Phylogenetic Reconstruction of the Evolution of Stylar Polymorphisms in Narcissus (Amaryllidaceae)1
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American Journal of Botany 91(7): 1007±1021. 2004. INVITED SPECIAL PAPER PHYLOGENETIC RECONSTRUCTION OF THE EVOLUTION OF STYLAR POLYMORPHISMS IN NARCISSUS (AMARYLLIDACEAE)1 SEAN W. G RAHAM2,4 AND SPENCER C. H. BARRETT3 2UBC Botanical Garden and Centre for Plant Research, 6804 SW Marine Drive, The University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4; and 3Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S 3B2 We investigated the origin of stylar polymorphisms in Narcissus, which possesses a remarkable range of stylar conditions and diverse types of ¯oral morphology and pollination biology. Reconstruction of evolutionary change was complicated by incomplete resolution of trees inferred from two rapidly evolving chloroplast regions, but we bracketed reconstructions expected on the fully resolved plastid- based tree by considering all possible resolutions of polytomies on the shortest trees. Stigma-height dimorphism likely arose on several occasions in Narcissus and persisted across multiple speciation events. As proposed in published models, this rare type of stylar polymorphism is ancestral to distyly. While there is no evidence in Narcissus that dimorphism preceded tristyly, a rapid transition between them may explain the lack of a phylogenetic footprint for this evolutionary sequence. The single instances of distyly and tristyly in Narcissus albimarginatus and N. triandrus, respectively, are clearly not homologous, an evolutionary convergence unique to Amaryllidaceae. Floral morphology was likely an important trigger for the evolution of stylar polymorphisms: Concentrated-changes tests indicate that a long, narrow ¯oral tube may have been associated with the emergence of stigma-height dimorphism and that this type of tube, in combination with a deep corona, likely promoted, or at least was associated with, the parallel origins of heterostyly. Key words: ancestral-state reconstructions; concentrated-changes test (CCT); ¯oral evolution; heterostyly; Narcissus; ndF; pol- lination biology; stigma-height dimorphism; stylar polymorphism; trnL-trnF. Flowering plants possess extraordinary diversity in repro- arrangement of sex-organ heights. The reciprocal herkogamy ductive traits, even among closely related species. This vari- that characterizes heterostyly is a structural mechanism that ation is the result of the evolutionary lability of reproductive functions to increase the pro®ciency of cross-pollination in characters and implies that there are diverse functional solu- species with perfect ¯owers (Lloyd and Webb, 1992a, b). Al- tions for achieving mating and fertility. The ¯oral diversi®- though heterostyly (both distyly and tristyly) has been studied cation that has accompanied the coevolution of ¯owers and intensively since the mid-nineteenth century (reviewed in Bar- animal pollinators is particularly striking and has resulted in rett, 1992), remarkably little is known about its evolutionary contrasting suites of ¯oral characters associated with different history. Only two studies have explicitly used phylogenetic pollinator groups (e.g., Grant and Grant, 1965; Armbruster, approaches to investigate the origins of heterostyly (distylyÐ 1993; Johnston et al., 1998; Schemske and Bradshaw, 1999). Schoen et al., 1997; tristylyÐKohn et al., 1996); neither was Although diversifying selection has played a prominent role able to identify the ancestral states or the precise evolutionary in ¯oral evolution, pervasive convergence in pollination mech- pathways involved in the evolution of these complex polli- anisms also characterizes many unrelated animal-pollinated nation mechanisms. groups. The multiple origins of the heterostylous genetic poly- Narcissus a small genus of animal-pollinated geophytes in morphisms distyly and tristyly across at least 28 diverse ani- Amaryllidaceae (monocots: Asparagales) with exceptional ¯o- mal-pollinated angiosperm families are a classic example of ral diversity (e.g., Figs. 1, 2), provides an excellent opportunity the convergent evolution of plant sexual systems (Darwin, for examining the evolutionary history of heterostyly. Four 1877; Ganders, 1979; Lloyd and Webb, 1992a, b; Barrett et major classes of stylar condition, stylar monomorphism, stig- al., 2000b). Most heterostylous species are adapted for polli- ma-height dimorphism, distyly, and tristyly (Fig. 2), are rep- nation by long-tongued pollinators and commonly possess ac- tinomorphic, tubular ¯owers with a stereotypically reciprocal resented among the 10 sections recognized in the genus (Hen- riques, 1887; Fernandes, 1935; Dulberger, 1964; Bateman, 1968; Lloyd et al., 1990; Arroyo and Dafni, 1995; Barrett et 