Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris

Abstract

Plant species may remain morphologically distinct despite gene exchange with congeners, yet little is known about the genomewide pattern of introgression among species. Here we analyze the effects of persistent gene flow on genomic differentiation between the sympatric sunflower species Helianthus annuus and H. petiolaris. While the species are strongly isolated in testcrosses, genetic distances at 108 microsatellite loci and 14 sequenced genes are highly variable and much lower (on average) than for more closely related but historically allopatric congeners. Our analyses failed to detect a positive association between levels of genetic differentiation and chromosomal rearrangements (as reported in a prior publication) or proximity to QTL for morphological differences or hybrid sterility. However, a significant increase in differentiation was observed for markers within 5 cM of chromosomal breakpoints. Together, these results suggest that islands of differentiation between these two species are small, except in areas of low recombination. Furthermore, only microsatellites associated with ESTs were identified as outlier loci in tests for selection, which might indicate that the ESTs themselves are the targets of selection rather than linked genes (or that coding regions are not randomly distributed). In general, these results indicate that even strong and genetically complex reproductive barriers cannot prevent widespread introgression.

Figure 1.—

The likely prehistoric distribution of three Helianthus species. Note that recently colonized areas are readily diagnosed because sunflowers are restricted to human-disturbed sites. Collections of H. annuus are indicated by squares and H. petiolaris by circles. Collections of H. argophyllus are not shown because the symbols would obscure its entire range.

Figure 2.—

Phylogenetic tree for Helianthus section Helianthus based on restriction site analyses of chloroplast DNA and nuclear ribosomal genes (redrawn from Rieseberg 1991). Three homoploid hybrid sunflower species are excluded from this tree so that information on geographical relationships of the focal taxa can be provided.

Figure 3.—

The distribution of interspecific G′_ST values in sympatric and allopatric pairs of sunflower species.

Figure 4.—

Autocorrelation of interspecific G′_ST values as a function of genetic distance along linkage groups (in centimorgans).

Figure 5.—

Distribution of interspecific F_ST values as a function of heterozygosity (H). The envelope of values corresponding to neutral expectations (with F_ST = 0.078) under a stepwise mutation model was constructed according to Beaumont and Nichols (1996) (see Table 5).

Figure 6.—

Distributions of F_ST and G′_ST of anonymous microsatellites (open circles and open bars) and EST-associated microsatellites (solid diamonds and solid bars). An asterisk indicates loci identified as outliers in the test of Beaumont and Nichols (1996) (see Table 5).