systematic botany volume 18 issue 1 1993 [doi 10.2307%2f2419786] peter c. hoch, jorge v. crisci,...

A Cladistic Analysis of the Plant Family OnagraceaeAuthor(s): Peter C. Hoch, Jorge V. Crisci, Hiroshi Tobe and Paul E. BerrySource: Systematic Botany, Vol. 18, No. 1 (Jan. - Mar., 1993), pp. 31-47Published by: American Society of Plant TaxonomistsStable URL: http://www.jstor.org/stable/2419786 .Accessed: 21/03/2013 15:01

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Systematic Botany (1993), 18(1) pp 31-47 ? Copyright 1993 by the American Society of Plant Taxonomists

A Cladistic Analysis of the Plant Family Onagraceae

PETER C. HOCH Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166

JORGE V. CRISCI Laboratorio de Sistematica y Biologia Evolutiva,

Museo de La Plata, 1900 La Plata, Argentina

HIROSHI TOBE Department of Biology, College of Liberal Arts and Sciences,

Kyoto University, Kyoto 606, Japan

PAUL E. BERRY Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166

ABSTRACT. A cladistic analysis of Onagraceae was performed using 17 characters from morphology, anatomy, palynology, embryology, and cytology, with its 16 genera as the terminal taxa, and with several possible outgroups within Myrtales. In the main analysis (all Myrtales as outgroup), seven equally parsimonious cladograms were produced, each with 29 steps and a consistency index of 0.82. A successive weighting procedure was applied, resulting in six cladograms with a consistency index of 0.93. All cladograms share the following nine monophyletic groups: 1) all taxa except Ludwigia; 2) C,rcaea (Fuchsra-Lopezia); 3) Fuchsra-Lopezia; 4) Gayophytum (Eprlobium-Boisduvalia) (Gongylocarpus-Xylonagra-Camissonra(Clarkia(Hauya-Calylophus-Gaura)) (Oenothera-Stenosiphon)); 5) Epilobium-Boisduvalia; 6) Gongylocarpus-Xylonagra-Camissonia(Clarkia(Hauya-Calylophus- Gaura))(Oenothera-Stenosiphon); 7) Clarkia(Hauya-Calylophus-Gaura); 8) Hauya-Calylophus-Gaura; and 9) Oenothera-Stenosiphon. One additional monophyletic group appears after applying the successive weighting procedure: Gayophytum (Eprlobium-Boisduvalra). Results of the cladistic analysis support a sister group relationship of Ludwigia to the rest of the genera. The clade of Crrcaea, Fuchsia, and Lopezia is the sister group of the remaining genera (except Ludwigia), but there is relatively less resolution of the relationships among those genera (the tribes Onagreae, Epilobieae, and Hauyeae). The other main conclusions are that the positions of Hauya and Gayophytum are problematic and not well resolved, and that the tribe Onagreae may be paraphyletic.

Onagraceae are a well-defined family of flow- ering plants, consisting of seven tribes, 16 genera, and approximately 652 species of world- wide distribution (Raven 1979, 1988). The family is unambiguously included in the order Myr- tales (Dahlgren and Thorne 1984; Johnson and Briggs 1984), sharing with all members of the order a number of traits, including a distinctive set of eight embryological characters (Tobe and Raven 1983). Within the order, Onagraceae are highly distinctive, forming a monophyletic group defined by the following synapomorphies: 1) a characteristic 4-nucleate embryo sac (Tobe and Raven 1983); 2) the presence of abundant raphides in the vegetative cells (Carlquist 1961, 1975; Metcalfe and Chalk 1950); 3) the presence of septa dividing the

sporogenous tissue (Tobe and Raven 1986a); 4) "paracrystalline beaded" pollen ektexine (Skvarla et al. 1975, 1976); and 5) viscin threads or ektexinous strands on the proximal pollen wall (Patel et al. 1984; Skvarla et al. 1978).

The family has been studied in close biosys- tematic detail and modern taxonomic revisions are available or in preparation for all species. Leaf, wood, and floral anatomy have been studied extensively; chromosome numbers are known for most taxa; and breeding systems and pollinators, flavonoids, palynology, and embryology have all been investigated for most of the family (references cited below).

One conclusion from these studies has been that most of the genera of the family are quite distinctive; five of the seven tribes are mono-

31


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generic, another includes two genera, and only one includes more than two genera (Table 1). Pollen of Onagraceae has been recognized in the fossil record from strata of Maestrichtian Age (73-65 MYA) at the end of the Cretaceous period (Drugg 1967; Pares Regali et al. 1974a, 1974b), indicating that the family is old enough that the very distinctive genera in the family may represent evolutionary lines that diverged in the remote past and subsequently have evolved separately (Raven 1988).

A major phylogenetic hypothesis within the family is that Ludwigia is the sister group of all other Onagraceae. This was first suggested by Eyde (1977, 1979, 1981), based on the presence in Ludwigia alone of a unique suite of anatomical characters: central vascular bundles in the ovary; massive, highly ovuliferous placentas; ar- chaic nectary position; and 4+ merous peri- anths. Eyde's hypothesis is generally supported by data from chemosystematics (Averett and Ra- ven 1984) and cytology (Kurabayashi et al. 1962; Raven and Tai 1979; Raven 1988). In a study of the 40 N-terminal amino acid residues of the small subunit of ribulose bisphosphate carbox- ylase, Martin and Dowd (1986) found that Lud- wigia has a terminal sequence common to most other plants, including other families of Myr- tales, whereas the other 10 species of Onagra- ceae examined share a highly distinctive sequence, accounting for at least three nucleotide differences. Martin and Dowd's study also dem- onstrated branching of Lopezia, Circaea, and Fuchsia in sequence from the other branch of the family, but did not resolve relationships among the other five genera (in three tribes) included in their study. Crisci et al. (1990) analyzed restriction site variation in rDNA in a limited sample of taxa in Onagraceae; the resulting cladograms did not unambiguously resolve relationship among the taxa tested, although a final bootstrap cladogram from Dollo analysis supported a sister group relationship between Epilobium and Oenothera, another between Fuchsia and Hauya, and one between Fuchsia-Hauya and Circaea. In summary, despite the large amount of information available for the family from these and other studies, the only strongly supported hypothesis is that Lud- wigia is the sister group to the rest of the family. Hypotheses regarding relationships of the other main groups of the family have only weak or conflicting data in their support.

