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Buzz-Pollinated Dodecatheon Originated from Within The American Journal of Botany 91(6): 926±942. 2004. BUZZ-POLLINATED DODECATHEON ORIGINATED FROM WITHIN THE HETEROSTYLOUS PRIMULA SUBGENUS AURICULASTRUM (PRIMULACEAE): ASEVEN-REGION CPDNA PHYLOGENY AND ITS IMPLICATIONS FOR FLORAL EVOLUTION1 AUSTIN R. MAST,2,4 DANIELLE M. S. FELLER,2,5 SYLVIA KELSO,3 AND ELENA CONTI2 2Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland; and 3Department of Biology, Colorado College, Colorado Springs, Colorado 80903 USA We sequenced seven cpDNA regions from 70 spp. in Dodecatheon, Primula subgenus Auriculastrum, and outgroups, reconstructed their cpDNA phylogeny with maximum parsimony, and determined branch support with bootstrap frequencies and Bayesian posterior probabilities. Strongly supported conclusions include the (1) paraphyly of Primula subgenus Auriculastrum with respect to a mono- phyletic Dodecatheon, (2) sister relationship between the North American Dodecatheon and the Californian P. suffrutescens, (3) novel basal split in Dodecatheon to produce one clade with rugose and one clade with smooth anther connectives, (4) monophyly of all sections of Primula subgenus Auriculastrum, and (5) exclusion of the enigmatic Primula section Amethystina from the similar Primula subgenus Auriculastrum. These results support the origin of the monomorphic, buzz-pollinated ¯ower of Dodecatheon from the heterostylous ¯ower of Primula. We marshal evidence to support the novel hypothesis that the solanoid ¯ower of Dodecatheon represents the ®xation of recessive alleles at the heterostyly linkage group (pin phenotype). Of the remaining traits associated with their solanoid ¯owers, we recognize at least six likely to have arisen with the origin of Dodecatheon, one that preceded it (¯ower coloration, a transfer exaptation in Dodecatheon), and one that followed it (rugose anther connectives, an adaptation to buzz pollination). Key words: adaptation; buzz pollination; Cortusa; Dodecatheon; exaptation; heterostyly; Primula subgenus Auriculastrum; so- lanoid ¯owers. The nodding, often brilliantly purple and yellow, ``shooting of Dodecatheon, and the later ®ne-tuning of the buzz-polli- star'' ¯owers of the largely North American genus Dodecath- nation syndrome. eon (15 spp. in the Primulaceae) represent to many the most During the buzz pollination of Dodecatheon, pollen is re- familiar example of the buzz-pollination syndrome. Yet the moved from the anthers by vibrations that originate with a phylogenetic context for the genus, and thus the evolutionary settled bee's indirect ¯ight muscles and are transferred to the origins of individual ¯oral features, has remained largely am- androecium via its legs and mandibles (Harder and Barclay, biguous. Here, we reconstruct the chloroplast phylogeny for 1994). Pendant ¯owers with re¯exed petals and large, con- Dodecatheon and its closest relatives in the Primulaceae and spicuous, connivent, poricidal anthers, as seen in Dodecath- consider the evolution of ¯oral features critical to the plant± eon, were dubbed ``solanoid'' by Vogel (1978). Solanoid ¯ow- pollinator relationship in light of the phylogeny. The hypoth- ers are independently derived in numerous buzz-pollinated esis that emerges involves the co-opting of preexisting features genera (Vogel, 1978; Buchmann, 1983; Faegri, 1986; Endress, (including one of the two ¯oral morphologies present in the 1994), including Ardisia, Lysimachia, and Cyclamen, three distylous ancestor), the genesis of new features with the origin close relatives of Dodecatheon in the Myrsinaceae (sensu KaÈl- lersjoÈ et al., 2000). 1 Manuscript received 7 August 2003; revision accepted 22 January 2004. While the solanoid ¯owers of Dodecatheon make them in- The authors thank individuals and institutions who provided ®eld assis- stantly recognizable at anthesis, sterile, pre-anthetic, and fruit- tance, leaf material, lab space and assistance, advice, and hospitality, including ing individuals of Dodecatheon are strikingly similar to mem- A. Anderberg, P. Ashby, A. Batten, B. Baldwin, M. Black, K. Chambers, J. Cole, P. Endress, T. Eriksson, P. Eveleigh, T. Forbis, N. Fujii, J. Grant, S. bers of Primula subgenus Auriculastrum (ca. 30 spp. from Hamm, N. Holmgren, D. Lang, K. Lever, A. Liston, M. Matthews, R. Mc- North America, Paci®c coastal Asia, and Europe). Both genera Beath, R. Olmstead, C. Parker, G. Pellegrino, N. Repke, J. Richards, C. Ro- have members that grow in moist alpine meadows and stream- land, T. Rye, J. SchoÈnenberger, I. Scott, J. Sime, F. Tahbaz, S. Wagen, B. sides, have chromosome numbers of 2n 5 44, and produce Wessa, Y.