Abstract
Genetic variants that are neutral within, but deleterious between, populations (Dobzhansky-Muller Incompatibilities) are thought to initiate hybrid dysfunction and then to accumulate and complete the speciation process. To identify the types of genetic differences that might initiate speciation, it is useful to study inter-population (intra-species) hybrids that exhibit reduced fitness. In Caenorhabditis briggsae, a close relative of the nematode C. elegans, such minor genetic incompatibilities have been identified. One incompatibility between the mitochondrial and nuclear genomes reduces the fitness of some hybrids. To understand the nuclear genetic architecture of this epistatic interaction, we constructed two sets of recombinant inbred lines by hybridizing two genetically diverse wild populations. In such lines, selection is able to eliminate deleterious combinations of alleles derived from the two parental populations. The genotypes of surviving hybrid lines thus reveal favorable allele combinations at loci experiencing selection. Our genotype data from the resulting lines are consistent with the interpretation that the X alleles participate in epistatic interactions with autosomes and the mitochondrial genome. We evaluate this possibility given predictions that mitochondria-X epistasis should be more prevalent than between mitochondria and autosomes. Our empirical identification of inter-genomic linkage disequilibrium supports the body of literature indicating that the accumulation of mito-nuclear genetic incompatibilities might initiate the speciation process through the generation of less-fit inter-population hybrids.
Highlights
Biological species comprise genetically related populations of organisms whose inter-population hybrid offspring suffer complete loss of fitness: either hybrid inviability or hybrid sterility (Mayr, 1942)
The study of mito-nuclear epistatic interactions segregating within populations offers the opportunity to better understand the genetic basis of incipient speciation (Chou and Leu, 2010; Johnson, 2010; Burton and Barreto, 2012; Hill, 2015)
With both intra-specific and inter-specific genetic incompatibilities segregating in C. briggsae populations, this species is ideal for studying speciation genetics (Woodruff et al, 2010; Kozlowska et al, 2012; Yan et al, 2012; Bi et al, 2015), especially with respect to the involvement of mitochondria in generating deleterious epistatic interactions in hybrids
Summary
Biological species comprise genetically related populations of organisms whose inter-population hybrid offspring suffer complete loss of fitness: either hybrid inviability or hybrid sterility (Mayr, 1942). Understanding the mechanistic process of how one formerly interbreeding population becomes two such reproductively isolated species occupies much of the contemporary study of speciation. This focus has, generally, taken the form of identifying the molecular and genetic basis. Deleterious epistatic interactions between genetic variants contributed by both parents at fertilization can produce hybrid dysfunction phenotypes like hybrid inviability or hybrid sterility. These effects, by definition, reduce hybrid fitness to zero and eliminate gene flow between the nascent species. More mild hybrid dysfunction phenotypes, such as developmental delay, might reduce gene flow
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