Academic journal article Genetics

Pleiotropic Quantitative Trait Loci Contribute to Population Divergence in Traits Associated with Life-History Variation in Mimulus Guttatus

Academic journal article Genetics

Pleiotropic Quantitative Trait Loci Contribute to Population Divergence in Traits Associated with Life-History Variation in Mimulus Guttatus

Article excerpt

ABSTRACT

Evolutionary biologists seek to understand the genetic basis for multivariate phenotypic divergence. We constructed an F^sub 2^ mapping population (N = 539) between two distinct populations of Mimulus guttatus. We measured 20 floral, vegetative, and life-history characters on parents and F^sub 1^ and F^sub 2^ hybrids in a common garden experiment. We employed multitrait composite interval mapping to determine the number, effect, and degree of pleiotropy in quantitative trait loci (QTL) affecting divergence in floral, vegetative, and lifehistory characters. We detected 16 QTL affecting floral traits; 7 affecting vegetative traits; and 5 affecting selected floral, vegetative, and life-history traits. Floral and vegetative traits are clearly polygenic. We detected a few major QTL, with all remaining QTL of small effect. Most detected QTL are pleiotropic, implying that the evolutionary shift between these annual and perennial populations is constrained. We also compared the genetic architecture controlling floral trait divergence both within (our intraspecific study) and between species, on the basis of a previously published analysis of M. guttatus and M. nasutus. Eleven of our 16 floral QTL map to approximately the same location in the interspecific map based on shared, collinear markers, implying that there may be a shared genetic basis for floral divergence within and among species of Mimulus.

EVOLUTIONARY biologists have long sought to understand the genetic basis for adaptive divergence between populations with complex multivariate phenotypes. Adaptation to a novel environment may involve evolutionary change of multiple genetically correlated traits as the population approaches a new phenotypic optimum (FiSHER 1930; ORR 2000). If variation in individual traits is governed largely by trait-specific loci, the selected traits may be able to evolve independently (unless they are constrained by linkage disequilibrium), whereas those that are governed by pleiotropic loci are going to be evolutionarily constrained. The degree of pleiotropy can have profound effects on the evolutionary trajectory of particular traits (LANDE 1979) and therefore on the nature of divergence of multiple traits between populations.

An understanding of the degree of pleiotropy affecting multiple traits sheds light on one of the classic debates in evolutionary biology-whether phenotypic divergence is the result of fixation of one or two mutations of large effect or due to many mutations of small effect. Each of these two options could have different effects on the nature of evolutionary divergence. One of the earliest views of the genetic basis of adaptation was that phenotypic divergence was extremely gradual, consisting of many genes, each having an infinitesimally small effect on the trait (FiSHER 1930). This view of adaptation had widespread support among early empiricists (DOBZHANSKY 1937; HUXLEY 1942; MULLER 1949), although it was later challenged in favor of the alternate view that adaptations were largely the result of substitutions of single genes with large effects (GouLD 1980; GOTTLIEB 1984; TURNER 1985). The debate continued (CoYNE and LANDE 1985; ORR and COYNE 1992) until more recent evidence based on quantitative trait locus (QTL) mapping analyses allowed more rigorous testing of this hypothesis. To date, genetic mapping studies have provided support for both possibilities, some where few large-effect QTL underlie divergence (UOEBLEY and STEC 1991; BRADSHAW et al. 1995,1998; SUCENA and STERN 2000; COLOSIMO et al. 2004). Other studies have demonstrated that divergence can result from many QTL of small effect (Liu et al. 1996; LAURIE et al. 1997; ZENG et al. 2000; FISHMAN et al. 2002). However, these patterns are generally interpreted with respect to individual traits rather than accounting for correlations among traits. For example, consider a pair of populations divergent for two traits, and the difference in each trait is controlled by 5 QTL. …

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