Developmental rate displays effects of inheritance but not of sex in inter-population hybrids of Tigriopus californicus

Abstract

Coevolved interactions between mitochondrial-encoded and nuclear-encoded genes within populations can be disrupted by inter-population hybridization resulting in reduced hybrid fitness. This hybrid breakdown may be an important factor contributing to reproductive isolation between populations or species, and strong selection among hybrids to maintain compatible mitonuclear genotypes occurs in at least some species. Despite potentially differential consequences of mitonuclear incompatibilities in females and males due to maternal inheritance of the mitochondrial genome, the extent to which phenotypic variation associated with hybrid breakdown is sex-specific and heritable remains unresolved. Here we present two experiments investigating variation in developmental rate among reciprocal inter-population hybrids of the intertidal copepod Tigriopus californicus. Developmental rate is a proxy for fitness in this species that is substantially influenced by variation in mitonuclear compatibility among hybrids. First, we show that F2 hybrid developmental rate is the same in females and males, suggesting that effects of mitonuclear incompatibilities on this trait are likely experienced equally by the two sexes. Second, we demonstrate that variation in developmental rate among F3 hybrids is heritable; times to copepodid metamorphosis of F4 offspring of fast-developing F3 parents (12.25 {+/-} 0.05 d, {+/-} SEM) were significantly faster than those of F4 offspring of slow-developing parents (14.58 {+/-} 0.05 d). Taken together, these results provide evidence for strong effects of mitonuclear interactions across generations of hybrid eukaryotes with no differences between the sexes, and support key roles of mitonuclear incompatibility in hybrid breakdown and reproductive isolation.