Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. × divaricarpa, and A. holboellii (Brassicaceae)

Abstract

Arabis drummondii, A. holboellii and their hybrid A. x divaricarpa are widespread perennials of open habitats in North America. A phylogenetic analysis based on noncoding chloroplast DNA sequences (trnL intron and trnL/F intergenic spacer) resolved A. drummondii as a monophyletic taxon, but found A. holboellii to bear chloroplast haplotypes from highly diverged evolutionary lineages. This raised the question of a possible polyphyletic origin of A. holboellii. Arabis x divaricarpa was found to be of recent and polytopic origin, a result consistent with its presumed hybrid origin. One hundred and three chloroplast haplotypes were detected within 719 Arabis accessions investigated. The majority of chloroplast-types were estimated to have arisen prior to the Wisconsin glaciation. Phylogeographical analysis using nested clade analysis, suggested for A. holboellii (i). past fragmentation events, partitioning genetic variation in several instances between the Sierra Nevada, the Southern Rocky Mountains and the Colorado Plateau on the one hand and the Central to Northern Rockies of the United States and adjacent Cascades on the other; and for both parental species (ii). recolonization of major areas formerly covered by the Wisconsin glaciation by three haplotypes; and (iii). restricted gene flow indicating isolation by distance in areas south of the last glacial maximum. Arabis x divaricarpa is closely codistributed with its parental species and resampled their haplotypes. The highest genetic diversity was found in the Rocky Mountains from Idaho and Montana south to Utah and Colorado. This area was further hypothesized to have played a major role in the origin of both parental species and probably represented an important glacial refugium. However, evidence for glacial refugia was also found in arctic and boreal regions of Alaska and near the Great Lakes. In comparison to nuclear ribosomal internal transcribed spacer data, chloroplast DNA divergence was very high and evidently predated the origin of A. drummondii and possibly A. holboellii. Divergence of major chloroplast lineages dates back to the middle of the Pleistocene at least. Extensive hybridization is the most likely evolutionary factor working on A. holboellii to explain the revealed discrepancy in nuclear DNA and chloroplast DNA diversification.

Hybrid apomicts trapped in the ecological niches of their sexual ancestors

“…Individuals carrying the oldest cpDNA haplotypes AA, AB, and AC, which are represented by suprahaplotype S8 (∼0.7-2 million y) (44) (Fig. 2), had either none, both, or one of the apomixis-related APOLLO and UPGRADE2 alleles.…”

“…S3, and Tables S3 and S4). Widespread hybridization (44,48) reflects similar apomixis frequencies across the major cpDNA-haplotype lineages (lineage I = 54.26%, lineage II = 47.74%, and lineage III = 50.64% apomixis) (Figs. 1B and 2 and Tables S2 and S4), corroborates previous findings of high genotypic diversity in other agamic complexes (e.g., T. officinale) (52), and is furthermore supported by a computational study (53).…”

Multilocus Patterns of Nucleotide Diversity, Population Structure and Linkage Disequilibrium inBoechera stricta, a Wild Relative of Arabidopsis

“…Boechera is a widespread North American group with great potential for studies of ecology and evolution, occurring in diverse habitats, with a range of mating systems, as well as highly variable phenotypes (Mitchell-Olds 2001). B. stricta (previously Arabis drummondii) is a morphologically and genetically well-defined, monophyletic, short-lived perennial crucifer species (Dobes et al 2004). Genetic and molecular analyses indicate that B. stricta is predominantly diploid, sexual, and inbreeding (F IS ¼ 0.9 and F IT ¼ 0.95) (Schranz et al 2005;Song et al 2006).…”

Comparative Genetic Mapping inBoechera stricta, a Close Relative of Arabidopsis

“…Numerous studies have analyzed molecular and phenotypic diversity of Boechera species. This includes the molecular evolutionary analysis of gene families (Bishop et al, 2000;Schein et al, 2004;Benderoth et al, 2006), the phylogeography of haplotypes (Dobeš et al, 2004b;Song et al, 2006), the occurrence of supernumary B chromosomes (Böcher, 1951;Sharbel et al, 2004), variation in breeding systems and ploidy (Sharbel and MitchellOlds, 2001;Schranz et al, 2005;Schranz et al, 2006a), drought tolerance (Knight et al, 2006), morphological and taxonomical diversity (Rollins, 1993;Al-Shehbaz, 2003;Windham and Al-Shehbaz, 2006), and the evolved responses to pathogen or insect pests (Roy, 1993;Roy and Kirchner, 2000;Jones et al, 2006). The further elucidation of these and other patterns of variation would be greatly aided by the creation and analysis of segregating genetic stocks.…”

“…Genetic and molecular analyses indicate that B. stricta is predominantly inbreeding, diploid, and sexual and most accessions form a monophyletic group (referred to as lineage II in Dobeš et al, 2004b;Schranz et al, 2005), whereas many other species in the genus are apomictic, of hybrid origin, and/or triploid (Sharbel and Figure 1. Relationships, number of species, and base-chromosome numbers for the eight tribes of lineage I of the Brassicaceae.…”