Combined Phylogenetic Analyses Reveal Interfamilial Relationships and Patterns of floral Evolution in the Eudicot Order Fabales
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Cladistics Cladistics 1 (2012) 1–29 10.1111/j.1096-0031.2012.00392.x Combined phylogenetic analyses reveal interfamilial relationships and patterns of floral evolution in the eudicot order Fabales M. Ange´ lica Belloa,b,c,*, Paula J. Rudallb and Julie A. Hawkinsa aSchool of Biological Sciences, Lyle Tower, the University of Reading, Reading, Berkshire RG6 6BX, UK; bJodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK; cReal Jardı´n Bota´nico-CSIC, Plaza de Murillo 2, CP 28014 Madrid, Spain Accepted 5 January 2012 Abstract Relationships between the four families placed in the angiosperm order Fabales (Leguminosae, Polygalaceae, Quillajaceae, Surianaceae) were hitherto poorly resolved. We combine published molecular data for the chloroplast regions matK and rbcL with 66 morphological characters surveyed for 73 ingroup and two outgroup species, and use Parsimony and Bayesian approaches to explore matrices with different missing data. All combined analyses using Parsimony recovered the topology Polygalaceae (Leguminosae (Quillajaceae + Surianaceae)). Bayesian analyses with matched morphological and molecular sampling recover the same topology, but analyses based on other data recover a different Bayesian topology: ((Polygalaceae + Leguminosae) (Quillajaceae + Surianaceae)). We explore the evolution of floral characters in the context of the more consistent topology: Polygalaceae (Leguminosae (Quillajaceae + Surianaceae)). This reveals synapomorphies for (Leguminosae (Quillajaceae + Suri- anaceae)) as the presence of free filaments and marginal ⁄ ventral placentation, for (Quillajaceae + Surianaceae) as pentamery and apocarpy, and for Leguminosae the presence of an abaxial median sepal and unicarpellate gynoecium. An octamerous androecium is synapomorphic for Polygalaceae. The development of papilionate flowers, and the evolutionary context in which these phenotypes appeared in Leguminosae and Polygalaceae, shows that the morphologies are convergent rather than synapomorphic within Fabales. The current order Fabales was identified almost two analyses of Fabales using molecular data sets have decades ago (Chase et al., 1993), but remains ill-defined recovered conflicting interfamilial relationships and in terms of morphological synapomorphies. Further- failed to provide support for these relationships (Doyle more, the relationships between the four families placed et al., 2000; Persson, 2001; Bello et al., 2009). Here, we in the order, Leguminosae, Polygalaceae, Quillajaceae, explore morphology as a source of characters to help and Surianaceae, remain uncertain. Two of the families, resolve this problem. We test whether combined anal- Polygalaceae and Leguminosae, are species-rich and yses can recover robustly supported and resolved widely distributed. They include ca. 21 ⁄1000 and phylogenetic relationships, and also whether any syna- 727 ⁄19 325 genera and species, respectively (Persson, pomorphies can be identified that characterize the order, 2001; Lewis et al., 2005). In contrast, the monogeneric families, and any novel groups. family Quillajaceae comprises just two species, found in Our morphological survey focuses on reproductive Chile and Brazil (Fuks, 1983; Lersten and Horner, traits as a potentially rich source of characters. In 2005). The other species-poor family of Fabales, Suri- general, the performance of reproductive characters in anaceae, comprises about five genera and ten species, phylogenetic inference has proved little better than other and is restricted to Australia and Mexico, but includes morphological characters (Bateman and Simpson, 1998; also the pantropically distributed species Suriana mari- Lavin et al., 2001). However, some studies have shown tima L. (Crayn et al., 1995). Previous phylogenetic improved phylogenetic resolution after inclusion of floral characters (e.g. in caesalpinioid legumes, Heren- *Corresponding author: deen et al., 2003). Floral traits are often fundamental for E-mail address: [email protected] family diagnosis, so combined analyses that include Ó The Willi Hennig Society 2012 2 M.A. Bello et al. / Cladistics 1 (2012) 1–29 floral characters alongside molecular data could have gous, a resolved phylogeny that incorporates floral potential to yield resolved phylogenies and morpholog- development characters can provide insight into the ical synapomorphies for suprafamilial groupings. Given nature of this intriguing convergence. For example, the limits of molecular data in reconstructing topologies phylogenetic continuities between non-homologous for rapidly radiating groups (Wortley et al., 2005), we structures with shared function were described by Baum expect combined analyses including