-M. Yuan, L. Zhang, the Copenhagen Botanic Garden, Rancho Santa valvate capsules on long scapes arising from a rosette of Ana Botanic Garden, Royal Botanic Garden Edinburgh, and Tromsù Botanic ¯eshy, lance-shaped leaves with involute vernation. In an often Garden. C. Hardy, R. Nyffeler, and three anonymous reviewers provided help- ful comments on drafts of this paper. This work was supported by grants from quoted observation, Thompson (1953, p. 75) noted that Do- the Swiss National Fund (3100-061674.00/1) and the Equal Opportunity Pro- decatheon jeffreyi and Primula parryi are ``virtually indistin- gram of the University of Zurich to E. Conti, and the leaf material shared guishable when the corollas and inserted anthers are re- with us by F. Tahbaz was collected through the support of the Lawrence R. moved.'' Recent authors (Thompson, 1953; Wendelbo, 1961b; Heckard Fund of the Jepson Herbarium. Richards, 1993, 2002; Holmgren, 1994) have taken this sim- 4 Present address: Department of Biological Sciences, Florida State Uni- versity, Tallahassee, FL 32306; E-mail: [email protected]. ilarity as evidence for a close phylogenetic relationship 5 Present address: Department of Biological Sciences, Florida State Uni- between Dodecatheon and Primula subgenus Auriculastrum versity, Tallahassee, Florida 32306 USA. (particularly Primula section Parryi). 926 June 2004] MAST ET AL.ÐFLORAL EVOLUTION IN DODECATHEON AND PRIMULA 927 This view that similarities between Dodecatheon and Prim- thus increases female ®tness; Barrett, 2002). Distyly, and the ula subgenus Auriculastrum have shared evolutionary origins functionally similar tristyly, are currently known in 28 ¯ow- is bolstered by the results of phylogenetic analyses of cpDNA ering plant families (Barrett et al., 2000; Barrett, 2002). (KaÈllersjoÈ et al., 2000; Mast et al., 2001; Trift et al., 2002) Within Primula, distyly is thought to be controlled by at and the internal transcribed spacers of the nuclear ribosomal least three tightly linked loci (Ernst, 1925, 1936, 1957; Lewis, DNA (Martins et al., 2003). In each of these studies, the single 1949; Dowrick, 1956), that are frequently referred to as the sampled exemplar of Dodecatheon is resolved as most closely ``heterostyly supergene'' (e.g., Ganders, 1979; Barrett, 2002). related to subgenus Auriculastrum. In the only molecular study The style length, stigmatic papillae length, and female mating to date to sample each of the four sections of subgenus Au- type are thought to be controlled by locus G, the pollen size riculastrum, Mast et al. (2001) found weak support (66% boot- and male mating type by locus P (or two separate loci Pp and strap frequency) for an unexpected sister relationship between Pm, respectively; Kurian and Richards, 1997), and the anther Dodecatheon and the monotypic Primula section Suffrutescens height by locus A. Pins are homozygous recessive for these (Richards, 2002). Primula suffrutescens, a sub-shrubby species loci (gpa/gpa) and thrums are heterozygous (GPA/gpa; Bate- with wedge-shaped leaves from rock crevices and granite scree son and Gregory, 1905; Lewis and Jones, 1992). The rarity of in the Sierra Nevada of California, lies close to the Paci®c homozygote thrums might be due to the presence of recessive Northwest center of diversity for Dodecatheon, yet it shares sublethal alleles linked to GPA (Kurian and Richards, 1997; fewer morphological and ecological similarities with Dode- Richards, 1998). The loci are likely ordered GPA, at least in catheon than does Primula section Parryi. Primula subgenus Auriculastrum (Kurian and Richards, 1997), Unsampled in these previous molecular studies is a section based on the frequency of observed recombinations (Dowrick, of Primula that could modify our views on the proper circum- 1956; Lewis and Jones, 1992; but see Charlesworth and Char- scription of Primula subgenus Auriculastrum and thus the evo- lesworth, 1979). lutionary context for the origin of Dodecatheon. This section, The objectives of this study are to reconstruct the chloro- the Asian Primula section Amethystina (eight spp.), has ¯eshy, plast phylogeny of Dodecatheon and Primula subgenus Au- toothed leaves and globose capsules that are reminiscent of riculastrum and to use this to address four questions: (1) Are subgenus Auriculastrum (Smith and Fletcher, 1942). Further- traditionally recognized taxa (Dodecatheon, Primula subgenus more, uncertainty remains regarding its leaf vernation, because Auriculastrum, and sections therein) monophyletic? (2) If Do- published observations (Smith and Fletcher, 1942, 1950; Wen- decatheon is nested in Primula, does our increased character delbo, 1961a; sketches by J. Haldova in Halda, 1992) are con- sampling support a sister relationship between it and the mor- ¯icting and inconclusive (Mast et al., 2001). Leaf vernation phologically and ecologically similar Primula section Parryi? has seldom changed state
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