1 Manuscript received 2 September 2003; revision accepted 5 March 2004. al., 1996, 1997; Arroyo and Barrett, 2000; Baker et al., 2000b, The authors thank John Blanchard for sharing his broad expertise of the genus and for providing material from his live collection. Juan Arroyo and c; Arroyo et al., 2002; Thompson et al., 2003). No other het- Mark Chase also provided material. We also thank Juan Arroyo, Lawrence erostylous taxon displays this range of stylar variation. Nar- Harder, Angela Baker, John Thompson, and Luis Villar for helpful discussions cissus may therefore provide one of our best opportunities for and locality information. Hardeep Rai and Heath O'Brien provided substantial investigating the evolutionary pathways by which heterosty- assistance with laboratory work. Alan Meerow and Peter Endress provided lous polymorphisms originated. A diversity of ¯ower shapes helpful comments on the manuscript. This work was funded by Discovery Grants from the Natural Sciences and Engineering Research Council of Can- is found in Narcissus (Fig. 1), particularly associated with co- ada (NSERC) to S. W. G. and S. C. H. B. rona size and ¯oral tube length. It would therefore be valuable 4 E-mail: [email protected]. to assess the possible functional role of ¯oral morphology in 1007 1008 AMERICAN JOURNAL OF BOTANY [Vol. 91 stimulating evolutionary transitions among the different stylar tionary relationships and the selective mechanisms leading to conditions. evolutionary transitions among them. Species of Narcissus can be classi®ed as to whether they In Narcissus, the evolutionary sequence(s) in which the dif- are monomorphic, dimorphic, or trimorphic for style length ferent stylar polymorphisms originated from stylar monomor- (reviewed in Barrett et al., 1996). Here we use the term ``stylar phism is not known. A simple model based on increasing ¯oral polymorphism'' to refer to populations or species that are di- complexity posits an evolutionary transition series from an- morphic or trimorphic for style length, irrespective of the type cestral monomorphism, through stigma-height dimorphism, to of polymorphism (stigma-height dimorphism, distyly, tristyly) distyly, and then ®nally to tristyly. Theoretical support for that they exhibit. Monomorphic species are usually composed parts of this sequence of events comes from models for the of plants with long-styled ¯owers, with stigmas protruding be- evolution of distyly and tristyly. Lloyd and Webb's (1992a, b) yond the two anther levels that typically occur in members of ``pollen-transfer'' model for the evolution of distyly proposes this genus (e.g., Figs. 1d, h; 2a). This condition is referred to that it evolves from a monomorphic ancestor with approach as ``approach herkogamy'' (see Webb and Lloyd, 1986, for a herkogamous ¯owers, via an intermediate stage of stigma- review of herkogamy) and is the most common stylar condi- height dimorphism. The ``inbreeding avoidance'' model for the tion in Narcissus. In some monomorphic species (e.g., N. ser- evolution of distyly (Charlesworth and Charlesworth, 1979) otinus, Fig. 1m; N. viridi¯orus, Fig. 1n) the stigma is located also posits an intermediate stage of stigma-height dimorphism, just above or at the same level as the anthers. Populations with but the ancestral condition in this case is assumed to be a stylar monomorphism often display considerable quantitative homostylous population with long styles and long-level an- variation in style length, but do not exhibit the clear bimodality thers. Finally, Charlesworth's (1979) model of the evolution or trimodality that characterizes species with stylar polymor- of tristyly commences with an ancestral monomorphic long- phism (Barrett et al., 1996). styled population, with a transient dimorphic stage that then There are two types of stylar dimorphism in Narcissus. The becomes invaded by the M-morph, establishing stylar trimor- most common, stigma-height dimorphism (Fig. 2b), involves phism. The dimorphic stage involves a population with recip- populations with two ¯oral morphs that differ in style length rocal herkogamy, and therefore stigma-height dimorphism is (long- and short-styled plants, hereafter referred to as L- and not explicitly dealt with in this model. The particular evolu- S-morphs), but which have anthers placed at roughly the same tionary sequences in these three models are supported by de- position at the top of the ¯oral tube (Dulberger, 1964; Baker tailed theoretical arguments and are certainly plausible; how- et al., 2000c; Arroyo et al., 2002). This polymorphism occurs ever, empirical support from comparative analyses of heter- in approximately a dozen species distributed among three sec- ostylous groups of both the ancestral states and intermediate tions of the genus (Apodanthi, Fig. 1g; Jonquillae, Fig.