morphological data and Donoghue (2002). Here, we use a phylogenetic to be an efficient route to a better resolved and better framework to determine whether the papilionate syn- supported phylogeny, as well as offering insight into drome is phylogenetically continuous within Fabales, floral evolution. even if it is not a synapomorphy and all characters fail Trends in floral evolution within Leguminosae have tests of homology sensu Patterson (1982). Finally, an been the focus of detailed research that can be exploited evolutionary module that Bello et al. (2010) proposed for phylogeny reconstruction (e.g. Tucker, 1984, 1987, for the the keeled flowers of Polygalaceae can be re- 1988, 1989, 1991, 1992, 1996, 1998, 2000a,b, 2001a,b, evaluated by comparing the distribution of its compo- 2002a,b, 2003a,b, 2006; Tucker and Stirton, 1991; nent traits (bracteoles, lateral sepals, lateral petals) in a Tucker and Douglas, 1994; Tucker and Kantz, 1997; phylogenetic context. Prenner and Klitgaard, 2008), but no explicitly phylo- genetic studies have extended this research to other families placed in the order Fabales. A broader study Materials and methods integrating recent data for Quillajaceae, Surianaceae, and Polygalaceae (Bello et al., 2007, 2010) has potential Compiling matrices to test earlier hypotheses regarding evolutionary trends across the order. Quillajaceae and Surianaceae exhibit Morphological data were assembled for 66 morpho- numerous differences in the organization of their repro- logical characters (Appendices 1 and 2) across 75 taxa, ductive whorls, despite their similarity in both inflores- including two outgroups. Scanning electron microscopy cence structure and perianth and gynoecial merosity was used to observe floral characters from Polygalaceae (Bello et al., 2007). On the other hand, Leguminosae and Kramaria and characters were scored from photo- flowers resemble those of Quillajaceae in several traits micrographs (Figs 1 and 2) following the procedure (Bello et al., 2007). described in Bello et al. (2007). Other characters were One interesting morphological phenomenon in Fab- scored from the literature (Appendix 2). Three fruit ales that is highlighted here is the presence of papilionate characters (winged fruit, fruit consistency, and fruit flowers (or ‘‘keeled’’ flowers sensu Westerkamp, 1997) in dehiscence) were included as reproductive characters most species of the two species-rich families, Polygala- related to floral morphology, because gynoecium struc- ceae and Leguminosae. Westerkamp and Weber (1999) ture ultimately determines fruit morphology. A charac- investigated the homology of the papilionate flowers of ter describing the habit was also included, because it was Fabales, comparing mature floral characters in Legu- easily scored for all taxa. Other non-floral characters minosae and Polygalaceae. They concluded that despite were considered but rejected, because it proved impos- functional similarities and a common pentamerous sible to score an adequate sample for all the study taxa. condition, the keeled flowers of these two families are Previously published molecular data were compiled not homologous. Prenner (2004a) made a further for these 75 taxa from two gene regions, matK and rbcL comparison of the morphologies of papilionate flowers (Appendix 1). In cases where it was impossible to of Leguminosae and Polygalaceae, highlighting mor- exactly match morphological and molecular sampling, phological characters shared between the two families DNA data from congeners was used. For some taxa, that could be inherited from a common ancestor and DNA sequences representing congeners were not avail- thus be truly homologous. However, he was cautious in able either, so only morphological data were scored for his conclusions, because the homology of these charac- a subset of the species surveyed here. We analysed three ters was not tested in the context of a phylogeny. matrices with combined data to check the consistency Considerably more data are now available for the of the results using different data sets with different flowers of Polygalaceae (Bello et al., 2010), so the proportions of missing data. The first matrix (matrix A) relationships between papilionate flowers in these two has all 75 taxa included in the morphological survey, families can be further evaluated. Investigation of the whether or not molecular data were available. This morphologies in a phylogenetic context will allow a test matrix, with a total of 3208 characters, has 20 taxa of whether the papilionate flowers represent a conver- without any DNA data, and 25 are represented by just gent (Westerkamp and Weber, 1999) or homologous a single DNA marker (20 with rbcL and five with matK (Prenner, 2004a) syndrome within Fabales. Even if few only). Matrix A includes 24 ingroup species to repre- or none of the characters