Changing patterns of genetic differentiation in the slender wild oat, Avena barbata

Abstract

The slender wild oat (Avena barbata) was widely studied in California using allozymes in the 1970s and interpreted as a case of ecotypic adaptation to contrasting moisture environments. However, common garden studies suggested that the moist-associated ("mesic") ecotype had high fitness in both moist and dry habitats, thus predicting an adaptive spread into areas occupied by the dry associated ("xeric") ecotype. To test this prediction, we revisited 100 populations of A. barbata that were screened genetically 40 y ago. As expected, mesic allozyme and morphological markers are much more common than in the 1970s. The less-fit xeric ecotype, while still widespread, has declined markedly in range and frequency. Genotyping by sequencing of modern populations reveals striking genetic uniformity within each of the two ecotypes. In recombinants between the two ecotypes, the mesic allele at a major fitness quantitative trait locus (QTL) shows a high frequency but so do many other genomic regions not identified as fitness QTL. Additional introduced genotypes are diverse and more widespread than in the past, and our results show that these have spread into the former range of the xeric ecotype to an even greater extent than the mesic ecotype has. While these results confirm the prediction of contemporary evolution from common gardens, they also suggest that much of the change has been driven by additional waves of introduced genotypes.

Keywords: adaptation; admixture; colonization history; contemporary evolution.

Fig. 1.

Change in frequency of the mesic morphological markers (pubescent stems and light lemmas) in Avena barbata at 100 sites in California between the 1970s and 2010. Graphs depict the latitudinal cline in morph frequencies modeled using GLMM. Black lines represent the model estimate, while gray lines depict the uncertainty around the model (from 1,000 random samples from the error distribution of model parameters). Symbols plot the frequency of the morphs at each site. Statistical significance of the model in Table 1.

Fig. 2.

Tileplot depicting genotype calls at 12,415 GBS loci across 212 accessions of A. barbata collected in California in 2010. At 7,530 mapped loci, homozygotes are classified as matching the Xeric or Mesic genotypes, or belonging to a Northern genotype (allele not present in either mesic or xeric). At 4,885 loci, the same allele (Southern) was present in both mesic and xeric and thus did not segregate in the mapping population (41). Heterozygotes are shown in gray. Also shown is the cpDNA chloroplast of each accession (35). Finally, the results of Structure analysis (44) are presented estimating the proportion of each accession’s genome that derives from the mesic and xeric ecotypes or the “northern” group of genotypes. A high resolution copy of the image is presented in SI Appendix Fig. S1.

Fig. 3.

Locations where at least one individual was sampled that could be classified as xeric ecotypes (orange), mesic ecotypes (blue), recombinants between mesic and xeric (green), or which contain genetic material from the “northern” group of genotypes (purple). Individuals are classified based on allozyme data (43, 45, 46) in the 1970s and based upon GBS results (Fig. 2) in 2010. We classified individuals as recombinant if they contain a mixture of the alleles present in the mesic and xeric genotypes. Any individuals with “third” alleles (i.e., alleles not present in either mesic or xeric) were classified as “northern.” For GBS data, we set a minimum of 10% third alleles to be considered northern.

Fig. 4.

Intrapopulation genetic variation of GBS markers in four populations of A. barbata. The proportion of each individual’s genome that derives from the mesic, xeric, or northern genotypes is indicated by the stacked bar chart (redrawn from the output of Structure). Fiddletown (monomorphic for the xeric ecotype in 1970 (43)) was sampled widely over a contiguous area, while the other populations were sampled along transects from low elevation to high (Lick Observatory and Calistoga) and east to west (Geyserville).

Fig. 5.

Frequencies of mesic (blue) and xeric (orange) alleles across the genome in recombinants between mesic and xeric ecotypes in California in 2010. Only those recombinants that contained <10% northern genotype (from Structure; Figs. 3 and 4) were included in our calculation of the frequencies. The location of two fitness QTL (37) is indicated by bars above the graph.