A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus

Abstract

Much evidence has shown that postzygotic reproductive isolation (hybrid inviability or sterility) evolves by the accumulation of interlocus incompatibilities between diverging populations. Although in theory only a single pair of incompatible loci is needed to isolate species, empirical work in Drosophila has revealed that hybrid fertility problems often are highly polygenic and complex. In this article we investigate the genetic basis of hybrid sterility between two closely related species of monkeyflower, Mimulus guttatus and M. nasutus. In striking contrast to Drosophila systems, we demonstrate that nearly complete hybrid male sterility in Mimulus results from a simple genetic incompatibility between a single pair of heterospecific loci. We have genetically mapped this sterility effect: the M. guttatus allele at the hybrid male sterility 1 (hms1) locus acts dominantly in combination with recessive M. nasutus alleles at the hybrid male sterility 2 (hms2) locus to cause nearly complete hybrid male sterility. In a preliminary screen to find additional small-effect male sterility factors, we identified one additional locus that also contributes to some of the variation in hybrid male fertility. Interestingly, hms1 and hms2 also cause a significant reduction in hybrid female fertility, suggesting that sex-specific hybrid defects might share a common genetic basis. This possibility is supported by our discovery that recombination is reduced dramatically in a cross involving a parent with the hms1-hms2 incompatibility.

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

“…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). This strongly suggests that other loci are also involved in the sterility in this cross.…”

A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern,Ceratopteris richardii

“…This contrasts with recent studies in Drosophila, where several genes have recently been cloned that cause almost complete reproductive isolation (Tinget al 1998;Barbash et al 2003;Presgraves 2003;Masly et al 2006). Likewise, major QTL for sterility are frequently detected in flowering plants (Moyle and Graham 2005;Fishman and Willis 2006;Sweigart et al 2006). The lack of major QTL for spore viability in ferns might be due to the use of DHLs for QTL mapping.…”

“…Reproductive isolation has long been thought to accumulate gradually following population separation (Stebbins 1950;Dobzhansky 1951;Mayr 1963;Coyne and Orr 1989), but an understanding of reproductive isolation at the genetic and molecular levels did not emerge until recently. Genetic mapping of hybrid incompatibilities has provided insights into the number, location, and effect of the genetic factors underlying intrinsic postzygotic reproductive barriers (Naveira 1992;True et al 1996;Coyne et al 1998;Presgraves 2003;Tao et al 2003a,b;Moyle and Graham 2005;Fishman and Willis 2006;Sweigart et al 2006). Likewise, studying transmission ratio distortion (TRD) of marker loci in segregating hybrid populations has proven to be a sensitive assay for loci underlying reproductive barriers between parental populations (e.g., Fishman et al 2001a;Harushima et al 2002;Hall and Willis 2005).…”

Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

“…This is particularly striking in the context of other forms of male sterility in Mimulus hybrids. A nuclear Dobzhansky-Muller incompatibility causes complete pollen sterility (many unfilled pollen grains) in a fraction of F 2 hybrids between the same parental lines (Fishman and Willis, 2001;Sweigart et al, 2006). However, in this case, maximum seed set was also greatly reduced in male steriles (Sweigart et al, 2006), causing positive correlations between male and female fertility (Fishman and Willis, 2001).…”