This paper employs principles of phylogenetic systematics to evaluate generic and tribal relationships within the Onagraceae, using a cladistic analysis based on information available from morphology, anatomy, palynology, embryology, and cytology (references to specific studies are cited under "character definition").

MATERIALS AND METHODS

We use the principles of phylogenetic systematics as originally developed by Hennig (1966), who maintained that only strictly monophyletic taxa may be regarded as historical en- tities and that the logical basis for inferring monophyly is to show that the component taxa of a group possess one or more shared, derived character states or synapomorphies. The distribution of synapomorphies is determined by the parsimony criterion (minimizing homoplasy). On the basis of these synapomorphies, taxa are ordered into one or more hierarchical sets rep- resented by branching diagrams.

The 16 genera of Onagraceae are considered the terminal taxa. Clarkia is treated to include Heterogaura (Lewis and Raven 1992), following the convincing molecular analysis by Sytsma and Gottlieb (1986). Table 1 shows the tribal classification, the genera and their acronyms, estimated numbers of species, and geographical distributions. Diagnostic features of each genus are also listed in Table 1; these putative autapomorphies are not included as characters in our analysis because they do not suggest relationships, although several (noted in the Table) are included as terminal states in multi-state characters. Several taxonomically useful characters that proved too homoplasious to be used in this analysis are used in combination to distinguish certain taxa. For example, all species of Ludwigia lack a floral tube, a clearly apomorphous condition within Myrtales and Onagraceae, but so do the seven species of Epilobium sect. Chamae- nerion, an otherwise unrelated group (Raven 1976). Similarly, tubular red flowers (found also in some species each of Fuchsia, Lopezia, and Epilobium) are combined with asymmetrically winged seeds (found also in Hauya, although the homology of these wings may be question- able) to distinguish Xylonagra from the taxa in tribe Onagreae with which it otherwise appears to be related (Munz 1965; Raven 1964, 1988).



TABLE 2. Characters and character states used for cladistic analysis of Onagraceae. All multistate characters (4, 6, 7, 9, 10) are treated as non-additive (unordered).

Character Character states

1. Stipules 0 = present; 1 = absent 2. Starchy pollen 0 = present; 1 = absent 3. Reciprocal translocations 0 = absent; 1 = present 4. Stigma type 0 = undivided; 1 = non-commissural long linear lobes; 2 = non-com-

missural short broad lobes; 3 = commissural lobes 5. Sepal persistence 0 = persistent; 1 = deciduous 6. Ratio stamens/sepals 0 = 2 (or more); 1 = 1; 2 = 1/2 7. Floral merism 0 = 4 and more; 1 = 4; 2 = 2 8. Stigma surface 0 = wet; 1 = dry 9. Histogenesis of outer 0 = subdermal; 1 = mixed, primarily subdermal; 2 = mixed, primarily

integument dermal; 3 = exclusively dermal 10. Sporogenous tissue 0 = no division; 1 = tapetal septa; 2 = parenchymatous septa 11. Pollen monads/tetrads 0 = monads; 1 = tetrads 12. Stylar vasculature 0 = minor stylar bundles; 1 = no minor stylar bundles 13. Ovary vasculature 0 = central vascular supply present; 1 = central vascular supply absent 14. Anther wall development 0 = Basic or Dicot type; 1 = Monocot type 15. Ovule archesporium 0 = 1-celled; 1 = multi-celled 16. Ovule parietal tissue 0 = thin (4-6 cells); 1 = thick (10-25 cells) 17. Early development of inner 0 = not retarded; 1 = retarded

integument

No autapomorphy delimits Camissonia; this could suggest that the genus is paraphyletic, an hypothesis now being assessed (W. L. Wagner, unpubl. data). In the absence of specific alternative hypotheses about the monophyletic units in or involving Camissonia, we include it in the traditional sense (Raven 1969), especially because its general placement in tribe Onagreae is not in dispute. Because of its close relationship with Stenosiphon, Oenothera also lacks an autapomorphy, but the two genera together share a synapomorphic stigma type (cf. character 4); again, this could suggest that Oenothera is paraphyletic, and this possibility is currently being studied. Boisduvalia lacks an autapomorphy, but it shares two synapomorphies with Epilobium; studies in progress on tribe Epilo- bieae may revise the phylogenetic hypotheses about these genera, but they together clearly form a monophyletic clade.

Data from 17 characters were derived from morphology, anatomy, palynology, cytology, and embryology (Table 2). Character polarity was determined by the outgroup comparison method (Humphries and Funk 1984; Maddison et al. 1984; Watrous and Wheeler 1981). Table 3 contains the data matrix used in this analysis.

Selection of an outgroup for Onagraceae is problematical, despite the unequivocal place-

ment of the family in the order Myrtales. In their cladistic analysis of the order, Johnson and Briggs (1984) placed Onagraceae as the sister group of Trapaceae, with the two families as the sister group either of Lythraceae s.l. (including Duabangaceae, Punicaceae, and Sonnerati- aceae) or of all families of Myrtales other than Myrtaceae s.l. (including Heteropyxidaceae and Psiloxylaceae). The branch formed by Onagra- ceae and Trapaceae is supported by one synapomorphy (reduced inflorescence), one reversion (leaf teeth), and six parallel character gains. Dahlgren and Thorne (1984) specifically reject the hypothesis of a close relationship of Ona- graceae with Trapaceae, suggesting instead that Onagraceae diverged from the rest of Myrtales just after Myrtaceae s.l. diverged (i.e., all families of Myrtales other than Myrtaceae as outgroup) or that Onagraceae and Lythraceae form an early branch marked by at least four shared characters (libriform and septate wood fibers, fuchsioid teeth, pinnate petal venation, and fi- brous seed exotegmen). In their analysis of amino acid sequences in Onagraceae and Myrtales, Martin and Dowd (1986) concluded that Ona- graceae form the sister group to all other families of the order that they studied (Lythraceae, Combretaceae, Melastomataceae, and Myrta- ceae).



