Species trees have traditionally been inferred from a few selected markers, and genome‐wide investigations remain largely restricted to model organisms or small groups of species for which sampling of fresh material is available, leaving out most of the existing and historical species diversity. The genomes of an increasing number of species, including specimens extracted from natural history collections, are being sequenced at low depth. While these data sets are widely used to analyse organelle genomes, the nuclear fraction is generally ignored. Here we evaluate different reference‐based methods to infer phylogenies of large taxonomic groups from such data sets. Using the example of the Oleeae tribe, a worldwide‐distributed group, we build phylogenies based on single nucleotide polymorphisms (SNPs) obtained using two reference genomes (the olive and ash trees). The inferred phylogenies are overall congruent, yet present differences that might reflect the effect of distance to the reference on the amount of missing data. To limit this issue, genome complexity was reduced by using pairs of orthologous coding sequences as the reference, thus allowing us to combine SNPs obtained using two distinct references. Concatenated and coalescence trees based on these combined SNPs suggest events of incomplete lineage sorting and/or hybridization during the diversification of this large phylogenetic group. Our results show that genome‐wide phylogenetic trees can be inferred from low‐depth sequence data sets for eukaryote groups with complex genomes, and histories of reticulate evolution. This opens new avenues for large‐scale phylogenomics and biogeographical analyses covering both the extant and the historical diversity stored in museum collections.

Museum collections are essential for understanding biodiversity and next-generation sequencing methods (NGS) offer new opportunities to generate genomic data on specimens of extinct species for phylogenetic and other studies. Hesperelaea is a monotypic Oleaceae genus that was collected only once, 140 years ago on Guadalupe Island, Mexico. This lineage is almost certainly extinct, and has been considered an insular paleoendemic of unknown relationship within subtribe Oleinae. Here, a genome skimming approach was attempted on the H. palmeri specimen to generate genomic data in order to interpret the biogeographic history of Hesperelaea in a phylogenetic framework. Despite highly degraded DNA, we obtained the complete plastome, the nuclear ribosomal DNA cluster (nrDNA), and partial sequences of low-copy genes. Six plastid regions and nrDNA internal transcribed spacers were used for phylogenetic estimations of subtribe Oleinae, including data from previous studies. Bayesian and maximum likelihood phylogenies strongly place Hesperelaea within an American lineage that includes Forestiera and Priogymnanthus. Molecular dating suggests an Early Miocene divergence between Hesperelaea and its closest relatives. Our study thus confirms that Hesperelaea was a paleoendemic lineage that likely predates Guadalupe Island, and provides a notable example of the high potential of NGS for analyzing historical herbarium specimens and revolutionizing systematics.

The olive family, Oleaceae, is a group of woody plants comprising 28 genera and ca. 700 species, distributed on all continents (except Antarctica) in both temperate and tropical environments. It includes several genera of major economic and ecological importance such as olives, ash trees, jasmines, forsythias, osmanthuses, privets and lilacs. The natural history of the group is not completely understood yet, but its diversification seems to be associated with polyploidisation events and the evolution of various reproductive and dispersal strategies. In addition, some taxonomical issues still need to be resolved, particularly in the paleopolyploid tribe Oleeae. Reconstructing a robust phylogenetic hypothesis is thus an important step toward a better comprehension of Oleaceae’s diversity. Here, we reconstructed phylogenies of the olive family using 80 plastid coding sequences, 37 mitochondrial genes, the complete nuclear ribosomal cluster and a small multigene family encoding phytochromes (phyB and phyE) of 61 representative species. Tribes and subtribes were strongly supported by all phylogenetic reconstructions, while a few Oleeae genera are still polyphyletic (Chionanthus, Olea, Osmanthus, Nestegis) or paraphyletic (Schrebera, Syringa). Some phylogenetic relationships among tribes remain poorly resolved with conflicts between topologies reconstructed from different genomic regions. The use of nuclear data remains an important challenge especially in a group with ploidy changes (both paleo- and neo-polyploids). This work provides new genomic datasets that will assist the study of the biogeography and taxonomy of the whole Oleaceae.

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