Evolutionary genetics of plant adaptation: insights from new model systems

Abstract

Flowering time and mating system divergence are two of the most common adaptive transitions in plants. We review recent progress toward understanding the genetic basis of these adaptations in new model plant species. For flowering time, we find that individual crosses often reveal a simple genetic basis, but that the loci involved almost always vary within species and across environments, indicating a more complex genetic basis species-wide. Similarly, the transition to self-fertilization is often genetically complex, but this seems to depend on the amount of standing variation and time since species divergence. Recent population genomic studies also raise doubts about the long-term adaptive potential of self-fertilization, providing evidence that purifying selection is less effective in highly selfing species.

Figure 1

Variation in the genetic basis of flowering time behavior within and between Mimulus species. Major effect QTL for flowering time in Mimulus were identified in three QTL mapping studies performed in the greenhouse [15,19] or growth chambers [8••]. The map shows collection sites for parental lines used in mapping experiments (N_A2/G_A2 is a sympatric site). Crosses indicate annual M. guttatus (G_A), perennial M. guttatus (G_P), or annual M. nasutus (N_A), with numbers corresponding to distinct parental lines. Shading indicates flowering cue being tested: no shading = critical photoperiod, light grey = long-day flowering, and dark-grey = vernalization requirement under long days. Only two major effect QTL were identified in each population (colored arrows), indicating a simple genetic basis. QTL (linkage group: candidate genes) are listed on right. Notice that some QTL (LG7 and LG8b) are observed in multiple crosses, whereas all others vary with genotype and/or environment. Candidate genes: SUPPRESSOR OF PHYA 2 (SPA2), GIBBERELIC ACID REQUIRING 1 (GA1), GIBBERELLIC ACID REQUIRING 2 (GA2), FLOWERING LOCUS T (FT), GIBBERELLIC ACID INSENSITIVE (GAI), VERNALIZATION1 (VRN1), SHORT VEGETATIVE PHASE (SVP), FLOWERING LOCUS D (FLD), FLOWERINC LOCUS C (FLC), MADS-BOX AFFECTING (MAF). *The M. guttatus reference genome contains 8 full/partial copies of FT. ^‡Three paralogous copies of SVP underlie this QTL.

Figure 2

Recent speciation and the genomic consequences of mating system divergence in young species pairs of Mimulus and Capsella. (a) Speciation occurred recently and was associated with a transition to selfing and floral divergence in both species pairs ([32,33••,34], Brandvain et al., unpublished data). M. nasutus evolved from self-compatible, predominantly outcrossing M. guttatus, while C. rubella evolved from self-incompatible C. grandiflora. (b) M. guttatus, M. nasutus’ likely ancestor, contains more than twice the level of synonymous nucleotide diversity than C. grandiflora, the progenitor of C. rubella (Brandvain et al., unpublished data, [33••]). Levels of nucleotide divergence are similar to nucleotide diversity within the outcrossing species in both species pairs. (c) The evolution of selfing in Mimulus and Capsella resulted in proportional reductions in genomic variation and increases in putatively deleterious variation (Brandvain et al., unpublished data, [33••]), as well as extreme reductions in effective recombination (Brandvain et al., unpublished data, [32]). The upper and lower arrows represent genomic changes in the highly selfing M. nasutus relative to M. guttatus, and the highly selfing C. rubella relative to C. grandiflora, respectively. Because the median intra-locus recombination estimate was zero in C. rubella, the ratio of effective recombination was calculated using the median in C. grandiflora (0.131) and the mean in C. rubella (0.0038); the ratio is >65× if calculated using the mean in C. grandiflora (0.26). Photo credits: Mimulus: Andrea L. Sweigart. Capsella: Young Wha Lee and Gavin Douglas.