Fitness landscapes support the dominance theory of post-zygotic isolation in the mussels Mytilus edulis and M. galloprovincialis

Abstract

We studied the genetic basis of post-zygotic isolation in the marine mussels Mytilus edulis and Mytilus galloprovincialis. Evidence was obtained for a high number of recessive Dobzhansky-Muller substitutions in the genome of these two mussel taxa. We analysed the segregation of unlinked diagnostic markers in the progeny of two backcrosses and an F2 cross, 36 h and 200 days after fertilization. Directional selection favouring M. galloprovincialis genotypes was observed in both kinds of cross. In the F2, epistatic interactions between each pair of chromosome fragments mapped by the markers were identified in addition. Our results imply that homozygous-homozygous interactions are required for breakdown of coadaptation, in accordance with the dominance theory of post-zygotic isolation. Endogenous post-zygotic selection distributed over many loci throughout the genome provides the missing factor explaining the astonishing persistence and strength of barriers to neutral introgression in such a dispersive taxon as Mytilus.

Figure 1

(a) Observed tri-locus hybrid index distribution in backcrosses (pooling the two backcrosses, BC1 and BC2, over the two sampling times, 36 h and D200), expected hybrid index distribution from single-locus frequencies with the assumption of no linkage and expected hybrid index distribution from single-locus Mendelian expectations and no linkage. (b) The deviations of the observed distribution from the Mendelian expectation with no linkage and the expectation from single-locus frequencies and no linkage.

Figure 2

(a) Tri-locus hybrid index distributions in the F₂ generation, 36 h and 200 days after fertilization; and (b) deviation from the Mendelian expectation with no linkage in the D200 sample.

Figure 3

(a–c) Bi-locus fitness landscapes in the F₂ generation. (d) Averaged pairwise landscape obtained by considering symmetrical genotypes (e.g. EEGG and GGEE) to be identical.

Figure 4

Cline shapes and linkage disequilibria, D, obtained from a simple two-locus one-dimensional stepping-stone model. The black arrow gives the direction of propagation of waves of advance. Bold lines are the results obtained with the averaged pairwise landscape of figure 3d. Thin lines are the results obtained with an additive model with a selection coefficient of 0.175.