Academic journal article Genetics

Sequence Diversity, Reproductive Isolation and Species Concepts in Saccharomyces

Academic journal article Genetics

Sequence Diversity, Reproductive Isolation and Species Concepts in Saccharomyces

Article excerpt

ABSTRACT

Using the biological species definition, yeasts of the genus Saccharomyces sensu stricto comprise six species and one natural hybrid. Previous work has shown that reproductive isolation between the species is due primarily to sequence divergence acted upon by the mismatch repair system and not due to major gene differences or chromosomal rearrangements. Sequence divergence through mismatch repair has also been shown to cause partial reproductive isolation among populations within a species. We have surveyed sequence variation in populations of Saccharomyces sensu stricto yeasts and measured meiotic sterility in hybrids. This allows us to determine the divergence necessary to produce the reproductive isolation seen among species. Rather than a sharp transition from fertility to sterility, which may have been expected, we find a smooth monotonic relationship between diversity and reproductive isolation, even as far as the well-accepted designations of S. paradoxus and S. cerevisiae as distinct species. Furthermore, we show that one species of Saccharomyces-S. cariocanus-differs from a population of S. paradoxus by four translocations, but not by sequence. There is molecular evidence of recent introgression from S. cerevisiae into the European population of S. paradoxus, supporting the idea that in nature the boundary between these species is fuzzy.

THE concept of a species is central to the biological sciences (Mallet 1995; Coyne and Orr 1998), but the definition of a species is controversial. There are several sometimes conflicting definitions of species. The biological species concept (BSC) is based on patterns of breeding: species are considered to be units reproductively isolated from other such units, but within which interbreeding and genetic recombination reduce the possibility of divergence. Asexual reproduction in many organisms including fungi (Taylor et al. 2000), hybridization in plants (Rieseberg 1997) and fungi (Taylor et al. 2000), and lateral gene transfer between bacteria (Gogarten and Townsend 2005) create problems for the BSC. The genotypic cluster species concept (GCSC) can accommodate some gene flow between species (clusters) as long as their integrity remains such that they can be distinguished (Mallet 1995). Genotypic clusters can be at the subpopulation level as well as at species level. The phylogenetic species concept (PSC) defines the species as a distinct monophyletic group on the basis of evolutionary history and geographical extent. This concept faces the difficulties of incomplete knowledge and a somewhat arbitrary delineation of specific boundaries (Hudson and Coyne 2002).

Sequence and chromosomal evolution can produce genetic divergence and can reduce or prevent interbreeding, as required by these species concepts. Although these concepts do not always agree (Isaac et al. 2004), early analyses of Saccharomyces strains by interbreeding (Naumov 1987) (BSC) and DNA/DNA reassociation (Martini and Martini 1987; Vaughan Martini 1989) (PSC) were concordant in supporting the existence of three distinct species: Saccharomyces cerevisiae, S. paradoxus, and S. bayanus. These studies also confirmed the identification of one natural hybrid (S. pastorianus). Recent studies of reproductive compatibility have defined three new species within the complex on the basis of BSC: S. cariocanus, S. mikatae, and S. kudriavzevii (Naumov et al. 1995a,b, 2000).

S. cerevisiae is a well-known model organismassociated with human activity (baking and brewing). Its closest relative is S. paradoxus, which is often isolated from Quercus (oak) trees and has little or no association with human activity. The two species show perfect synteny with no gross chromosomal rearrangements between them (Fischer et al. 2000; Kellis et al. 2003) and a level of sequence divergence of ~15% (Cliften et al. 2001). The different species within the sensu stricto complex can mate and generate viable hybrids, indicating an absence of prezygotic isolation. …

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