TABLE 3. Data matrix used for cladistic analysis of Onagraceae, using the rest of the order Myrtales as outgroup. Acronyms as in Table 1; characters numbered as in Table 2. All multistate characters are treated as non-additive. a Alternate state coded for Trapaceae; b alternate state coded for Lythraceae as outgroups.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

OUT ?/Oa ? 0 0 0 oi/a oi/a ? ? 0 0 0 0 O/?a ?/Ob 0 0/?b LUD 0 0 0 0 0 ? 0 0 3 1 ? 0 0 0 1 0 0 FUC 0 1 0 0 1 0 1 0 0 1 0 1 1 0 0 0 0 LOP 0 1 0 0 1 2 1 0 0 1 0 1 1 0 0 0 0 CIR 0 0 0 0 1 1 2 0 0 1 0 1 1 0 0 0 0 HAU 0 0 0 0 1 0 1 0 2 2 0 1 1 1 0 1 0 GON 1 0 ? 0 1 0 1 0 3 1 0 1 1 0 0 1 0 GAY 1 0 1 0 1 0 1 0 3 1 0 1 1 0 0 0 1 XYL 1 0 ? 0 1 0 1 0 3 1 0 1 1 0 0 1 0 CAM 1 0 1 0 1 0 1 0 3 1 0 1 1 0 0 1 0 CAL 1 0 1 0 1 0 1 0 2 2 0 1 1 1 0 1 0 GAU 1 0 1 2 1 0 1 0 2 2 0 1 1 1 0 1 0 OEN 1 0 1 1 1 0 1 0 1 1 0 1 1 0 0 1 0 STE 1 0 1 1 1 0 1 0 1 1 0 1 1 0 0 1 0 CLA 1 0 1 3 1 0 1 1 3 2 0 1 1 1 0 1 0 EPI 1 0 0 3 1 0 1 1 3 1 1 1 1 0 0 0 1 BOI 1 0 0 3 1 0 1 1 3 1 1 1 1 0 0 0 1

In summary, there are at least four hypotheses for the outgroup of Onagraceae: 1) Tra- paceae alone, 2) Lythraceae s.l. alone, 3) all Myrtales except Myrtaceae s.l., and 4) all Myr- tales. For the characters in this analysis, the outgroup coding for Myrtales with (4) and without Myrtaceae (3) is the same, so we combined these two hypotheses and used all Myrtales. We repeated the analysis including all three outgroups simultaneously; to do this we added four characters to the data matrix that are the synapomorphies for Onagraceae mentioned above. The outgroup hypotheses produce differences in the polarization of some characters (Table 3). Because the topologies for the ingroup were essentially the same for each outgroup, we present the complete results using all Myrtales as the outgroup (abbreviated as OUT for the analysis), and we discuss the results of the other outgroup options.

Character Definition and Codification. 1) STIPULES. These are variable in size, often mi- nute and/or deciduous, and sometimes absent in Myrtales, including some Lythraceae, but are entirely absent in 11 of the 16 genera of Ona- graceae (Keating 1982; Munz 1965).

2) STARCHY POLLEN. Baker and Baker (1979, 1982) found that genera of Onagraceae can be characterized as having either starchy or starchless pollen at anthesis. In all Onagraceae, starch is accumulated in early development; in those

taxa with starchless pollen, the starch is later converted into lipids (Baker and Baker 1982). Lythraceae are mixed for this character, all Myr- taceae and Melastomataceae tested are starchless, and Trapaceae are untested (Baker and Ba- ker 1979). Although Baker and Baker (1982) suggested that the ancestor of Onagraceae had starchless pollen, because of the mixed condition of this character in the outgroups, we code the outgroup condition as undefined.

3) RECIPROCAL TRANSLOCATION HETEROZY- GOSITY. Reciprocal translocations have been reported in many genera of Onagraceae (summarized in Raven 1979), but not in any other member of Myrtales. Minor translocation differences characterize species or groups of species in Circaea (Seavey and Boufford 1983), Bois- duvalia (Seavey 1977), and Epilobium (summarized in Seavey and Raven 1978), but in these genera translocations rarely if ever occur within species and are not a regular part of the reproductive biology of any species. By contrast, in tribe Onagreae, reciprocal translocations occur between and within populations, and at least four genera (Calylophus, Gaura, Gayophytum, and Oe- nothera) include at least some permanent structural heterozygotes (Raven 1979). This chromosomal behavior is a complex, characteristic feature in Onagreae and may involve derived structural attributes of the chromosomes (Kur- abayashi et al. 1962; Raven 1979). There are in-



sufficient data to score Gongylocarpus or Xylo- nagra for this character. We have coded the character as presence or absence of infraspecific translocation heterozygosity.

4) STIGMA TYPE. Undivided stigmas characterize most genera of Onagraceae and all other Myrtalean families. Two distinct types of divided stigmas are found within the family (Eyde 1982): non-commissural (receptive around the entire surface of the lobes; all species of Oeno- thera and Stenosiphon with long linear lobes differ somewhat from Gaura, which has short broad lobes) and commissural (receptive only on the flattened adaxial surface of the lobes; all species of Clarkia, and some species each of Epilobium and Boisduvalia). Even though the latter two genera are mixed for this character (those taxa without the divided commissural type have entire stigmas), divided commissural stigmas characterize all species considered to be primitive in both genera (Raven 1976; Hoch and Crisci, unpubl. data), and entire stigmas appear to have evolved repeatedly and secondarily in association with autogamy (Raven 1976; Raven and Raven 1976). There is no evidence to suggest that either type of divided stigma developed from the other; we treat this character as unordered.

