Recent Speciation of Capsella Rubella from Capsella Grandiflora, Associated with Loss of Self-Incompatibility and an Extreme Bottleneck

Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck Ya-Long Guoa,1, Jesper S. Bechsgaardb,1, Tanja Slottec, Barbara Neufferd, Martin Lascouxc, Detlef Weigela,2, and Mikkel H. Schierupb,2 aDepartment of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tu¨bingen, Germany; bEcology and Genetics, Institute of Biological Sciences, University of Aarhus, 8000 Aarhus C, Denmark; cProgram in Evolutionary Functional Genomics, Uppsala University, 75326 Uppsala, Sweden; and dDepartment of Systematic Botany, University of Osnabru¨ck, 49076 Osnabru¨ck, Germany Edited by Spencer C. H. Barrett, University of Toronto, Toronto, Canada, and accepted by the Editorial Board January 26, 2009 (received for review August 13, 2008) Flowering plants often prevent selfing through mechanisms of thaliana, the work horse for much of plant molecular genetics, self-incompatibility (S.I.). The loss of S.I. has occurred many times has become self-compatible relatively recently, apparently by the independently, because it provides short-term advantages in sit- gradual fixation of multiple, independent mutations that weak- uations where pollinators or mates are rare. The genus Capsella, ened or disabled the S.I. system throughout its geographical which is closely related to Arabidopsis, contains a pair of closely range (15, 16). related diploid species, the self-incompatible Capsella grandiflora We set out to investigate the breakdown of S.I. in Capsella and the self-compatible Capsella rubella. To elucidate the transi- rubella to test the generality of the pattern described for A. tion to selfing and its relationship to speciation of C. rubella,we thaliana. The genus Capsella includes the 2 diploid species C. have made use of comparative sequence information. Our analyses rubella and Capsella grandiflora (2n ϭ 16) and the tetraploid indicate that C. rubella separated from C. grandiflora recently species C. bursa-pastoris (2n ϭ 32) (17, 18). The 2 diploid species Ϸ ( 30,000–50,000 years ago) and that breakdown of S.I. occurred at show striking morphological differences, particularly for flower EVOLUTION approximately the same time. Contrasting the nucleotide diversity size. That they are also genetically diverged can be concluded patterns of the 2 species, we found that C. rubella has only 1 or 2 from the observation that even when experimental crosses do alleles at most loci, suggesting that it originated through an not fail completely, F1 hybrids are often sterile (17). The extreme population bottleneck. Our data are consistent with self-incompatible C. grandiflora has the narrowest distribution diploid speciation by a single, selfing individual, most likely living and is found in western Greece, some of the Greek islands, in Greece. The new species subsequently colonized the Mediter- Albania and, rarely, in northern Italy. The self-compatible C. ranean by Northern and Southern routes, at a time that also saw rubella occurs throughout the Mediterranean, and has occasion- the spread of agriculture. The presence of phenotypic diversity ally followed European settlers to the Americas and to Australia. within modern C. rubella suggests that this species will be an By far the most successful species is the self-compatible C. interesting model to understand divergence and adaptation, start- bursa-pastoris, an invasive weed with an impressive ecological ing from very limited standing genetic variation. range that is found throughout the world (17, 19–21). Selfers are often better pioneers, because the ability to self-fertilize allows any flowering plant species are obligate outcrossers that the establishment of new populations by individual plants (6–9, Mcannot self-fertilize because of self-incompatibility (S.I.), 22, 23). The potential to spread and become a cosmopolitan often determined by a single S-locus (1–3). Differences in the species therefore often appears higher for selfers than outcross- underlying mechanisms indicate that S.I. has evolved indepen- ers. In accordance with this, C. rubella, like its selfing congener dently at least 10 times. However, loss of S.I. is even more C. bursa-pastoris, has a larger distribution range than the out- common, and is thought to be most prevalent when mating crossing C. grandiflora. opportunities are limited because of low population densities or The S-locus of C. grandiflora is very polymorphic because of absence of pollinators, situations most likely to occur at the edges strong frequency dependent selection, and comprises at least 38 of a species’ range or on islands (3–9). Loss of obligatory haplotypes (24, 25), which is very similar to what has been outcrossing in flowering plants is often associated with subse- reported for A. lyrata (26). The origin of C. rubella might have quent appearance of differences in a variety of reproductive been associated with the breakdown of S.I. in a C. grandiflora traits, such as flowering time and floral morphology (10). These, population. An obvious candidate for sustaining the causative together with chromosomal rearrangements, reduce gene flow between populations with different mating systems, and may eventually lead to reproductive isolation and speciation (11). Author contributions: Y.