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HYBRID INCOMPATIBILITIES
The development of postzygotic barriers, particularly hybrid sterility and inviability, is a key stage in the speciation process. However, despite a strong theoretical framework, we know surprisingly little about the evolutionary history and genetic mechanisms of hybrid incompatibilities in plants.  Our explorations of hybrid sterility in interspecific  Mimulus hybrids are revealing the processes that drive divergence between species as well as those that generate variation within species.

Dobzhansky-Muller incompatibilities and hybrid sterility

Hybrid sterility may be caused by chromosomal rearrangements or by genic interactions (Dobzhansky-Muller incompatibilities).  Crosses between M. nasutus (selfer) and M. guttatus exhibit partial sterility consistent with D-M incompatibilities (Fishman & Willis 2001) and we have mapped two loci that jointly cause male and female sterility in F2 hybrids (Sweigart et al. 2006).  Fine-mapping and within-species characterization of these D-M loci is being led by collaborator Andrea Sweigart, currently a postdoc in the lab. 

 

Chromosomal rearrangements, hybrid sterility, and local adaptation

Mechanisms of postzygotic isolation may vary broadly within Mimulus. In contrast to the yellow monkeyflowers, hybrids between Mimulus lewisii and M. cardinalis exhibit the underdominant hybrid male sterility consistent with chromosomal rearrangements as a direct cause of meiotic dysfunction in heterospecific heterozygotes. Comparative linkage mapping indicates that at least two inversions and one translocation distinguish these closely related sister taxa, and QTLs for both pre-mating barriers (flower color, nectar volume, elevational adaptation, etc.) and post-mating barriers cluster in rearranged regions (Fishman et al. , in revision). To test chromosomal models of ecological speciation, Ph.D. student Angela Stathos is now investigating the fitness costs, geographic distribution, and filtering effects of rearrangements in experimental and naturally occurring hybrids.

 

Cytoplasmic male sterility

Incompatibilities between cytoplasmic (mitochrondrial and chloroplast) genomes and nuclear genes are theoretically likely, common in crop plants, and potentially widespread among wild plant populations.  Theory predicts than any maternally-transmitted element that causes male sterility, but that increases female fertility even slightly, should selfishly spread through a population.  However, the individual fitness costs of male sterility, as well as frequency-dependent selection for maleness, should concomittantly select for nuclear alleles that restore male function. Once both elements have reached fixation, the population appears hermaphroditic again, but CMS may be revealed in hybrids with other populations or species. The coevolutionary dynamics of CMS-restoration cause rapid genome turnover, are essential to the evolution of gynodioecy, and may contribute to the development of species barriers. 

M. guttatus x M. nasutus hybrids segregate for an anther-sterile phenotype consistent with M. guttatus carrying both a CMS mitochondrial genome and the dominant nuclear allele at a locus controlling restoration of male fertility (Rf). Rf maps as a single Mendelian locus (Fishman & Willis 2006) with pleiotropic effects on flower size characters (Barr & Fishman 2010b). Like Rf loci in crop plants, the Mimulus restorer maps to a cluster of tandemly duplicated pentatricopeptide repeat (PPR) genes (Barr & Fishman 2010a). Ongoing projects include positional cloning of Rf and examination of the signature of selection in the region (with former postdoc Camille Barr) and studies of the geographical distribution of both nuclear and mitochrondrial components of CMS within M. guttatus (with collaborator Andrea Case at Kent University).