5) SEPAL PERSISTENCE. Sepals are persistent in most members of Myrtales, including Lythra- ceae and Trapaceae, and in Ludwigia; in all other Onagraceae, sepals fall off after anthesis.

6) RATIO OF STAMENS TO SEPALS. There are twice as many stamens as sepals in most Myr- tales (or sometimes more than twice as many) and most Onagraceae. This ratio is reduced to 1 in Circaea and Trapaceae, and to 1/2 in Lopezia. Ludwigia has ratios of both 2 and 1 and is scored as undefined. The character is unordered because stamen reduction occurs non-homolo- gously in Circaea and Lopezia (Boufford 1982).

7) FLORAL MERISM. In Ludwigia and most Myrtales, perianth parts are in multiples of 4 and more, often variable within genera. Tra- paceae and most other genera of Onagraceae have strictly 4-merous flowers, whereas those of Circaea are 2-merous. In the absence of a specific hypothesis about the evolution of this character, we treat it as unordered.

8) STIGMA SURFACE. Onagraceae constitute one of relatively few families in which variation has been found in structural and physio- logical features of the receptive surface of the

stigma (Heslop-Harrison 1990; Heslop-Harri- son and Shivanna 1977). Clarkia, Epilobium and Boisduvalia have dry, papillate receptive surfaces, whereas the receptive surfaces in other genera are wet with stigma surface secretions (Heslop-Harrison 1990). Combretaceae and Me- lastomataceae have wet stigmas, but Myrtaceae and Lythraceae are mixed for this character, although the latter has predominantly dry stigmas; Trapaceae have not been tested. Because all Myrtalean groups tested have at least some wet stigmas, that condition is likely to be primitive for the order. However, the more conser- vative coding of the outgroup of Onagraceae as undefined gives the same tree topologies for our data matrix.

9) HISTOGENESIS OF THE OUTER INTEGU- MENT. Four different types of developmental mode of the outer integument (oi) were de- tected by Tobe and Raven (1985) and found to be consistent within genera: 1) oi of subdermal origin, with derivatives of subdermal initials reaching the tip of the mature oi in the ovule primordium (Circaea, Fuchsia, and Lope- zia); 2) oi of both subdermal and dermal origin, with derivatives of subdermal initials extending more than half the length of the mature oi (but not to the top; Oenothera and Stenosi- phon); 3) similar to 2) but with derivatives of subdermal initials extending less than half the length of the mature oi (Hauya, Calylophus, and Gaura); and 4) oi of exclusively dermal origin (remaining eight genera of Onagraceae). Bou- man (1984) postulated that the integument of entirely subdermal origin is primitive in angiosperms as a whole, and that of dermal origin advanced. Although Tobe and Raven (1985) suggested that these character states form an ordered series from 0 (subdermal only) to 3 (dermal only), we have treated them as unordered because the basis of these character trans- formations is not clear. There are insufficient data to assign a character state to the Myrtalean outgroups, so they are coded as undefined.

10) SPOROGENOUS TISSUE. The microsporoge- nous tissue of at least some species of all 16 genera of Onagraceae is divided into packets by septa composed of tapetum and/or paren- chyma (Raven 1964; Tobe and Raven 1986a). This widespread presence of septa is a synapomorphy for Onagraceae because it occurs no- where else in Myrtales except in the isolated family Oliniaceae (Tobe and Raven 1984). Par-



enchymatous septa have a more elaborate structure than do tapetal septa; they have been found in all taxa examined of Calylophus, Clarkia, Gaura, and Hauya, and in two unrelated and otherwise advanced species of Ludwigia (Tobe and Raven 1986a). Tobe and Raven suggested that this feature evolved independently (perhaps two times) in Ludwigia, but that its occurrence in the other four genera is a synapomorphy. They also suggested that the absence of tapetal septa in some taxa or samples may only be apparent (they dis- integrate early, prior to anther dehiscence, and are not easily observed in all samples) or is due to extreme reduction of the anthers (in some annuals), and therefore, represents a secondary loss. We have scored for presence of tapetal (1) or parenchymatous (2) septa if any members of a genus have that state, except in the case of Ludwigia, which we have scored only for presence of tapetal septa. Even though Tobe and Raven (1986a) suggested that parenchymatous septa are more advanced than tapetal ones, we treat this character as unordered.

11) POLLEN MONADS/TETRADS. In most genera of Onagraceae and in all Myrtalean outgroups, pollen is released in monads. However, pollen is released in tetrads with clear bridge connections between the grains in all species of Boisduvalia and all of Epilobium with the ex- ception of section Chamaenerion and some populations of E. brachycarpum C. Presl (Skvarla et al. 1975). In the species of Ludwigia where tetrads occur, the mechanism of tetrad cohesion differs from that in Epilobieae (Skvarla et al. 1975). Also, the distribution of tetrads/polyads in Ludwigia is complex: most sections shed their pollen as tetrads, several (including the large, possibly basal sect. Myrtocarpus) shed them as polyads, two (including sect. Oligospermum) shed them as monads, and several sections are mixed (Praglowski et al. 1983; Skvarla et al. 1975). Fi- nally, tetrads occur in two species of Camissonia, but they lack bridge connections between the grains, and seem certain to have arisen independently (Praglowski et al. 1987; Skvarla et al. 1975). We have scored the Epilobieae for presence of tetrads, Ludwigia as mixed, and Camis- sonia (and other genera) as absent.

12) STYLAR VASCULATURE. In a study of the floral anatomy of Onagraceae, Eyde (1981) reported the presence of minor stylar vascular bundles in all species examined of Ludwigia, not- ing that this also characterizes other Myrtalean

families. No other genera of Onagraceae have these stylar bundles, and their loss is considered a derived condition (Eyde 1982).

13) OVARY VASCULATURE. Most angiosperms and all families of Myrtales have a central (axile) vascular supply to the ovary. Eyde (1981, 1982) found that all Onagraceae have a derived "transseptal" vascular supply, which also occurs variously in Myrtaceae, Oliniaceae, Puni- caceae, and Rhynchocalycaceae (Graham 1984; Schmid 1984). Ludwigia has both central and transseptal vascular routes to the ovary, whereas the remaining genera of Onagraceae have lost the central route (Eyde 1981).

