A phylogeny of the evening primrose family (Onagraceae) using a target enrichment approach with 303 nuclear loci

Abstract

Background: The evening primrose family (Onagraceae) includes 664 species (803 taxa) with a center of diversity in the Americas, especially western North America. Ongoing research in Onagraceae includes exploring striking variation in floral morphology, scent composition, and breeding system, as well as the role of these traits in driving diversity among plants and their interacting pollinators and herbivores. However, these efforts are limited by the lack of a comprehensive, well-resolved phylogeny. Previous phylogenetic studies based on a few loci strongly support the monophyly of the family and the sister relationship of the two largest tribes but fail to resolve several key relationships.

Results: We used a target enrichment approach to reconstruct the phylogeny of Onagraceae using 303 highly conserved, low-copy nuclear loci. We present a phylogeny for Onagraceae with 169 individuals representing 152 taxa sampled across the family, including extensive sampling within the largest tribe, Onagreae. Deep splits within the family are strongly supported, whereas relationships among closely related genera and species are characterized by extensive conflict among individual gene trees.

Conclusions: This phylogenetic resource will augment current research projects focused throughout the family in genomics, ecology, coevolutionary dynamics, biogeography, and the evolution of characters driving diversification in the family.

Keywords: Evening primrose; HybSeq; Onagraceae; Phylogenetics; Phylogenomics; Plant systematics; Target enrichment.

Fig. 1

Onagraceae. subfamily Ludwigioideae. A Ludwigia octovalvis. Flower and immature capsule. Baldwin Co., Alabama (image Warren Wagner in 2003). Subfamily Onagroideae B-L. B Tribe Hauyeae. Hauya elegans subsp. lucida. Branch with flower at anthesis and in bud. Cultivated at San Diego Zoo (image Wikipedia in 2008). C, D Tribe Circaeeae. C. Fuchsia inflata. Inflorescence. Cusco, Peru (image P. Berry in 1978). D Circaea pacifica. Inflorescence and young fruit. Benton Co Oregon (image G. Carr-4162b in 2006). E, F Tribe Lopezieae. E Lopezia racemosa subsp racemosa. Flower with inflorescence and leaves. Puebla, Mexcio (image Jon Amith in 2007). F Megacorax gracielanus. Chasmogamous flower with bud and stem with leaves. Sierra de Coneto, Durango, Mexico (image M. Socorro Gonzalez-Elizondo in 2021). G Tribe Gongylocarpeae. Gongylocarpus fruticulosus. Stem with flowers and gall-like mature fruit embedded in pith of stem, indehiscent, and inset showing flower closeup. Isla Magdalena, Baja California Sur, Mexico (images Jon Rebman in 2016). Tribe Epilobieae H-J H. Chamaenerion angustifolium subsp. circumvagum. Stem with inflorescence with open flowers and maturing capsules. MN (image Peter M. Dziuk, Minnesota Wildflowers in 2002). I Epilobium nankotaizanense. Habit with flower. Taiwan (image Ching-I Peng in 2008). J Epilobium canum subsp latifolium. Stem with flowers and some dispersed seeds. Curry Co., OR (image Gerry Carr 6317b in 2015). Tribe Onagreae. K, L K. Xylonagra arborea. Stem with flowers and very young fruit. Cultivated at Missouri Botanical Garden, originally from Baja California, Mexico (image Ching-I Peng in 1982). L. Taraxia ovata. Habit with flowers. Monterey, CA (image Christian Schwarz)

Fig. 2

Tribe Onagreae. A-L. A Clarkia rhomboidea. Stem with flower and immature capsule. Jefferson Co., OR (image Gerry Carr 6468b in 2006). B Chylismiella pterosperma. Stem with leaves, flower, and buds. Inyo Co., CA (image Larry Blakely in 2001). C Gayophytum diffusum subsp. diffusum. Stem with flowers and buds. Tulare CA (image Peter Raven collection). D Eremothera boothii susbp. boothii. Flowers and buds. Mono Co., CA (image Michael Moore 3260 in 2015). E Camissonia contorta. Plant with flowers and young capsules. Klickitat Co., WA (image Gerry Carr 0356b in 2009). F Neoholmgrenia andina. Plant with fading flower and immature capsule. Harney Co., OR (image Gerry Carr 0996b in 2011). G Tetrapteron graciliflorum. Plant with flower and immature capsule. Marin Co., CA (image David Greenberger in 2018). H Camissoniopsis cheiranthifolia subsp. cheiranthifolia. Stem with flowers and immature capsules. San Mateo Co., CA (image Leslie Flint in 2015). Inset of immature capsule. Monterey, CA (image Steve Rovell in 2016). I Eulobus californicus. Stem with flowers. San Diego Co., CA (image Ron King in 2021). J Chylismia eastwoodiae. Flowers and buds with capsules in background. Emery Co., UT (image Rob Raguso in 2001). K Oenothera tetraptera. Plant with flower (from Oageng Modise) and immature capsule. South Africa (image Behrens in 2021). Inset of dehisced capsule with seeds clustered inside. South Africa (image Warren Wagner in 2008). L Oenothera toumeyi. Stem with flowers. Cochise Co., AZ (image Rob Raguso in 1996)

Fig. 3

Best-scoring ASTRAL-II tree (displayed as a cladogram) based on 303 input best-scoring maximum likelihood gene trees from RAxML. Numbers above branches represent the number of gene trees in concordance with a particular clade in the species tree (blue in pie chart), whereas those below indicate gene trees in conflict (red/green in pie chart). Pie charts were constructed using 206 genes, and additionally represent the portion of conflicting gene trees that support the main alternative (green), those that support all remaining alternatives (red), and finally those with no information (gray), which could be due to bootstrap support < 50% for the branch in question or missing data (Fig. S1, Additional file 2). The ASTRAL tree and concatenated ML tree are represented with branch lengths (with the exception of tip branch lengths) in Figure S2 (Additional file 2) and individual tree files are provided in the Dryad repository that accompanies this study

Fig. 4

Distribution of support for the monophyly of 17 of 22 genera (x-axis) in Onagraceae among 303 gene trees using DiscoVista. Gene trees (y-axis) are shown to strongly support (dark green), weakly support (teal), weakly reject (pink), or strongly reject (maroon) genera. Shown in blue are gene trees that do not contain any data for a certain genus

Fig. 5

Alternative topologies for clades within Onagraceae. The relative frequency of gene trees is shown for quartets of taxa (bar graphs). Green bars indicate the RAxML-ASTRAL topology, teal and light blue bars indicate alternative topologies. Dotted lines indicate 1/3 of the total gene trees for each quartet; roughly equal proportions for the three possible topologies indicate a polytomy within the present dataset. a Early-diverging Onagraceae; b Placement of Hauya; c Monophyly of Circaea and Fuchsia; d Monophyly of Megacorax and Lopezia; e Early-diverging Onagreae, where clades X and Y refer to the following groups: clade X comprises Camissoniopsis, Eremothera, Camissonia, Tetrapteron, and Neoholmgrenia; clade Y comprises Clarkia, Chylismiella, and Gayophytum; f Clades within Oenothera, the quartet at node I is ((Lineage B, sect. Pachylophus), Lineage A + sect. Calylophus) Outgroup) and node II is ((Lineage A, sect. Calylophus), (Lineage B + sect. Pachylophus) Outgroup), the mode common alternative topology for node I is shown