Phylogeny and biogeography of wild roses with specific attention to polyploids

Abstract

Background and aims: The genus Rosa (150-200 species) is widely distributed throughout temperate and sub-tropical habitats from the northern hemisphere to tropical Asia, with only one tropical African species. In order to better understand the evolution of roses, this study examines infrageneric relationships with respect to conventional taxonomy, considers the extent of allopolyploidization and infers macroevolutionary processes that have led to the current distribution of the genus.

Methods: Phylogenetic relationships among 101 species of the genus Rosa were reconstructed using sequences from the plastid psbA-trnH spacer, trnL intron, trnL-F spacer, trnS-G spacer and trnG intron, as well as from nuclear glyceraldehyde 3-phosphate dehydrogenase (GAPDH), which was used to identify putative allopolyploids and infer their possible origins. Chloroplast phylogeny was used to estimate divergence times and reconstruct ancestral areas.

Key results: Most subgenera and sections defined by traditional taxonomy are not monophyletic. However, several clades are partly consistent with currently recognized sections. Allopolyploidy seems to have played an important role in stabilizing intersectional hybrids. Biogeographic analyses suggest that Asia played a central role as a genetic reservoir in the evolution of the genus Rosa.

Conclusions: The ancestral area reconstruction suggests that despite an early presence on the American continent, most extant American species are the results of a later re-colonization from Asia, probably through the Bering Land Bridge. The results suggest more recent exchanges between Asia and western North America than with eastern North America. The current distribution of roses from the Synstylae lineage in Europe is probably the result of a migration from Asia approx. 30 million years ago, after the closure of the Turgai strait. Directions for a new sectional classification of the genus Rosa are proposed, and the analyses provide an evolutionary framework for future studies on this notoriously difficult genus.

Keywords: Rosa; allopolyploidy; ancestral area reconstruction; biogeography; divergence time; hybridization; phylogeny; taxonomy.

Fig. 1.

Morphological diversity of flowers and fruits of a few representatives of Rosa. (A) Flower of Rosa hugonis. (B) Flower of R. moyesii. (C) Flower of R. multibracteata. (D) Flower of R. odorata. (E) Flower of R. praelucens. (F) Flower of R. prattii. (G) Flower of R. tsinglingensis. (H) Flower of R. roxburghii. (I) Flower of R. rubus. (J) Flower of R. roxburghii. (K) Flower of R. villosa. (L) Flower of R. primula. (M) Fruit of R. sikangensis. (N) Fruits of R. omeiensis. (O) Fruit of R. mairei. (P) Fruit of R. macrophylla. (Q) Fruits of R. sweginzowii.

Fig. 2.

Phylogenetic relationships among Rosa species as reconstructed by Maximum Likelihood analyses of three chloroplast regions (psbA-trnH spacer, trnL region and trnG region). Bootstrap values are placed as close as possible to the node supported. The ploidy level of each species is given after its name (see Erlanson, 1929, 1934, 1938; Roberts, 1977; Yokoya et al., 2000; Roberts et al., 2009; Jian et al., 2010). The names of known polyploids are in bold (in R. sect. Caninae all species are presumed to be polyploids even when the ploidy number is not exactly known). Wissemann’s (2003) classification is compared with our clades. A P designates our Pimpinellifoliae clade, a C our Cinnamomeae clade, an S our Synstylae clade, Ca our Caninae clade and Ru our Rubiginae clade.

Fig. 3.

Network representing the relationships among copies of GAPDH obtained from Rosa species. A ‘c’ followed by a number indicates the number attributed to one particular clone sequenced. The groups are compared with our main clades from the chloroplast analyses. Purple is attributed to Rosa subgen. Platyrhodon, yellow to R. sect. Banksianae, bright orange to R. sect. Bracteatae, brown to R. sect. Laevigatae, light pink to Pimpinellifoliae clade, green to Cinnamomeae clade, light blue to Synstylae clade and a deeper blue to R. sect. Caninae. Two species have a particular colour, R. spinosissima is highlighted with a deeper pink colour and R. abyssinica with a light orange colour. Two types of copies, C1 and C2, are distinguished in our Cinnamomeae group. Some polyploids have several copies with different affinities. The names of known polyploids are in bold (in R. sect. Caninae all species are presumed to be polyploids even when the ploidy number is not exactly known).

Fig. 4.

Chronogram obtained from BEAST analyses of chloroplast regions. Branches are coloured according to the ancestral area reconstruction analyses (DEC model) including fossils information. A P designates our Pimpinellifoliae clade, a C our Cinnamomeae clade and an S our Synstylae clade. The names of known polyploids are in bold (in R. sect. Caninae all species are presumed to be polyploids even when the ploidy number is not exactly known).