14) ANTHER WALL DEVELOPMENT. Four types of histogenetic origin of the middle layers in anther wall development are known in angiosperms: Basic, Dicotyledonous, Monocotyle- donous, and Reduced (Davis 1966, p. 10). The Basic type, in which the middle layers share a common origin with both the endothecium and tapetum, characterizes most Onagraceae. Clark- ia, Calylophus, Gaura, and Hauya, on the other hand, have the Monocotyledonous type (Tobe and Raven, unpubl. data). Anther wall development is not known for many Myrtales, although Myrtaceae and most Combretaceae have the Basic type, and Sonneratiaceae and at least one genus of Lythraceae have the Dicotyledon- ous type; the type in Trapaceae is not known (Tobe and Raven 1983).

15) OVULE ARCHESPORIUM. Differentiation of parietal and primary sporogenous cells occurs in the archesporium of the ovule; this archesporium is one-celled in Ludwigia (Tobe and Ra- ven 1986b), but multi-celled in the rest of the family (Tobe and Raven, unpubl. data). Lythra- ceae have only multi-celled archesporia. Tra- paceae and other Myrtales have both one-celled and multi-celled archesporia (Tobe and Raven 1983); these outgroups are coded as undefined.

16) OVULE PARIETAL TISSUE. The parietal tissue, which is derived from the primary parietal cell lying above the megaspores, is usually 4-6 cells thick in Ludwigia (Tobe and Raven 1983), Circaea, Lopezia, Fuchsia, Gayophytum, Epilobium, and Boisduvalia, and in other Myrtales including Lythraceae and Trapaceae, but is remarkably thick (10-25 cells thick) in the rest of Onagra- ceae (Tobe and Raven, unpubl. data).

17) EARLY DEVELOPMENT OF INNER INTEGUMENT. In Gayophytum, Epilobium, and Boisduvalia, the early development of the inner



integument is retarded so that the inner integument becomes much shorter than the outer integument. In other genera of Onagraceae and other families of Myrtales except Lythraceae (condition unknown), the inner integument is as long as, or longer than, the outer integument in early development stages (Tobe and Raven, unpubl. data).

Five of the 17 characters (4, 6, 7, 9, and 10) have more than two character states. As discussed under each character, none of them is treated as additive (i.e., the number of steps between two states is taken to be the absolute value of their arithmetic difference; equivalent to "ordered" in other analyses).

The data matrix was analyzed using a Wagner parsimony algorithm (Farris 1970; Kluge and Farris 1969) from Farris's phylogenetic package, Hennig86 (version 1.5; Farris 1988; Platnick 1989), run on a CompuAdd 320sc computer applying the implicit enumeration option for cal- culating trees. We also used the successive weighting procedure in Hennig86, which cal- culates weights from the best fits to the most parsimonious trees, using rescaled consistencies (rc), which are the products of the character consistency (c) and the character retention index (r). The product is scaled to lie in the range 0-10. The weighting procedure is repeated on successively produced trees until the trees no longer change (Farris 1989). Strict consensus trees were calculated using the "nelsen" option in Hennig86 every time an analysis yielded more than one most-parsimonious tree (Page 1989).

RESULTS

Using Myrtales as the outgroup, seven equally parsimonious cladograms were generated by our data matrix (Fig. 1A-G). All have 29 steps and a consistency index of 0.82. The strict consensus tree of the seven cladograms (Fig. 1H) shows that nine monophyletic groups appear in all of them, listed with their synapomorphies: 1) all taxa except LUD (deciduous sepals, merous condition never more than 4, absence of minor stylar bundles, absence of central ovular vascular supply, and ovule archesporium 1-celled); 2) CIR(FUC-LOP) (outer integument of subdermal origin); 3) FUC-LOP (starchless pollen); 4) GAY(EPI-BOI) (GON- XYL-CAM(CLA(HAU-CAL-GAU)) (OEN-STE)) [absence of stipules (with reversion in HAU),

presence of reciprocal translocations (with re- versions in HAU and in EPI-BOI)]; 5) EPI-BOI [pollen in tetrads; commissural stigma lobes (parallel with CLA); dry papillate stigma surface (parallel with CLA); inner integument development retarded, (parallel with GAY)]; 6) GON-XYL-CAM(CLA(HAU-CAL-GAU)) (OEN- STE) (ovule parietal tissue thick); 7) CLA(HAU- CAL-GAU) (parenchymatous septa; anther wall development Monocot type); 8) HAU-CAL- GAU (outer integument of mixed origin, primarily dermal); and 9) OEN-STE (non-commissural linear stigma lobes; outer integument of mixed origin, primarily subdermal).

The configuration for the base of the seven cladograms is identical in the relationships of the taxa LUD, CIR, LOP, FUC. On the branch with the remaining taxa, six trees present GAY(EPI-BOI) as a monophyletic group that is the sister group of the rest of the taxa (Fig. 1B- G). In the seventh tree, EPI-BOI form the sister group of the rest of the taxa (Fig. 1A). Among the six trees with the GAY(EPI-BOI) hypothesis, the variation concerns the relative disposition of GON and XYL relative to CAM(CLA(HAU- CAL-GAU)) (OEN-STE); this is caused by the unknown states for GON and XYL in character 3.

