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Systematics and leaf architecture of the Gunneraceae.

V. Discussion

A. EVOLUTIONARY TRENDS

Gunnera appears to have undergone a large amount of morphological evolution in its leaves and growth habit, while its fruit and flower morphology have remained largely conservative. The basal position of G herteri is supported by its incipient polystely, with three steles in the stems reported by Mattfeld (1933) and four steles in young stems becoming a complete ring in mature specimens examined by Wilkinson (2000). Other small-leafed species are mildly polystelic, as are those of the subgenera Milligania and Misandra (Batham, 1943; Wilkinson, 1998, 2000). Larger species have many steles; e.g., 59 in G. perpensa and hundreds in species of the subgenus Panke (Batham, 1943; Wilkinson 1998, 2000). Our analyses suggest that ancestral Gunnera was a small, sympodially branching, cauline herb, producing axes in the axils of its leaves, lacking stolons, and with isophyllous, opposite leaves. Leaves were low rank, were ovate with a rounded and crenate apex, had a decurrent base with three distinct veins in the petiole, and had reticulate, palinactinodromous primary venation. They had radially elongated, irregular, shared areoles lacking freely ending veinlets. Leaf tissue probably contained druses. Many of these characters may be plesiomorphies shared with the ancestor of herbaceous Saxifragaceae (Figs. 15, 16, 18).

[FIGURE 18 OMITTED]

Gunnera evolved by the acquisition of a number of important apomorphies, such as the development of a physiologically complex intracellular symbiosis with Nostoc cyanobacteria (cf. Bergman et al., 1992) and the production of paniculate, anemophilous infloresences with unisexual male flowers apically, and female or hermaphroditic flowers basally. The primitively microreticulate, tricolpate pollen of basal Saxifragaceae developed the bulging mesocolpia distinctive of Gunnera (cr. Praglowski, 1970; Jarzen, 1980).

From this stock the subgenus Gunnera evolved unicellular trichomes, reniform leaves with bases becoming lobate, a "trichotomous" midvein, moderate-sized primaries, reticulate orthogonal tertiaries, teeth with admedial veins of a lower order than the principal vein, and secondaries originating at increasingly obtuse angles apically. The descendent lineage is also united in having larger pollen. This clade diverged into two lineages: the Prorepens clade, which remained of small stature and tended to become dioecious, and the "Megaphyll" clade, which tended to increase its leaf size and rank (Figs. 16, 18), as well as the frequency of hermaphroditic flowers and the number of steles within its stem. This clade shows a trend toward increasing leaf rank, from low second rank in the Prorepens clade, toward higher second rank in the members of the basal megaphyll clade, and finally to third-rank leaves in the subgenus Panke (Figs. 16, 18). This coherent increase in leaf rank differs from that implied in the phylogenies of Wanntorp et al. (2002). Within the small-leafed Prorepens clade, the subgenus Misandra developed glandular sinuses and well-developed areolation. The subgenus Milligania evolved narrower, ovate, actinodromously veined leaves, with the conjunctal veins of the teeth often joining the principal vein alternately. The split between Milligania and Misandra is also supported by aspects of the Nostoc symbiosis. In Gunnera monoica of subgenus Milligania, mature Nostoc colonies appear to be highly productive (Stock & Silvester, 1994). This is not the case in G. magellanica of subgenus Misandra, in which the more basal and mature colonies of cyanobionts show less nitrogenase activity (Soderback et al., 1990). This is mirrored by evidence that Milligania seems to control its symbiont to such a degree that the cyanobionts lose the ability to synthesize the full range of photosynthetic proteins (Silvester, 1976), whereas in G. magellanica there has been no such loss (Soderback & Bergman, 1992).

