Abstract
Epistasis may have important consequences for a number of issues in quantitative genetics and evolutionary biology. In particular, synergistic epistasis for deleterious alleles is relevant to the mutation load paradox and the evolution of sex and recombination. Some studies have shown evidence of synergistic epistasis for spontaneous or induced deleterious mutations appearing in mutation-accumulation experiments. However, many newly arising mutations may not actually be segregating in natural populations because of the erasing action of natural selection. A demonstration of synergistic epistasis for naturally segregating alleles can be achieved by means of inbreeding depression studies, as deleterious recessive allelic effects are exposed in inbred lines. Nevertheless, evidence of epistasis from these studies is scarce and controversial. In this paper, we report the results of two independent inbreeding experiments carried out with two different populations of Drosophila melanogaster. The results show a consistent accelerated inbreeding depression for fitness, suggesting synergistic epistasis among deleterious alleles. We also performed computer simulations assuming different possible models of epistasis and mutational parameters for fitness, finding some of them to be compatible with the results observed. Our results suggest that synergistic epistasis for deleterious mutations not only occurs among newly arisen spontaneous or induced mutations, but also among segregating alleles in natural populations.
Highlights
Epistasis is expected to arise from the interaction of genes in complex biological networks whose expression is tightly regulated and coordinated (Pérez-Pérez et al 2009; de Visser et al 2011; Hsuan-Chao Chiu et al 2012; Sohail et al 2017), and may have important consequences for a number of issues in quantitative genetics and evolutionary biology (Wagner et al 1998; Wolf et al 2000)
The population of Exp I had been maintained in the laboratory for about 100 generations before the inbreeding experiment, whereas that of Exp II was evaluated only 13 generations after its capture, being likely to keep its genetic composition close to that of the original natural population
A number of mutation-accumulation experiments have shown some evidence of synergistic epistasis (e.g., Mukai 1969; Whitlock and Bourguet 2000; Dickinson 2008)
Summary
Epistasis is expected to arise from the interaction of genes in complex biological networks whose expression is tightly regulated and coordinated (Pérez-Pérez et al 2009; de Visser et al 2011; Hsuan-Chao Chiu et al 2012; Sohail et al 2017), and may have important consequences for a number of issues in quantitative genetics and evolutionary biology (Wagner et al 1998; Wolf et al 2000). Inbreeding depression may occur either under the partial dominance hypothesis, where deleterious recessive allelic effects are exposed in homozygosis in inbred lines, or under the overdominance hypothesis, which implies heterozygote advantage for fitness. Assuming a model of inbreeding depression caused by the increase in the frequency of homozygous deleterious mutations by inbreeding, a linear decline of fitness with the inbreeding coefficient implies absence of epistasis whereas synergistic epistasis is expected to produce an accelerated decline in fitness (Lynch and Walsh 1998). We show results from two laboratory experiments using full-sib lines founded from two different natural populations of Drosophila melanogaster, which show a consistent accelerated decline for fitness, pointing towards synergistic epistasis among naturally segregating deleterious alleles. We propose a model of epistasis able to explain the empirical results
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