally analysed in local chicken breeds by Bortoluzzi et al (2020) (Chapter 3). In fact, the authors showed that populations that remained small for a long period of time have been able to minimize the effects of genetic drift on the deleterious variation contrary to recently bottlenecked populations that are more susceptible to genetic stochasticity [25]. These conclusions have important implications for management, as also illustrated in recent simulations of Kyriazis et al (2019).…”

“…Over time, if unrestrained, the amount of genetic variation necessary for adaptation is expected to erode, taking a population (or species) to the brink of extinction [162]. Although the effects of genetic drift on individual genomes have been thought to be gradual, recent studies have shown that the response of a population to genetic drift depends on the type and time-frame of the bottleneck [25] (Chapter 3), the (long-term) persistence of a population small in size [174,256], and the presence of a conservation programme [1,28] (Chapter 4).…”

“…In fact, genetic drift can reduce the viability and adaptive potential of a population [170]. Recent studies in wild and domesticated species [257,318,292,25,1] have shown that the risk of extinction in small populations is also a consequence of harmful mutations that can lower the fitness of an individual carrying them. The rationale is the reduced efficiency of natural selection at purging harmful mutations because of genetic drift [223,165].…”

From sequence to phenotype: the impact of deleterious variation in livestock

“…This can be inferred by quantifying homozygous stretches in the genome called runs of homozygosity (ROH). ROHs are enriched for homozygous deleterious variants (Bortoluzzi et al 2019), and therefore is useful as indicator for inbreeding risk. While both methods can provide accurate estimates of the deleterious load, it usually does not provide any lead to the effects of any particular deleterious variants, nor does it indicate which variants contribute to the negative fitness effects in inbred populations (if present).…”