Abstract
Dobzhansky-Muller incompatibilities can result from the interactions of more than a single pair of interacting genes and there are several different models of how such complex interactions can be structured. Previous empirical work has identified complex conspecific epistasis as a form of complex interaction that has contributed to postzygotic reproductive isolation between taxa, but other forms of complexity are also possible. Here, I probe the genetic basis of reproductive isolation in crosses of the intertidal copepod Tigriopus californicus by looking at the impact of markers in genes encoding metabolic enzymes in F2 hybrids. The region of the genome associated with the locus ME2 is shown to have strong, repeatable impacts on the fitness of hybrids in crosses and epistatic interactions with another chromosomal region marked by the GOT2 locus in one set of crosses. In a cross between one of these populations and a third population, these two regions do not appear to interact despite the continuation of a large effect of the ME2 region itself in both crosses. The combined results suggest that the ME2 chromosomal region is involved in incompatibilities with several unique partners. If these deleterious interactions all stem from the same factor in this region, that would suggest a different form of complexity from complex conspecific epistasis, namely, multiple independent deleterious interactions stemming from the same factor. Confirmation of this idea will require more fine-scale mapping of the interactions of the ME2 region of the genome.
Highlights
Dobzhansky-Muller (DM) incompatibilities are thought to underlie the evolution of much of the postzygotic reproductive isolation in hybrids, but the types of interactions involved in these incompatibilities are not well understood [1]
The T. californicus GOT2 protein is most closely related to a mitochondrial-targeted aspartate transaminase (ACO10233) found in another copepod species, and these fall within a group of arthropod mitochondrial-targeted aspartate transaminases proteins
There was a significant amount of inter-population divergence in GOT2 sequences in comparisons among seven different T. californicus populations and this divergence includes a large number of amino-acid changing mutations (Sequence alignment available in File S1)
Summary
Dobzhansky-Muller (DM) incompatibilities are thought to underlie the evolution of much of the postzygotic reproductive isolation in hybrids, but the types of interactions involved in these incompatibilities are not well understood [1]. A model developed by Kondrashov [10] suggests that with gene flow among populations, i.e. parapatry, that the initial DM incompatibility is likely to involve only a single pair of interacting loci; subsequent DM incompatibilities are more likely to involve interactions with the alleles in the first DM incompatibility and could involve multiple pairwise incompatibilities (as in Figure 1B) or more complex epistasis involving three or more alleles. At this point there are few clear examples from empirical studies of complexity stemming from the involvement of the same factor in multiple independent incompatibilities
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