When the successive weighting procedure was applied, six minimum-length trees resulted after the third round of weighting, with length 216, and the consistency index improved to 0.93 (note that the high value for the length is a function of the weight being scaled up to a value of 10). The values of the range and number of steps, consistency index (c), retention index (r), and weight (rc x 10) for each character are listed in Table 4. The strict consensus tree (Fig. 2) of the six weighted trees has the same length (216) as the weighted trees and is identical to one of them. In this case, we use only the strict consensus tree. The reason for this is that the implicit enumeration option of Hennig86 regards trees as distinct if there is any possible character interpretation that will distinguish them. If the strict consensus tree is not longer than the several trees from this option, this shows that the extra branches in the latter trees, although possibly supported, are not necessary to account for the characters. Ten monophyletic groups appear in the consensus tree (Fig. 2), including the same nine groups that appear in the original seven trees. The ad-



out out lud lud

loplo fucfu bicir boi

epi~~~~~~~~~~~~~~~~~~p epi a gay gon gon

xyl xyl cam cam

A ~~~~~oen oe ste B ste cla otcla _ out L { i hau H _ out L { i hau out -calluca

lud cgau l p gau lop

gau ucbo

fuc boili p d r epi gay gon gon xyl xyl cam cam oen o-en D ste

ste cla cia ~~~~~~~~~~~~~~~hau

hau cal cal out gau gau lop out fuc

lud cir boi lop epi fuc boi

cr epi xyl gay xyl F gon

cam~~~~~~~~~~a ogon oen

ciam E - cam ~~oen rste l ste clau

out hau lud Lcal lud calloga

lop gau fuc fuc boi cir

cir epi gay r | gay - epi

gon boi xyl gon cam

oen y G s ste -cam oen L cla

ha F-ste cia~~~~~~~~~~~~~~~~l cal hau gau cal

-gau



ditional monophyletic group is GAY(EPI-BOIS) (inner integument development retarded). Af- ter the procedure, the maximum weight of 10 was assigned to characters 2, 5-7, 9-17. A weight of 5 was assigned to character 4; a weight of 3 to character 1; and a weight of 2 to characters 3 and 8. The character state changes are shown in Figure 2.

Using the alternative outgroup hypothesis of Lythraceae, the same seven most parsimonious trees, six weighted trees, and consensus trees result, all having the same lengths and consistencies as those produced with Myrtales as outgroup. Including Myrtales, Lythraceae, and Trapaceae (in that order) in a single analysis produced trees with exactly the same topologies for Onagraceae as those produced by using Myrtales or Lythraceae alone as outgroups. The analysis with Trapaceae as outgroup produces 14 trees (length 30, consistency index 0.80), seven of which have identical topologies to those produced by using Myrtales or Lythraceae as the outgroup (Fig. 3A). The other seven trees place CIR as the sister group to the rest of the genera except LUD (Fig. 3B); the relationships of the other genera are identical to those in the first seven trees. The successive weighting procedure produces 12 trees (length 228, consistency index 0.89), six with the same topologies as the six from the Myrtales outgroup analysis, and six with the same altered position for CIR.

DISCUSSION

The strongest result of this analysis is the unequivocal sister group relationship of Lud- wigia to the rest of the genera in the Onagraceae, with five synapomorphies in support of the relationship. This agrees with the molecular data of Martin and Dowd (1986), who found that nine genera of Onagraceae, but not Ludwigia, shared a unique N-terminal sequence of the ribulose bisphosphate carboxylose small subunit.

Within the non-Ludwigia branch of the family, our results are also clear in placing the clade of Circaea, Fuchsia, and Lopezia as the sister group of the remaining genera (except with Trapaceae as outgroup, as discussed below). This relation-

TABLE 4. Character consistencies (c) and retention indices (r) as the best fits on the seven equally parsimonious trees from Hennig86, and used to calculate weights for phylogenetic analysis of Onagraceae. Characters numbered as in Table 2. Final weights were obtained after the third round of the successive weighting procedure in Hennig86. Weights were truncated to integers.

Consis- Reten- Weight Char- Range Number tency tion (rc x Final acter of steps of steps index (c) index (r) 10) weight

1 1 2 0.5 0.75 3 3 2 1 1 1 1 10 10 3 1 2 0.50 0.83 4 2 4 3 4 0.75 0.66 5 5 5 1 1 1 1 10 10 6 2 2 1 1 10 10 7 2 2 1 1 10 10 8 1 2 0.5 0.5 2 2 9 3 3 1 1 10 10

10 2 2 1 1 10 10 11 1 1 1 1 10 10 12 1 1 1 1 10 10 13 1 1 1 1 10 10 14 1 1 1 1 10 10 15 1 1 1 1 10 10 16 1 1 1 1 10 10 17 1 1 1 1 10 10

ship is also consistent with the results of Martin and Dowd (1986), although that study showed Lopezia, Circaea, and Fuchsia in sequence near the base of the non-Ludwigia branch, not as a monophyletic sub-branch as in our results. The results of both our study and that of Martin and Dowd differ from Raven's (1988) interpretation of generic relationships only in that he included Hauya with Lopezia, Circaea, and Fuchsia, as the more generalized members of "the second evolutionary line of Onagraceae" (i.e., excluding Ludwigia), whereas Hauya here forms a clade with Onagreae. However, results from a survey of rDNA restriction site variation in some genera of Onagraceae (Crisci et al. 1990) placed Hauya on a branch with Fuchsia and Circaea (Lo- pezia was not included in the survey), and not on a branch with Oenothera (the only genus of Onagreae included); this is compatible with Ra-

FIG. 1. A-G. The seven most parsimonious cladograms of Onagraceae taxa, using all Myrtales as outgroup (length = 29, consistency index = 0.82). H. Strict consensus cladogram derived from the seven most parsimonious cladograms. Refer to Table 1 for acronyms.



