Natural Variation for a Hybrid Incompatibility Between Two Species of Mimulus

Abstract

Understanding the process by which hybrid incompatibility alleles become established in natural populations remains a major challenge to evolutionary biology. Previously, we discovered a two-locus Dobzhansky-Muller incompatibility that causes severe hybrid male sterility between two inbred lines of the incompletely isolated wildflower species, Mimulus guttatus and M. nasutus.An interspecific cross between these two inbred lines revealed that the M. guttatus (IM62) allele at hybrid male sterility 1 (hms1) acts dominantly in combination with recessive M. nasutus (SF5) alleles at hybrid male sterility 2 (hms2) to cause nearly complete hybrid male sterility. In this report, we extend these genetic analyses to investigate intraspecific variation for the hms1-hms2 incompatibility in natural populations of M. nasutus and M. guttatus, performing a series of interspecific crosses between individuals collected from a variety of geographic locales. Our results suggest that hms2 incompatibility alleles are common and geographically widespread within M. nasutus, but absent or rare in M. guttatus. In contrast, the hms1 locus is polymorphic within M. guttatus and the incompatibility allele appears to be extremely geographically restricted. We found evidence for the presence of the hms1 incompatibility allele in only two M. guttatus populations that exist within a few kilometers of each other. The restricted distribution of the hms1 incompatibility allele might currently limit the potential for the hms1-hms2 incompatibility to act as a species barrier between sympatric populations of M. guttatus and M. nasutus. Extensive sampling within a single M. guttatus population revealed that the hms1 locus is polymorphic and that the incompatibility allele appears to segregate at intermediate frequency, a pattern that is consistent with either genetic drift or natural selection.KEY WORDS: Dobzhansky-Muller incompatibility, hybrid incompatibility, Mimulus, natural variation, speciation.Postzygotic reproductive isolation typically evolves when diverging populations accumulate different alleles at multiple loci that are incompatible when brought together in hybrid genomes; negative epistasis between the heterospecific alleles renders hybrids inviable or sterile (this scenario is commonly referred to as the Dobzhansky-Muller model;Bateson 1909;Dobzhansky 1937;Muller 1942). Recent studies have described in detail the genetic architecture of hybrid incompatibility (e.g. Harushima

Geographical variation in postzygotic isolation and its genetic basis within and between twoMimulusspecies

“…Vickery (1956Vickery ( , 1973Vickery ( , 1978 and Sweigart et al (2007) provided evidence that postzygotic isolation within and among populations of both species varied geographically, though biometrical line crosses were not used to determine the genetic basis. In one particular cross of two inbred lines, the main nuclear and mitochondrial loci underlying two forms of hybrid male sterility were mapped, and at least some of the alleles were shown to have restricted geographical distributions (Sweigart et al 2007;Case & Willis 2008). However, the extent to which this isolation varied across the geographical ranges of these largely sympatric species was unclear.…”

“…This suggests that the nuclear incompatibility alleles involved are not polymorphic within species, but several considerations argue strongly against this. First, genetic mapping studies and laborious testcross analysis of the two major loci, hms1 and hms2, underlying hybrid sterility in the Oregon IM Â SF cross revealed that, while the M. nasutus hms2 incompatibility allele appears fixed within that species, the M. guttatus hms1 incompatibility allele is geographically localized at intermediate frequencies only in the IM population (Sweigart et al 2007). At least some of the individuals that we sampled from that population probably lacked that allele, since we did not observe complete sterility in any F 2 s in the cross with the M. nasutus SF population (Sweigart et al 2006).…”

“…Previous crossing and mapping studies have provided evidence for population variation in postzygotic isolation owing to reduced seed set, germination and two forms of hybrid sterility (e.g. Vickery 1978;Martin & Willis 2007;Sweigart et al 2007;Case & Willis 2008). But because these studies involved crosses with a few inbred lines or populations of each species, the extent of isolation and its variation among populations is largely unknown.…”

Geographic variation in hybridization across a reinforcement contact zone of chorus frogs (Pseudacris)

“…First, hybrid incompatibilities may vary across geography, such that selection against hybridization is stronger in some regions or acts at different life history stages across areas (Parris, 2001; Sætre, Kr.l, M., Bureš, S., & Ims, R. A. 1999; Sweigart, Mason, & Willis, 2007; Veen et al., 2001). In chorus frogs, even males derived from the same population vary substantially in levels of hybrid sterility, lending support for this hypothesis (Lemmon & Lemmon, 2010).…”

Evolution of reproductive isolation in plants

“…But intraspecific polymorphisms for hybrid sterility factors are not restricted to highly selfing species. One such factor causing hybrid male sterility in crosses between the outcrossing Mimulus guttatus and the selfing M. nasutus was found to be polymorphic in the outcrossing M. guttatus and to be strongly geographically restricted (Sweigart et al, 2007).…”