Species–level phylogeny of Allium subgenus Melanocrommyum: Incomplete lineage sorting, hybridization and trnF gene duplication

Abstract

Noncoding chloroplast DNA sequences are widely employed markers in plant species-level phylogenetics and phylogeography. However, chloroplast capture (hybridization) and incomplete sorting of ancestral lineages could confound phylogenetic inference using chloroplast DNA. Recently, we studied the phylogeny of Allium subg. Melanocrommyum based on nuclear rDNA internal transcribed spacer (ITS) sequences and showed that, although the subgenus is monophyletic, most sections are either para-or polyphyletic. To get insights from the chloroplast genome we sequenced the plastid trnL-trnF region in 434 individuals representing 100 species of A. subg. Melanocrommyum and found 74 chloroplast haplotypes. The sequences were analyzed using tree-based (Bayesian and maximum parsimony) and network-based (statistical parsimony network) approaches. The analyses revealed high level of chloroplast haplotype sharing among up to 15 species, as well as presence of several closely related haplotypes within single species. Several characteristics of the data violate the main assumptions of standard tree building methods that is the persistence of ancestral haplotypes and their co-existence with descendant alleles as well as multifurcating relationships among these alleles. The taxon groups inferred from chloroplast trnL-trnF sequence analyses were congruent with the nuclear phylogeny. Thus, bi-and uniparentally inherited datasets strongly contradict the morphology-based taxonomic classification of A. subg. Melanocrommyum. Also, the present study (1) reports a trnF gene duplication in A. subg. Melanocrommyum, (2) infers few putative homoploid hybrid taxa, and (3) shows that natural interspecies hybrids occur rarely in the subgenus. Generally, our data strongly advocate including multiple accessions per species in species-level phylogenetic studies, and show the advantages of networks over tree building methods for analyzing sequences from noncoding chloroplast loci in closely related species.

Chloroplast capture and intra- and inter-continental biogeographic diversification in the Asian – New World disjunct plant genus Osmorhiza (Apiaceae)

“…Yet it often reflects genealogical processes including incomplete lineage sorting and hybridization/introgression (Funk and Omland, 2003), two processes that are hard to distinguish for their similar phylogenetic signature (Wendel and Doyle, 1998). One extreme case is chloroplast capture, i.e., chloroplast of one species being transferred to another species through hybridization/introgression, a process that is common in plants ( Acosta and Premoli, 2010;Dorado et al, 1992;Fehrer et al, 2007;Gurushidze et al, 2010;Liston and Kadereit, 1995;Manos et al, 1999;Mir et al, 2009;Okuyama et al, 2005;Rieseberg and Soltis, 1991;Schilling and Panero, 1996;Soltis and Kuzoff, 1995;Wolfe and Elisens, 1995;Yuan and Olmstead, 2008).…”

Systematics of disjunct northeastern Asian and northern North AmericanAllium(Amaryllidaceae)

“…Similarly, Li et al (2010) provide ample views into the phylogenetic relationships and evolutionary and biogeographic pathways of Allium using chloroplast and nuclear sequence data of numerous Chinese endemic species, but their taxonomic sampling has fallen short in the inclusion of representative taxa from other regions of northeastern Asia. The same premise applies to other Allium phylogenies including species from all major taxonomic groups within the genus but focused on European and central Asian (Friesen et al 2006;Gurushidze et al 2008Gurushidze et al , 2010 or western North American (Californian) taxa (Nguyen et al 2008).…”

“…Likewise, noncoding regions of the chloroplast DNA (cpDNA) have also been effective to assess degree of relationships in plants, among them, the trnL (UAA) -trnF (GAA) intergenic region (Bakker et al 1999;Beardsley and Olmstead 2002 and references therein). Nevertheless, the evolutionary rate of this marker and other of chloroplast noncoding regions is not fully understood in the Alliaceae s.s. and (or) Amaryllidaceae alliance (Gurushidze et al 2010;Li et al 2010). Similarly, Li et al (2010) provide ample views into the phylogenetic relationships and evolutionary and biogeographic pathways of Allium using chloroplast and nuclear sequence data of numerous Chinese endemic species, but their taxonomic sampling has fallen short in the inclusion of representative taxa from other regions of northeastern Asia.…”

“…With the advent of molecular systematics, the first generic reassessment of Allium based on molecular data was that of Linne von Berg et al (1996), which marked the beginning of modern Allium systematics. Recent data from both nuclear and chloroplast genomes (e.g., Samoylov et al 1995Samoylov et al , 1999Linne von Berg et al 1996;Mes et al 1997Mes et al , 1999Shinoda 1998, 1999;Friesen et al 2000Friesen et al , 2006Gurushidze et al 2007Gurushidze et al , 2008Gurushidze et al , 2010Nguyen et al 2008;Li et al 2010) have refined the delineation of several taxonomic assemblages proposed based on morphological, anatomical, and cytological characters.…”

Interspecific Relationships in <I>Allium</I> subgenus <I>Melanocrommyum</I> sections <I>Acanthoprason</I> and <I>Asteroprason</I> (Amaryllidaceae) Revealed Using ISSR Markers

“…Only subg. Amerallium Traub has a second center of diversity in North America (Friesen et al 2006;Gurushidze et al 2010). The genus includes many medicinal and ornamental plants as well as vegetables.…”