OUT TRIBES

/sL U~~~~LD I

// 5 e p ;t/ L O~~~~~~LP IV

10(1) ~ ~ Tapetalrcles antr s a 9) O ) S s d oStamens/sepals / / =1 ~~~~~~~~~7(2 CIR 11

t / / ~~~~~~~~~~~Flowers 2-merous I10(1) Tapetal /

anther septa \ (0) 0.1. subdermal ^Zw P

5(1) Sepals deciduou) /EPI)Pleinerd l 7(1) Flowers 4-merous 8(1) Stigma dry VI\

12(1) Minor stylar 4(3) Stigma commisural BOI bundles absent 3(0) Reciprocal

13(1) Central ovary translocationspabsent vasculature absent \, / /

15(0) Ovule archesporium 1-celled GAY

1 (I1) Stipules absent

\^ /7(117) I.l. early GON 3(1) Reciprocal translocations present development retarded

16(1) Ovule parietal tissue thick t Y

- ~~~~~CAM 4(1) Stigma non-commisural

\ lobes linear

10(2)Parenchymatous anther septa 3 ()01 rmrl

u pbdermarl STE VI 14(1) Anther wall development Monocot type t ()Sim

commisural OEN \ $ ~~8(1) Stigma

9(2) O.l primarily dermal 4(2) Stigma CLA

norn-commisural


Trapaceae Trapaceae

LUD FUC LUD

LOP - CIR CIR FUC

LOP

A B ------x x

FIG. 3. Two alternative topologies for the bases of the cladograms generated when Trapaceae was used as outgroup for Onagraceae. A. Base of seven of the 14 trees, with identical topologies to those in Fig. 1A- G. B. Base of remaining seven trees, with alternative position for Ctrcaea; remainder of the trees ("x" in figure) also identical to those in Fig. 1A-G.

ven (1988) and also with recent analysis of rRNA sequences (Bult and Zimmer 1993).

Excluding Ludwigia and the clade of Circaea, Lopezia, and Fuchsia, the remaining 12 genera of the family (tribes Onagreae, Epilobieae, and Hauyeae) form a monophyletic group in all trees, a result that is congruent with the results of Martin and Dowd (1986), although Martin and Dowd examined only three of nine genera of Onagreae. Except for the placement of Hauya in this clade, our results also agree with those of Raven (1988), Crisci et al. (1990), and Bult and Zimmer (1992). Neither our results nor those of these other studies are able to resolve fully the relationships of the main lineages of Hauya, Epi- lobieae and Onagreae. Analysis of the combined data sets for Onagraceae may help to resolve these relationships.

Two pairs of genera (Oenothera-Stenosiphon and Epilobium-Boisduvalia) are coded identically for the characters used in this analysis, so their relationships are not addressed here. The close relationships of these genera have never been challenged in previous taxonomic treatments (Munz 1965; Raven 1976, 1988), but new anal-

yses are in progress to elucidate their relative phylogenies.

All members of Onagreae and Hauya form a monophyletic group in only one of the seven most-parsimonious trees (Fig. 1A); that clade is absent in the other trees and in all weighted trees, where instead Gayophytum forms a branch with Epilobium-Boisduvalia. This latter grouping, supported by one synapomorphy (inner integument development retarded), and one that ex- cludes Gayophytum from the Onagreae branch (ovule parietal tissue thick), is unexpected, and is contradicted in particular by reciprocal translocations (character 3), a synapomorphy for On- agreae that is sufficiently complex to argue against homoplasious evolution (Raven 1979, 1988). Chromosome number, which was not used in the cladistic analysis (see below), also supports placement of Gayophytum (x = 7) in Onagreae (all genera x = 7, except Gongylocar- pus), rather than with Epilobieae (x = 9). Nei- ther of the embryological characters has been studied very widely within the family. The position of Gayophytum, a small genus of very reduced annual plants (Lewis and Szweykowski

FIG. 2. The most parsimonious cladogram (see text) found after applying the successive weighting procedure. Most autapomorphies for genera and most synapomorphies for Onagraceae are not included; see text for details. Character state changes are superimposed on cladogram; single lines = synapomorphies; double lines = homoplasies (parallel or convergent evolution), X = reversals. Refer to Table 1 for acronyms and for names of tribes in current classification, indicated by numbers in right column. Abbreviations: I.I. = inner integument, O.I. = outer integument.



1964), is critical to the interpretation of tribe Onagreae and, therefore, should be a focal point of further phylogenetic research.

A branch including Clarkia, Gaura, Calylophus, and Hauya is supported by two additional embryological characters, and a branch with the latter three genera by another character. Except for the position of Hauya, this phylogeny is close to the traditional view of these genera (Munz 1965; Raven 1988). Hauya lacks the two synapomorphies (character 1, stipules absent, and character 2, reciprocal translocation heterozygosity present) that otherwise mark all taxa of Ona- greae; it (x = 10) differs from all Onagreae (x = 7, except Gongylocarpus with n = 11) in chromosome number (Raven 1979); and it groups with Fuchsia and Circaea, not Onagreae, based on nucleic acid analysis (Bult and Zimmer 1993; Crisci et al. 1990; Sytsma et al. 1991).

Our results suggest that the tribe Onagreae is paraphyletic because its genera never form a monophyletic group in any of our trees; Hauya always appears within that branch, and Gayo- phytum is more closely linked to Epilobieae than to other Onagreae in most trees. However, the molecular data just mentioned do not support a close relationship between Hauya and Ona- greae; Gayophytum has yet to be included in these studies. Until it is possible to determine which characters are homoplasious, it may be premature to consider Onagreae to be paraphyletic.

The fact that identical trees are produced using Myrtales (with or without Myrtaceae) or Lythraceae as outgroup, and that using Trapa- ceae gives only one small change, suggests that the resulting ingroup phylogeny is quite stable and robust. Running the three alternative outgroups together also gives the same ingroup topology. The variant position of Circaea in the Trapaceae analysis, because of the presence in those two taxa of a stamen/sepal ratio of 1 (character 6), is not supported by most other analyses of the family, although some of the trees (but not the bootstrap majority-rule consensus) generated by rDNA restriction site variation (Crisci et al. 1990) show a similar near-basal position for Circaea.

