Academic journal article Genetics

A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus

Academic journal article Genetics

A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus

Article excerpt

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.

IN the classic model of allopatric speciation, a single species splits into two or more geographically isolated populations that thereafter diverge independently. Integral to the completion of this process is the evolution of reproductive isolation among nascent species, which is essential to prevent gene exchange upon secondary contact. Complete isolation may be caused by any combination of reproductive barriers, including hybrid inviability or sterility. Although Darwin and his contemporaries were well aware of the propensity for interspecific hybrids to be inviable or sterile, they were naïve of genetics and thus could not conceive how such inherently maladaptive traits might evolve. The key insight of the genie model of postzygotic isolation, proposed independently by BATESON (1909), DOBZHANSKY (1937), and MULLER (1942) (commonly known as the Dobzhansky-Muller model), was that epistasis among two or more genes allows hybrid inviability or sterility to evolve without reducing the fitness of either ancestral lineage. In this model, alternate multilocus allele combinations evolve among geographically isolated populations, and inviability or sterility occurs only when novel incompatible genotypes come together in hybrids.

Soon after its conception, strong evidence for the Dobzhansky-Muller model of postzygotic isolation emerged from classical genetic demonstrations of hybrid incompatibilities in animals (e. g., PHILLIPS 1921; BELLAMY 1922; DOBZHANSKY 1937; COLE and HOLLANDER 1950) and plants (e. g., HOLLINGSHEAD 1930; HUTCHINSON 1932; CLAUSEN et al. 1940, 1941; BABCOCK et al. 1942; AVERS 1953). Recent years have seen resurgence in speciation research, accompanied by a directed effort to genetically map factors that contribute to hybrid incompatibilities (HOLLOCHER and Wu 1996; TRUE et al. 1996; Li et al. 1997; HARUSHIMA et al. 2001, 2002; PRESGRAVES 2003; TAO et al. 2003b; MOYLE and GRAHAM 2005). A few studies have even identified the genes that cause hybrid inviability and sterility (WITTBRODT et al. 1989; TING et al. 1998; BARBASH et al. 2003; PRESGRAVES et al. 2003). To date, much of our understanding of the genetics of postzygotic isolation is based on empirical studies of divergence between Drosophila species. Indeed, several patterns appear to characterize the genetic basis of hybrid incompatibility in Drosophila (reviewed in COYNE and ORR 2004) : ( 1 ) hybrid incompatibility alleles are generally recessive (PRESGRAVES 2003; TAO et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.