Minor Quantitative Trait Loci Underlie Floral Traits Associated With Mating System Divergence in Mimulus

Abstract

Abstract. The genetic basis of species differences provides insight into the mode and tempo of phenotypic divergence. We investigate the genetic basis of floral differences between two closely related plant taxa with highly divergent mating systems, Mimulus guttatus (large-flowered outcrosser) and M. nasutus (small-flowered selfer). We had previously constructed a framework genetic linkage map of the hybrid genome containing 174 markers spanning approximately 1800 cM on 14 linkage groups. In this study, we analyze the genetics of 16 floral, reproductive, and vegetative characters measured in a large segregating M. nasutus ϫ M. guttatus F 2 population (N ϭ 526) and in replicates of the parental lines and F 1 hybrids. Phenotypic analyses reveal strong genetic correlations among floral traits and epistatic breakdown of male and female fertility traits in the F 2 hybrids. We use multitrait composite interval mapping to jointly locate and characterize quantitative trait loci (QTLs) underlying interspecific differences in seven floral traits. We identified 24 floral QTLs, most of which affected multiple traits. The large number of QTLs affecting each trait (mean ϭ 13, range ϭ 11-15) indicates a strikingly polygenic basis for floral divergence in this system. In general, QTL effects are small relative to both interspecific differences and environmental variation within genotypes, ruling out QTLs of major effect as contributors to floral divergence between M. guttatus and M. nasutus. QTLs show no pattern of directional dominance. Floral characters associated with pollinator attraction (corolla width) and self-pollen deposition (stigma-anther distance) share several pleiotropic or linked QTLs, but unshared QTLs may have allowed selfing to evolve independently from flower size. We discuss the polygenic nature of divergence between M. nasutus and M. guttatus in light of theoretical work on the evolution of selfing, genetics of adaptation, and maintenance of variation within populations.

Mapping unexplored genomes II: genetic architecture of species differences in the woody Sonchus alliance (Asteraceae) in the Macaronesian Islands

“…Major QTL underlying plant species differences as implied by Gottlieb (1984) are consistent with several other QTL studies of pollination syndrome and some reproductive traits (Bradshaw et al 1995(Bradshaw et al , 1998Westerbergh and Doebley 2002;Bouck et al 2007) and yield and structural characteristics of domesticated crop species (Frary et al 2000;Liu et al 2002;van der Knaap and Tanksley 2003). In contrast, this study agrees with other findings that the majority of QTL had small to moderate effects (Lin and Ritland 1997;Fisherman et al 2002;Burke et al 2002;Rieseberg et al 2003;Lexer et al 2005). Those studies suggest that genetic architecture of species differences may vary greatly among taxa and traits.…”

The genic view of plant speciation: recent progress and emerging questions

“…An analysis of intraspecific divergence between annual and perennial Mimulus guttatus came to the same conclusion (Hall et al 2006). A comparison of the genetic architecture controlling floral trait divergence, both within divergent populations of M. guttatus and between M. guttatus and Mimulus nasutus ( Fishman et al 2002), implied that there may be a shared genetic basis for floral divergence within and among species of Mimulus (Hall et al 2006). …”

“…) provide strong support for the notion that major-effect genes are involved in premating reproductive isolation . In contrast to the genetic architecture of floral trait differences involved in pollinator attraction, QTL analyses of traits involved in interspecific mating system differences between inbreeding and outbreeding Mimulus species indicate that these trait differences (floral morphology and stigma-anther separation) are primarily controlled by loci with small effect (Lin & Ritland 1997;Fishman et al 2002). An analysis of intraspecific divergence between annual and perennial Mimulus guttatus came to the same conclusion (Hall et al 2006).…”

Natural variation for drought-response traits in the Mimulus guttatus species complex

“…Of the 12 populations included in the experiments, three [Oregon Dunes National Recreation Area, Oregon (DUN); Iron Mountain, Oregon (IM); and Sherar's Falls, Oregon (SF)] were well-characterized inbred lines that have been used extensively in other studies of adaptation to local environmental conditions (Fishman et al 2002;Hall and Willis 2006;Fishman and Willis 2008;Lowry et al 2009). For the remaining populations, three to Wve independent maternal families per population were included to encompass as much of the genetic variation within each population as possible, while allowing for replication within treatments in our experimental growth chamber.…”