-L.G., J.S.B., M.L., D.W., and M.H.S. designed research; Y.-L.G., Therefore, the relationship between the loss of S.I. and specia- J.S.B., and T.S. performed research; T.S. and B.N. contributed new reagents/analytic tools; Y.-L.G., J.S.B., D.W., and M.H.S. analyzed data; and Y.-L.G., J.S.B., D.W., and M.H.S. wrote tion is of particular interest. the paper. In the Brassicaceae, sporophytic S.I. is the ancestral condition. The authors declare no conflict of interest. The self-incompatibility (S)-locus in this family consists of 2 This article is a PNAS Direct Submission. S.C.H.B. is a guest editor invited by the Editorial determinant genes, SRK and SCR, which are normally not Board. separated by recombination. The transmembrane receptor ki- Freely available online through the PNAS open access option. nase encoded by SRK is expressed at the stigmatic surface of the Data deposition: The sequences reported in this paper have been deposited in the GenBank female, whereas the small soluble SCR ligand is deposited in the database (accession nos. FJ649697–FJ650362). pollen wall of the male. When SCR binds to SRK from the same 1Y.-L.G. and J.S.B. contributed equally to this work. haplotype, the S.I. response is initiated, preventing self- 2To whom correspondence may be addressed. E-mail: [email protected] or pollination through a series of downstream events (reviewed in [email protected]. ref. 12, 13). S.I. has been lost repeatedly within the Brassicaceae, This article contains supporting information online at www.pnas.org/cgi/content/full/ even within the same genus and/or species (13, 14). Arabidopsis 0808012106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0808012106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 26, 2021 0.42 At4g25100 At4g21150 Capsella rubella Capsella grandiflora 0.41 π 0.40 0.03 FRI PHYC 0.02 Nucleotide diversity ( ) 0.01 0.00 -1496-990 -504 -100 -30 -10 0 2 21 89 554 1013 1510 ADH FLC FRI PHYC Distance from SRK (kb) Unlinked Fig. 1. Nucleotide diversity in C. rubella and C. grandiflora. Distance from PI SRK is for the syntenic region from A. thaliana, because exact information is only available for C. rubella from close to SRK (see Table S2). Distance is not to scale. Note the break in the ordinate, to accommodate the nucleotide diversity value for SRK from C. grandiflora. mutation is the S-locus itself. However, although the S-locus has been implicated in the breakdown of S.I. in A. thaliana (15, 16, Fig. 2. C. rubella loci with 2 divergent haplotypes. Each allele is shown as a 27), whether it is any more likely to play a central role in the loss horizontal line. C. rubella alleles (black) have been sorted by similarity, with the of S.I. than other genes that are required for SRK/SCR activity 2 closest C. grandiflora alleles (red) shown above and below the C. rubella alleles. is unknown. In fact, A. thaliana has been shown to harbor Polymorphisms are shown as vertical lines. Most polymorphisms in C. rubella are variation for a gene that is closely linked to the S-locus and that also found in C. grandiflora. Although for PI only C. rubella sequences (18) were can modify expression of SRK (28). available, these also seem to fall into 2 dominant haplotypes. Here, we present data suggesting that breakdown of S.I. was associated with the origin of C. rubella Ϸ30,000–50,000 years of C. grandiflora [(average divergence is 0.0043; net divergence ago. S-locus diversity is compatible with a selective sweep, but 0.0017 (6 differences in 3496 base pairs)], suggesting a common diversity at other loci is also very low, indicating that the origin from the same functional haplotype in the ancestral transition to self-compatibility has been through an extreme species. For SCR, only the first of 2 exons are found in C. rubella, bottleneck. Because all loci we have examined have only 1 or 2 haplotypes in C. rubella, we hypothesize that this species has been and the sequences of different accessions are nearly identical (2 founded by a single C. grandiflora individual that had become segregating sites in 805 base pairs, see Table S3). The C. self-compatible. Our data furthermore indicate that breakdown grandiflora SCR sequence overlap with C. rubella sequences by 224 bp only, with only a single bp difference. of S.I. occurred near Greece, and spread with agriculture to the ␲ rest of Europe. Although nucleotide diversity ( )inC.

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