A constellation of dysfunctional hybrid phenotypes enforces reproductive isolation between Caenorhabditis nematode species.

Abstract

The evolution of complete reproductive isolation hinges on the cumulative action of reproductive isolating barriers that can manifest throughout the life cycle of an organism. Consequently, a comprehensive understanding of the features underlying the origin and maintenance of species requires assessing the relative contributions of distinct barriers to overall reproductive isolation. Here we characterize multiple interrelated isolating barriers for the nematode sister species Caenorhabditis remanei and Caenorhabditis latens. We quantified F1 hybrid male sterility and characterized multiple phenotypic causes associated with developmental abnormalities in the germline as well as non-germline gonad and somatic tissues, uncovering a complex suite of developmental defects contributing to strong postzygotic reproductive isolation. Despite these multifarious isolating barrier traits, assays testing for interspecies sperm transfer under "choice" conditions did not yield evidence of premating isolation. In contrast to other Caenorhabditis species pairs, we also found no evidence that ectopic sperm migration acts as a postmating-prezygotic barrier. The constellation of phenotypic defects in hybrids points to a polygenic or highly pleiotropic basis for hybrid dysfunction and implicates more rapid evolution of intrinsic postzygotic reproductive isolation than prezygotic isolation in these organisms.