Incompatibility between X chromosome factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species

The Dobzhansky-Muller model posits that postzygotic reproductive isolation results from the evolution of incompatible epistatic interactions between species: alleles that function in the genetic background of one species can cause sterility or lethality in the genetic background of another species. Progress in identifying and characterizing factors involved in postzygotic isolation in Drosophila has remained slow, mainly because Drosophila melanogaster, with all of its genetic tools, forms dead or sterile hybrids when crossed to its sister species, D. simulans, D. sechellia, and D. mauritiana. To circumvent this problem, we used chromosome deletions and duplications from D. melanogaster to map two hybrid incompatibility loci in F(1) hybrids with its sister species. We mapped a recessive factor to the pericentromeric heterochromatin of the X chromosome in D. simulans and D. mauritiana, which we call heterochromatin hybrid lethal (hhl), which causes lethality in F(1) hybrid females with D. melanogaster. As F(1) hybrid males hemizygous for a D. mauritiana (or D. simulans) X chromosome are viable, the lethality of deficiency hybrid females implies that a dominant incompatible partner locus exists on the D. melanogaster X. Using small segments of the D. melanogaster X chromosome duplicated onto the Y chromosome, we mapped a dominant factor that causes hybrid lethality to a small 24-gene region of the D. melanogaster X. We provide evidence suggesting that it interacts with hhl(mau). The location of hhl is consistent with the emerging theme that hybrid incompatibilities in Drosophila involve heterochromatic regions and factors that interact with the heterochromatin.     

LABORATORY EXPERIMENTS ON SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS?

We integrate experimental studies attempting to duplicate all or part of the speciation process under controlled laboratory conditions and ask what general conclusions can be made concerning the major models of speciation. Strong support is found for the evolution of reproductive isolation via pleiotropy and/or genetic hitchhiking with or without allopatry. Little or no support is found for the bottleneck and reinforcement models of speciation. We conclude that the role of geographical separation in generating allopatry (i.e., zero gene flow induced by spatial isolation) has been overemphasized in the past, whereas its role in generating diminished gene flow in combination with strong, discontinuous, and multifarious divergent selection, has been largely unappreciated.     

Does the speciation clock tick more slowly in the absence of heteromorphic sex chromosomes?

Squamates may be an attractive group in which to study the influence of sex chromosomes on speciation rates because of the repeated evolution of heterogamety (both XY and ZW), as well as an apparently large number of taxa with environmental sex-determination.     

The genomics of incompatibility factors and sex determination in hybridizing species of Cottus (Pisces)

Cottus rhenanus and Cottus perifretum have formed hybrid lineages and narrow hybrid zones that can be best explained through the action of natural selection. However, the underlying selective forces as well as their genomic targets are not well understood. This study identifies genomic regions in the parental species that cause hybrid incompatibilities and tests whether these manifest in a sex-specific manner to learn about processes that affect natural hybridization in Cottus. Interspecific F₂ crosses were analyzed for 255 markers for genetic mapping and to detect transmission distortion as a sign for genetic incompatibilities. The Cottus map consists of 24 linkage groups with a total length of 1575.4 cM. A male heterogametic (XY) sex determination region was found on different linkage groups in the two parental species. Genetic incompatibilities were incomplete, varied among individuals and populations and were not associated with the heterogametic sex. The variance between populations and individuals makes it unlikely that there are species-specific incompatibility loci that could affect the gene pool of natural hybrids in a simple and predictable way. Conserved synteny with sequenced fish genomes permits to genetically study the Cottus genome through the transfer of genomic information from the model fish species. Homology relationships of candidate genomic regions in Cottus indicate that sex determination is not based on the same genomic regions found in other fish species. This suggests a fast evolutionary turnover of the genetic basis of sex determination that, together with the small size of the heterogametic regions, may contribute to the absence of fitness effects related to the Haldane''s rule.