Systematics of Oenothera Section Oenothera Subsection Oenothera (Onagraceae)

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Abstract
In this comprehensive revision of Oenothera subsect. Oenothera, representing the most complex species group in the Onagraceae, 13 species are recognized. This subsection, known as "Euoenothera," has had a long history of study, notably cytogenetic and genetic work that elucidated the anomalous genetic system of permanent translocation heterozygosity (PTH). The group has been significant in studies of chloroplast function, genetics, self-incompatibility, genetic interactions between genome and plastome, and recently as a pharmacological crop for the fatty acid γ-linolenic acid. New cytological, common garden, and extensive herbarium studies were incorporated into a revised taxonomic system using features of the genome, plastome, and morphology that is consistent with other angiosperm classifications. All published names (562) were analyzed, including many names (156), especially from the cytogenetics literature, that have never been validly published. Of the 388 validly published specific and infraspecific names the greatest number (292) have been applied to the widespread PTH species (O. biennis, O. glazioviana, O. oakesiana, O. parviflora, and O. villosa), including many for naturalized European populations. Within the subsection there are three major genomes, designated A, B, and C, and five basic plastid genomes (plastomes I, II, III, IV, and V). Five species are delimited with the plesiomorphic features of primarily outcrossed flowers, bivalent formation in meiosis, and genomic homozygosity, and eight PTH species. The properties of the PTH system serve to partition and fix variation into perceptibly differentiated true-breeding strains. Our approach aggregates the essentially clonal PTH populations (or microspecies) into species delimited according to the composition of their genomic complexes, plastome type, and associated morphological characters to reflect the evolutionary history of the group and to provide a reliable means for identification. There are three basic lineages within Oenothera subsect. Oenothera, relating to genome and plastome composition. Five of the species have AA genomes and plastome I (O. elata, O. longissima, O. jamesii, O. wolfii, and O. villosa). The first three species have plesiomorphic characteristics of mostly outcrossed large flowers and formation of bivalents or small rings of chromosomes during meiosis. Oenothera longissima and O. jamesii appear to have been derived directly from O. elata. The other two AA plastome I species, O. wolfii and the polymorphic O. villosa, are both PTH species. The former, a rare Pacific coastal endemic, is presumably derived from O. elata subsp. hookeri, while O. villosa (widespread in the western half of North America) appears to have been derived from O. elata subsp. hirsutissima. The second lineage consists of two species of eastern North America with BB genomes and plastome III. Self-incompatibility, a plesiomorphic feature retained sporadically in O. grandiflora, does not occur elsewhere in the subsection. Oenothera nutans is a PTH species presumably derived directly from O. grandiflora. The third lineage consists of the very distinctive Allegheny Mountains shale barren endemic, O. argillicola, which has a CC genomic composition and is the only species with plastome V. Three additional PTH species with wide, primarily eastern North American natural ranges had hybrid origins: O. biennis (AB or BA with plastome II or III); O. oakesiana (AC with plastome IV); and O. parviflora (BC with plastome IV). All three species are widely naturalized, especially in Europe. Hybrids occur between many of the species (19 known combinations), especially the PTH species. When they represent a more widespread phenotype, they are included in the taxon they phenotypically most closely resemble and that has the same genome and plastome composition. Exceptionally, two morphologically distinctive additional PTH species of recent hybrid origin are recognized: O. glazioviana (AB-III), and O. stucchii (AA-I). Both originated in Europe via hybridization outside the indigenous range of the subsection, the former possibly in England and the latter in Italy. Oenothera glazioviana has achieved a nearly worldwide distribution.

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