Metapopulation structure and fine-scaled genetic structuring in crop-wild hybrid weed beets

Abstract

This study explores the microspatial and temporal genetic variation in crop-wild hybrid weed beets that emerged from the seed bank in a cultivated field surveyed over two successive years. We demonstrate the occurrence of demes highly genetically differentiated, kin-structured, characterized by moderate effective population sizes, differing in propensity for selfing, and arising from nonrandom genetic subsets of the seed bank. Only one deme identified in the first survey year significantly contributed to the weed beets that emerged in the second year. Spatial structuring appears to be primarily due to gravity seed dispersal and limited pollen flow among weed beet demes. Within each genetic cluster identified by Bayesian assignments and multivariate analyses, F(IS) estimates and level of biparental inbreeding--revealed by progeny analyses--dropped to non-significant values. This suggests that random mating occurs at the scale of genetically distinct demes over a very short scale. Our results highlight the need to carefully depict genetic discontinuities in weed species, when attempting to describe their local genetic neighborhoods within which genetic drift and selective processes occur.

Figure 1

Spatial distribution of weed beets sampled in two successive years. Weed beets sampled in 2003 and 2004 are visualized by white circles and gray circles, respectively. Five geographical distinct clusters of weed beets occurred in 2003 and were labeled from 1 to 5.

Figure 2

Bayesian assignment results from the non-spatial clustering algorithm described in Hubisz et al. (2009) and applied on the whole data set comprising the two temporal samples. (a) Mean (±s.d.) probabilities of the data Ln Pr(X∣K) over 10 replicated runs plotted as a function of the putative number of clusters K (gray square) and the standardized second-order rate of change of Ln Pr(X∣K), ΔK, as a function of K (black circle). (b) Bayesian assignment probabilities of membership for the whole data set of weed beets sampled in 2003 and 2004 into the three inferred clusters. Each individual is represented by a thin horizontal line (y axis) partitioned into three colored segments that represented the individual's estimated membership fractions depicted in K=3 clusters (x axis); black: cluster 1, dark gray: cluster 2; light gray: cluster 3.

Figure 3

Typology of weed beets and representation of genetic relatedness between geographical clusters of weed beets obtained by discriminant analysis of principal components (DAPC). Scatterplots show the first two principal components (a) and the first and third principal components (b) of the DAPC of weed beets genotypes. Eigenvalues corresponding to the represented components are filled in black. Points represent genotypes and geographical groups of weed beets are labeled inside their 95% inertia ellipse. Labels from 1 to 5: weed beets sampled in 2003; label numbered 6: weed beets sampled in 2004.

Figure 4

Two-dimensional Mantel correlogram summarizing the spatial genetic variation among weed beets that emerged from the seed bank the second survey year (2004). This windrose correlogram is on the basis of comparison of pairwise genetic distances against geographical distances between individuals. The seven circular and successive annuli represent interval distance classes with upper limits of 4, 7, 12, 19, 28, 39 and 52 m, respectively. Full-width boxes correspond to significant r_z values at P<0.05 after 10 000 permutations, whereas half-width boxes represent nonsignificant correlation coefficients. Boxes with dashed outlines are distance–direction classes with insufficient number of pairwise comparisons (<20) to ensure relevant r_z estimates. Shading represents the range of values covered by the normalized Mantel statistic r_z.

Figure 5

Graphical representation of siring event proportions mediated through pollen dispersal within and among the three genetic clusters of weed beets inferred by Bayesian assignments. Arrows indicate the proportion and the orientation of pollen flow events. Pollen flow proportions involving a mother plant sired by pollen donors located outside the studied sugar beet field are equal to 0.14, 0.07 and 0.09 for clusters 1, 2 and 3, respectively. These pollen donors are weed beets located in nearby fields surveyed by Fénart et al. (2007).