Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse

Abstract

The extent to which epistasis contributes to adaptation, population differentiation, and speciation is a long-standing and important problem in evolutionary genetics. Using recombinant inbred (RI) lines of Arabidopsis thaliana grown under natural field conditions, we have examined the genetic architecture of fitness-correlated traits with respect to epistasis; we identified both single-locus additive and two-locus epistatic QTL for natural variation in fruit number, germination, and seed length and width. For fruit number, we found seven significant epistatic interactions, but only two additive QTL. For seed germination, length, and width, there were from two to four additive QTL and from five to eight epistatic interactions. The epistatic interactions were both positive and negative. In each case, the magnitude of the epistatic effects was roughly double that of the effects of the additive QTL, varying from -41% to +29% for fruit number and from -5% to +4% for seed germination, length, and width. A number of the QTL that we describe participate in more than one epistatic interaction, and some loci identified as additive also may participate in an epistatic interaction; the genetic architecture for fitness traits may be a network of additive and epistatic effects. We compared the map positions of the additive and epistatic QTL for germination, seed width, and seed length from plants grown in both the field and the greenhouse. While the total number of significant additive and epistatic QTL was similar under the two growth conditions, the map locations were largely different. We found a small number of significant epistatic QTL x environment effects when we tested directly for them. Our results support the idea that epistatic interactions are an important part of natural genetic variation and reinforce the need for caution in comparing results from greenhouse-grown and field-grown plants.

Figure 1.

Comparison of field and greenhouse QTL LOD scores. This displays the output of WinQTLCartographer (Wang et al. 2004) composite interval mapping as QTL LOD score vs. genetic map position for the traits that were measured from lines grown in both field and greenhouse environments. (Top) Seed germination; (middle) seed length; (bottom) seed width. Field growth is a solid line, while greenhouse growth is a dashed line. Horizontal lines represent the significance levels established by permutations.

Figure 2.

Epistatic QTL for fitness traits in field-grown Arabidopsis. The programs Epistat and Epistacy were used to estimate the probabilities of interactions between map segments for these quantitative traits; the results from the two programs were combined in each scatter plot. The axes indicate the genetic map of A. thaliana with one chromosome following another so that the total is displayed linearly. The x- and y-axes correspond to marker X and marker Y in Table 2. The plotted squares indicate the P-value for an interaction between the map segments: = 0.001, = 0.003, = 0.005, = 0.007. Note that because of the correction for multiple comparisons, these values correspond to a 10-fold-higher statistical significance probability. The data in Table 2 contain the P = 0.001 subset of this graph.

Figure 3.

Network of additive and epistatic QTL for fruit number, germination, seed length, and width in field-grown A. thaliana. “A” indicates additive QTL from Table 1. Shaded lines labeled with “E” connect the epistatic interactions. For the epistatic interactions, the locations and cluster number shown are those from Tables 2 and 3.

Figure 3.

Network of additive and epistatic QTL for fruit number, germination, seed length, and width in field-grown A. thaliana. “A” indicates additive QTL from Table 1. Shaded lines labeled with “E” connect the epistatic interactions. For the epistatic interactions, the locations and cluster number shown are those from Tables 2 and 3.

Figure 3.

Network of additive and epistatic QTL for fruit number, germination, seed length, and width in field-grown A. thaliana. “A” indicates additive QTL from Table 1. Shaded lines labeled with “E” connect the epistatic interactions. For the epistatic interactions, the locations and cluster number shown are those from Tables 2 and 3.

Figure 3.

Network of additive and epistatic QTL for fruit number, germination, seed length, and width in field-grown A. thaliana. “A” indicates additive QTL from Table 1. Shaded lines labeled with “E” connect the epistatic interactions. For the epistatic interactions, the locations and cluster number shown are those from Tables 2 and 3.

Figure 4.

Epistatic QTL compared from greenhouse- and field-grown A. thaliana. The programs Epistat and Epistacy were used to estimate the probabilities of interactions between map segments for these quantitative traits; the results from the two programs were combined in each scatter plot. The axes indicate the genetic map of A. thaliana with one chromosome following another so that the total is displayed linearly. The x- and y-axes correspond to marker X and marker Y in Table 3. The plotted squares indicate the P-value for an interaction between the map segments: = 0.001, = 0.003, = 0.005, = 0.007. Note that because of the correction for multiple comparisons these values correspond to a 10-fold-higher statistical significance probability.