The Megaphyll clade evolved toward larger, thicker leaves that culminated in the Latin American radiation of Panke (Fig. 15, 16). This clade is characterized by the modification of the lobate leaf base, probably as an expansion of the leaf as basal lateral primaries grew from the petiole at angles increasingly obtuse to the midvein. This seems to have been accomplished by a more basal branching from the petiole vein and an expansion of the foliar part of the leaf, in which the primary veins that form the margin (without laminar tissue) are derived evolutionarily from the petiole. Marginal teeth lost the dark-staining apical process, although hints of a clear glandular, tylate process remain in G. perpensa. Tooth venation developed a second order of reticulate accessories. From this inferred ancestor there evolved an even larger-leafed clade, in which alveolarity and colleters, as well as quadrangular areoles and an orthogonal reticulum of quintenary veins, developed. The alveolarity is caused by the thickening of successive vein orders, probably for structural reasons related to larger leaves. Druses were again lost. This trend toward leaf expansion produced the massive leaves, as well as the fleshy stems (pachycauls), of Panke.

Of particular interest is the evolution of the primary venation pattern and the akroteria in Gunnera. The midvein patterns of more-derived lineages probably evolved through midvein bifurcation and the promotion of secondary veins to the status of primaries. Trichotomies in the subgenus Milligania and in G lobata are actually a pair of opposite secondaries arising from the midvein at moderately acute angles. In larger leaves (e.g., G perpensa, G macrophylla), these secondary veins were promoted to primary thickness, perhaps for structural reasons. These trichotomous midribs actually represent two quick bifurcations in immediate proximity. A similar near-trichotomy is found in young Panke leaves, which suggests evolutionary recapitulation (Fig. 6A-6C). The lowermost of these branches then gets promoted to the primary order and subsequently outgrows the more apical secondary branch, producing the bifurcation seen in mature Panke leaves.

The large pedate lobes of some species of the subgenus Panke may have allowed for great expansion in their size, providing greater photosynthetic area and the ability to overshadow smaller, weedy competitors. Size increase was accomplished by expanding the akroteria--i.e., marginal teeth at the ends of primary veins--followed by the formation of secondary, and then higher-order, teeth. The orbicular-leafed clade of Panke may be the result of the secondary venation system expanding between primaries through intercalary growth to fill out the increased space between marginal primaries as the leaf expanded. This is suggested by the increased number of interangular veins (i.e., secondary veins that joined and fused) in these species. This mode of marginal growth produced relatively shallow lobes and more distinct, higher-order teeth.

B. IMPLICATIONS FOR HISTORICAL BIOGEOGRAPHY

Our phylogenetic analysis suggests possible stages in the biogeographical history of Gunnera (Fig. 19). Mora-Osejo (1984) accounted for the Gondwana distribution of Gunnera by suggesting a radiation out of Antarctica. Our phylogeny harmonizes with biogeographical patterns and the sequence of continental drift separation in both Australasia and South America. On the other hand, Wanntorp and Wanntorp (2003) produce a less parsimonious vicariance pattern by proposing a mixture of vicariance and long-distance dispersal. Two major nodes in their scheme are not accounted for by commonly accepted scenarios for continental vicariance. In the case of G. macrophylla, they propose long-distance dispersal from New Zealand to New Guinea and Malaya and a parallel dispersal of small-leafed G. cordifolia from New Zealand to Australia (Tasmania). In the case of South American clades, they propose dispersal from South America to North America and then a return dispersal of Panke.

[FIGURE 19 OMITTED]

The earliest confirmed fossil record of Gunnera comes from pollen found in rocks of Turonian Age (Late Cretaceous) in Peru, ca, 93 Ma (ages from Geological Society of America, 1996). This supports an origin for the genus in West Gondwanaland (Brenner, 1968; Jarzen, 1980; Jarzen & Dettmann, 1989). The Peruvian pollen falls into the size range of all Gunnera species except those of the subgenus Ostenigunnera (Belsky et al., 1965). This suggests that it derives from the core Gunnera clade above the node of Ostenigunnera, placing a minimum age on that node.

