The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy

Abstract

Colonizing species may often encounter strong selection during the initial stages of adaptation to novel environments. Such selection is particularly likely to act on traits expressed early in development since early survival is necessary for the expression of adaptive phenotypes later in life. Genetic studies of fitness under field conditions, however, seldom include the earliest developmental stages. Using a new set of recombinant inbred lines, we present a study of the genetic basis of fitness variation in Arabidopsis thaliana in which genotypes, environments, and geographic location were manipulated to study total lifetime fitness, beginning with the seed stage. Large-effect quantitative trait loci (QTLs) for fitness changed allele frequency and closely approached 90% in some treatments within a single generation. These QTLs colocated with QTLs for germination phenology when seeds were dispersed following a schedule of a typical winter annual, and they were detected in two geographic locations at different latitudes. Epistatically interacting loci affected both fitness and germination in many cases. QTLs for field germination phenology colocated with known QTLs for primary dormancy induction as assessed in laboratory tests, including the candidate genes DOG1 and DOG6. Therefore fitness, germination phenology, and primary dormancy are genetically associated at the level of specific chromosomal regions and candidate loci. Genes associated with the ability to arrest development at early life stages and assess environmental conditions are thereby likely targets of intense natural selection early in the colonization process.

Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

“…The phenomenon that the maternal environment during seed development and maturation determines the germination phenology of Arabidopsis and other species is well-established knowledge (Kugler, 1951;Gutterman, 1980Gutterman, /1981Munir et al, 2001). However, as a major advance, we now know from ecological work with Arabidopsis (Huang et al, 2010;Moyers and Kane, 2010;Chiang et al, 2011;Barua et al, 2012;Kronholm et al, 2012) that natural genetic variation at the DOG1 locus is a major determinant for the local adaptation to novel environments, and we also know that the maternal environment controls DOG1 gene expression during seed maturation. For example, low temperature during seed maturation causes increased DOG1 gene expression and deeper primary dormancy of mature seeds (Chiang et al, 2011;Kendall et al, 2011;Nakabayashi et al, 2012).…”

“…Several recent publications clearly demonstrate that in Arabidopsis, QTLs with large effects on fitness colocalize with QTLs for field germination timing and seed dormancy (Huang et al, 2010;Moyers and Kane, 2010;Chiang et al, 2011;Barua et al, 2012;Kronholm et al, 2012). Germination phenology is under intense, geographically variable, natural selection in Arabidopsis, since it is the major determinant of fitness during the earliest stages of colonization (Huang et al, 2010;Moyers and Kane, 2010;Chiang et al, 2011;Barua et al, 2012;Kronholm et al, 2012). It is also evident that QTLs including DOG1 determine the phenotypic plasticity of seed germination/dormancy responses already on the mother plant in interaction with environmental factors such as seed maturation photoperiod and temperature.…”

“…For seed dormancy, analysis of Arabidopsis natural genetic variation has led to the cloning of AtDOG1 as the first specific seed dormancy gene (Bentsink et al, 2006) and has been shown to be important for local adaptation to different environments (Huang et al, 2010;Chiang et al, 2011;Footitt et al, 2011;Kendall et al, 2011;Kronholm et al, 2012). Homologs of the AtDOG1 gene are also known for the Brassicaceae species B. rapa (BrDOG1) and Lepidium sativum (Lesa-DOG1; Graeber et al, 2010).…”

The Time Required for Dormancy Release in Arabidopsis Is Determined by DELAY OF GERMINATION1 Protein Levels in Freshly Harvested Seeds

“…Natural Arabidopsis accessions show considerable differences in seed dormancy, which can for an important part be explained by a quantitative trait locus located at the DOG1 gene, both in laboratory (Bentsink et al, 2010) and field experiments (Huang et al, 2010). In addition, it was shown that differences in DOG1 expression between Arabidopsis accessions contribute to geographical variation in dormancy and germination (Chiang et al, 2011).…”

Genetic and physiological bases for phenological responses to current and predicted climates

“…Selection experiments under contrasting CO 2 or simulated seasonal conditions have identified distinct genetic responses in Arabidopsis that account for evolutionary changes in flowering time depending on the selection environment (Springer et al 2008;Scarcelli & Kover 2009). The fitness consequences of dormancy characteristics differ between seeds dispersed in autumn and those in spring, and seasonal QTL involved in dormancy response and fitness can also be identified (Donohue et al 2005;Huang et al 2010). Thus, knowledge at the genetic level of the basis of phenological traits, the amount of natural variation in these traits, the effect of season on expression of these traits and their fitness consequences in seasonal environments will be necessary to achieve more accurate predictions of the integrated life-history responses of plants to novel environments.…”