Speciation and the developmental alarm clock.

New species arise as the genomes of populations diverge. The developmental 'alarm clock' of speciation sounds off when sufficient divergence in genetic control of development leads hybrid individuals to infertility or inviability, the world awoken to the dawn of new species with intrinsic post-zygotic reproductive isolation. Some developmental stages will be more prone to hybrid dysfunction due to how molecular evolution interacts with the ontogenetic timing of gene expression. Considering the ontogeny of hybrid incompatibilities provides a profitable connection between 'evo-devo' and speciation genetics to better link macroevolutionary pattern, microevolutionary process, and molecular mechanisms. Here, we explore speciation alongside development, emphasizing their mutual dependence on genetic network features, fitness landscapes, and developmental system drift. We assess models for how ontogenetic timing of reproductive isolation can be predictable. Experiments and theory within this synthetic perspective can help identify new rules of speciation as well as rules in the molecular evolution of development.

Genetic basis to hybrid inviability is more complex than hybrid male sterility in Caenorhabditis nematodes.

Hybrid male sterility often evolves before female sterility or inviability of hybrids, implying that the accumulation of divergence between separated lineages should lead hybrid male sterility to have a more polygenic basis. However, experimental evidence is mixed. Here, we use the nematodes Caenorhabditis remanei and C. latens to characterize the underlying genetic basis of asymmetric hybrid male sterility and hybrid inviability. We demonstrate that hybrid male sterility is consistent with a simple genetic basis, involving a single X-autosome incompatibility. We also show that hybrid inviability involves more genomic compartments, involving diverse nuclear-nuclear incompatibilities, a mito-nuclear incompatibility, and maternal effects. These findings demonstrate that male sensitivity to genetic perturbation may be genetically simple compared to hybrid inviability in Caenorhabditis and motivates tests of generality for the genetic architecture of hybrid incompatibility across the breadth of phylogeny.

Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule.

Deciphering the genetic and developmental causes of the disproportionate rarity, inviability, and sterility of hybrid males, Haldane's rule, is important for understanding the evolution of reproductive isolation between species. Moreover, extrinsic and prezygotic factors can contribute to the magnitude of intrinsic isolation experienced between species with partial reproductive compatibility. Here, we use the nematodes Caenorhabditis briggsae and C. nigoni to quantify the sensitivity of hybrid male viability to extrinsic temperature and developmental timing, and test for a role of mito-nuclear incompatibility as a genetic cause. We demonstrate that hybrid male inviability manifests almost entirely as embryonic, not larval, arrest and is maximal at the lowest rearing temperatures, indicating an intrinsic-by-extrinsic interaction to hybrid inviability. Crosses using mitochondrial substitution strains that have reciprocally introgressed mitochondrial and nuclear genomes show that mito-nuclear incompatibility is not a dominant contributor to postzygotic isolation and does not drive Haldane's rule in this system. Crosses also reveal that competitive superiority of X-bearing sperm provides a novel means by which postmating prezygotic factors exacerbate the rarity of hybrid males. These findings highlight the important roles of gametic, developmental, and extrinsic factors in modulating the manifestation of Haldane's rule.

Ribosomal DNA sequence polymorphism and the delineation of two ascosporic yeast species: Metschnikowia agaves and Starmerella bombicola.

The relationship between mating success and sequence divergence in the internal transcribed spacer (ITS)/5.8S-D1/D2 rDNA region was examined in isolates tentatively assigned to Metschnikowia agaves and Starmerella bombicola. Both species are haplontic and heterothallic, such that the formation of mature asci can be used as a measure of genetic compatibility. Parsimony haplotype network analysis and mating success confirmed that all known isolates of M. agaves are conspecific. The previously reported D1/D2 polymorphism of five substitutions was not corroborated; the maximum divergence observed between any two strains was three substitutions, four with ITS. Of 39 putative S. bombicola strains, 36 formed an ITS-D1/D2 haplotype network using the 95% criterion. Thirty-five strains could mate with one or more compatible partner. The excluded strains did not mate. Mature asci arose from crosses between individuals differing by as many as five, but not six or seven substitutions in the D1/D2 domain. All strains capable of mating formed mature asci with at least one partner and all network members could be linked to another member by three or fewer substitutions. These results support the use of sequence divergence as a criterion for species delineation, but caution against describing poorly sampled species solely on the basis of that criterion.