Despite the large amount of systematic data available for the family, we were able to gen- erate only 17 phylogenetically informative characters. The non-informative characters that were not used in this study fall into three cat-

egories: 1) autapomorphies for particular genera (e.g., hooked hairs on indehiscent fruits of Circaea, comose seeds of Epilobium, fleshy berries in Fuchsia, etc.; see Table 1); 2) synapomorphies for the whole family (at least five, discussed in the introduction but mostly not included in the data matrix); and 3) characters for which much of the variation occurs within genera, e.g., leaf histology characters such as mesophyll differentiation or lamina structure (Keating 1982), and viscin pollen thread ultra- structure (Skvarla et al. 1978).

Previous analyses of the generic and tribal relationships of Onagraceae by Raven (1979, 1988) used two characters that we did not include in our cladistic analysis. One, the presence of interxylary phloem (Carlquist 1975, 1977), was proposed as an advanced character state in Onagreae, Epilobieae, and Lopezia, with its absence an apparent plesiomorphy in Lud- wigia, Fuchsia, Circaea, and Hauya. However, interxylary phloem is also absent in some genera of Onagreae and Epilobieae, such as Clarkia, Gayophytum, and Boisduvalia (Carlquist 1975, 1982); this may represent a secondary loss, however, as these are all annual plants where the stems are too young to be able to develop interxylary phloem. Carlquist (1982) also reported interxylary phloem in a species of Ludwigia. The overall analysis now suggests that the presence or absence of interxylary phloem has a strong ecological component (possibly related to drought tolerance), which limits its use as an informative phylogenetic character.

Raven also used information on chromosome numbers in his proposed phylogeny. Myrtales are extremely variable in this character, with possible base numbers of x = 11 in Myrtaceae, x = 8 in Lythraceae, and x = 12 in Trapaceae, but most exhibit extreme infra-familial variation (Raven 1975). Raven (1964, 1979) considered x = 11, found in Circaea, Fuchsia, Lopezia, and Gongylocarpus, as the plesiomorphic base number for the family, and suggested that x = 7 in all Onagreae except Gongylocarpus was a major synapomorphy to define the tribe, together with presence of reciprocal translocations and a specialized chromosome morphology (Kurabayashi et al. 1962). Other genera of Onagraceae have autapomorphic chromosome numbers (Ludwigia, x = 8; Hauya, x = 10); Epi- lobium and Boisduvalia have a probable base number of x = 9 (Raven 1976), but with a com-


1993] HOCH ET AL ONAGRACEAE 45

plex development of aneuploidy and polyploi- dy such that only a single species in the tribe now has n = 9. Lopezia and Clarkia also have a complex series of aneuploid chromosome numbers. We repeated our entire analysis adding a character for chromosome number, with outgroups undefined, and assigned an unordered series of states from 0 to 4 (x = 11 to 7) to the genera. This results in 19 most-parsimonious trees (length 34, consistency index still 0.82) that show less resolution in the branch with Onagreae, Epilobieae, and Hauya because the position of Gongylocarpus is now less certain, but with no change in the base of the cladograms nor in the terminal branches (Epilobium-Bois- duvalia, Oenothera-Stenosiphon, and Clarkia- [Hauya-Calylophus-Gaura]).

Raven (1979, 1988) used evidence regarding chromosome structure along with that regarding numbers to support his proposed phylogenies. Kurabayashi et al. (1962) reported that all members of Onagreae and Hauya have characteristic subequal metacentric chromosomes, of very different morphology than other tribes of the family. However, Tanaka et al. (1988) dis- tinguished two types of chromosome morphology among the genera of Onagreae, and placed Oenothera and Clarkia with Hauya in one group, and Gongylocarpus and Gaura with Epilobium in a second one. These conflicting data suggest that chromosome morphology, though sugges- tive, is not yet a reliable phylogenetic character in Onagraceae. In summary, we feel that chromosome numbers alone add little to the resolution of the phylogeny of Onagraceae; additional cytomorphological information, when coupled with data on chromosome numbers, may provide valuable characters in the future.

ACKNOWLEDGMENTS. This study was supported by grants from the National Science Foundation, most recently DEB-8906848, and the John D. and Catherine T. MacArthur Foundation to Peter H. Raven. We are grateful to Dr. Raven for his continuous encourage- ment and support and a thorough review of the manuscript. Several anonymous reviewers and the editor made very useful comments on the manuscript, for which we are grateful. We also thank Gloria Hoch for typing the manuscript.

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Article Contentsp. 31p. 32p. 33p. 34p. 35p. 36p. 37p. 38p. 39p. 40p. 41p. 42p. 43p. 44p. 45p. 46p. 47

Issue Table of ContentsSystematic Botany, Vol. 18, No. 1 (Jan. - Mar., 1993), pp. 1-174Front Matter [pp. ]Albert Charles Smith-Recipient of the 1992 Asa Gray Award [pp. 1-5]Chloroplast DNA Phylogenetic Studies in New World Phaseolinae (Leguminosae: Papilionoideae: Phaseoleae) [pp. 6-17]Allozyme Diversity and Genetic Structure in Southern Appalachian Populations of Poke Milkweed, Asclepias exaltata [pp. 18-30]A Cladistic Analysis of the Plant Family Onagraceae [pp. 31-47]Nuclear Ribosomal RNA Sequences for Inferring Tribal Relationships Within Onagraceae [pp. 48-63]Vanroyenella: A New Genus of Podostemaceae from Jalisco, Mexico [pp. 64-67]The Phylogeny and Biogeography of Nyssa (Cornaceae) [pp. 68-79]The South American Species of Arthrostylidium (Poaceae: Bambusoideae: Bambuseae) [pp. 80-99]Phylogenetic Implications of Pollen Morphology in Tribe Ajugeae (Labiatae) [pp. 100-122]The California Population of Agaricus bisporus Comprises at Least Two Ancestral Elements [pp. 123-136]A Re-Evaluation of the Horkelia bolanderi (Rosaceae) Complex, with the New Species Horkelia yadonii [pp. 137-144]A Simple Method to Test Genetic Allelism in Nearly Sterile Interspecific Plant Hybrids [pp. 145-149]Isozymic and Chromosomal Evidence for the Allotetraploid Origin of Gymnocarpium dryopteris (Dryopteridaceae) [pp. 150-172]ReviewReview: untitled [pp. 173]

Back Matter [pp. ]

systematic botany volume 18 issue 1 1993 [doi 10.2307%2f2419786] peter c. hoch, jorge v. crisci,...

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