A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during neogene and quaternary climate change

Abstract

BackgroundGrapes are one of the most economically important fruit crops. There are about 60 species in the genus Vitis. The phylogenetic relationships among these species are of keen interest for the conservation and use of this germplasm. We selected 309 accessions from 48 Vitis species,varieties, and outgroups, examined ~11 kb (~3.4 Mb total) of aligned nuclear DNA sequences from 27 unlinked genes in a phylogenetic context, and estimated divergence times based on fossil calibrations.ResultsVitis formed a strongly supported clade. There was substantial support for species and less for the higher-level groupings (series). As estimated from extant taxa, the crown age of Vitis was 28 Ma and the divergence of subgenera (Vitis and Muscadinia) occurred at ~18 Ma. Higher clades in subgenus Vitis diverged 16 – 5 Ma with overlapping confidence intervals, and ongoing divergence formed extant species at 12 – 1.3 Ma. Several species had species-specific SNPs. NeighborNet analysis showed extensive reticulation at the core of subgenus Vitis representing the deeper nodes, with extensive reticulation radiating outward. Fitch Parsimony identified North America as the origin of the most recent common ancestor of extant Vitis species.ConclusionsPhylogenetic patterns suggested origination of the genus in North America, fragmentation of an ancestral range during the Miocene, formation of extant species in the late Miocene-Pleistocene, and differentiation of species in the context of Pliocene-Quaternary tectonic and climatic change. Nuclear SNPs effectively resolved relationships at and below the species level in grapes and rectified several misclassifications of accessions in the repositories. Our results challenge current higher-level classifications, reveal the abundance of genetic diversity in the genus that is potentially available for crop improvement, and provide a valuable resource for species delineation, germplasm conservation and use.

Patterns of SNP distribution provide a molecular basis for high genetic diversity and genetic differentiation in Vitis species

“…2) representing genetic relationship between accessions and between species in this study are very similar to those in our previous study estimated by other algorithms (Wan et al 2013). …”

“…High nucleotide diversity (Table S9) and high CV value of nucleotide diversity (Table S53) in most Vitis species suggested high genetic variability in these species. Our previous study confirmed broad hybridization among species in the evolutionary history of Vitis (Wan et al 2013). In this case, the phylogenetic species concept may be unsuitable as suggested by López-Pujol et al (2012).…”

“…In this case, the phylogenetic species concept may be unsuitable as suggested by López-Pujol et al (2012). Our phylogenetic study demonstrated that the consensus phylogenetic tree in Vitis was impossible to obtain from numerous phylogenetic algorithms (Wan et al 2013).…”

“…Another disadvantage of tree building methods is that results may be very distinct among algorithms, among different numbers of permutation tests and among hierarchical genetic structures when the number of samples is vast for analyses (Peakall and Smouse 2006). In addition, strong evolutionary signals (historic hybridization and splitting, e.g., in Vitis (Wan et al 2013) may lead to unwieldy trees that are difficult to interpret. PCoA uses a strategy in which the essential signals in the data were quantified and used for estimation, thus minimizing influence from conflicting signals of patterns of genetic relationships among operational taxonomic units (OTUs) (Peakall and Smouse 2006).…”

“…The software "Proseq" was used to visually identify SNPs and manually create a spreadsheet containing all scored SNPs. All sequences were released in NCBI with NCBI accession numbers [Genbank: JX952227-JX960379, EMBL: HF544510-HF544512] (Wan et al 2013). …”