By the Campanian Age of the Late Cretaceous, post-Ostenigunnera-grade pollen occurs in Antarctica, New Zealand, Australia, and Africa. The node between the subgenus Milligania (in New Zealand and Tasmania) and the subgenus Misandra (centered in Tierra del Fuego) is datable by the separation of New Zealand from western Gondwanaland in the early Campanian, 80-84 Ma (Tulloch & Kimbrough, 1989; Laird, 1993). Australia also began to move away from Antarctica at about this time, but probably after New Zealand (Smith et al., 1994; Swenson et al., 2001). Campanian Gunnera pollen from Australia shows exine sculpturing similar to that of Milligania (Jarzen & Dettmann, 1989; Wanntorp et al., 2004), and it may be that the lineage of this group was by this time distinct from its Tierra del Fuego counterpart, which differs in exine sculpturing. This hypothesis would place G cordifolia near the base of Milligania just above the Prorepens node. As noted above, several general features of leaf morphology shared with Ostenigunnera suggest that this species is quite primitive. Indeed, Schindler (1905) separated G cordifolia from other species of Milligania in his diagnosis. However, its clavate fruit form and sometimes monoecious flowering habit suggest its placement near G monoica and G. strigosa. Gunnera pollen is absent from Australia after the Paleocene and does not reoccur there until the Pliocene (Jarzen & Dettmann, 1989). Thus it is possible that G cordifolia represents a Neogene redispersal event from New Zealand.

The subgenus Perpensum became distinct in the Campanian at more or less the same time as Milligania. South America and Africa were clearly separated by 90 Ma (Turonian), when Tethyan marine taxa reached the South Atlantic (Raven & Axelrod, 1974; Pitman et al., 1993; but for an estimate of 105 Ma see McLoughlin, 2001). This is when the ancestors of Gunnera perpensa would have been isolated. The post-G, perpensa Megaphyll clade would then have evolved in South America-Antarctica. Fossil pollen from the Late Cretaceous of Antarctica shows exine sculpturing similar to that of G macrophylla (Jarzen & Dettmann, 1989; Wanntorp et al., 2004). This pollen disappears from the Antarctic record in the earliest Tertiary, probably because of climatic cooling, which allowed only temperate species to spread between South America and Australia during the early Tertiary (Raven & Axelrod, 1975). This places the latest possible period for cladogenesis between the subgenera Pseudo-Gunnera and Panke at the end of the Cretaceous, although additional evidence suggests an earlier divergence.

Recently discovered megafossils of highly alveolar, palinactinodromous leaves from the Campanian-Maastrichtian of Wyoming and Montana show affinities with Panke (Fuller & Hickey, unpubl., cited in Wilkinson, 1998). Its earliest occurrence is in the Judith River Formation, dating to 80 Ma (Hicks, 1993; Hicks et al., 1995). This is consistent with evidence from the pollen record (Jarzen, 1980; Jarzen & Dettmann, 1989) and implies that the separation of Panke and Pseudo-Gunnera had already occurred on the South America-Antarctica landmass.

Although North and South America were separate, a selective dispersal corridor via islands was provided by the Caribbean plate (Raven & Axelrod, 1974, 1975; Pitman et al., 1993; Smith et al., 1994). The modern occurrence of Panke in Hawaii and the Juan Fernandez Islands indicates that this subgenus is prone to bird dispersal. Gunnera macrophylla is similarly found on oceanic islands today, including the young, volcanic Vanuatu archipelago. It probably reached its current Malaysian-New Guinean range by long- distance dispersal across the Indian Ocean via islands. Gunnera macrophylla-like pollen did not reach New Guinea until the Neogene, ca. 23 Ma (Jarzen & Dettmann, 1989). This was a time of global cooling that drove many austral tropical species northward (Raven & Axelrod 1972, 1974, 1975; Mercer, 1983). This pollen type was present, however, on the Indian subcontinent as it rafted northward during the early Tertiary (Jarzen & Dettmann, 1989).

C. ECOLOGICAL TRENDS

Given the great age of Gunnera, its apparent ecological conservatism is significant. Before the evolution of mutualism with Nostoc, the ancestors of Gunnera probably grew in a habitat much like that of its modern sister groups. Webb and Gornall (1989) suggested that the primitive Saxifraga inhabited damp areas on the margin of temperate forests. Chrysosplenium can be found in such habitats today and is particularly associated with damp, shady areas and stream banks within forests, especially gymnosperm-dominated forests (Hara, 1957; Ohwi, 1965; Yuzepchuk, 1971; Savile, 1975; Hickman, 1993). From the stream- or pond-edge of mid-Late Cretaceous gymnosperm-dominated forests, the ancestors of Gunnera may have spread to more open areas while still requiring damp conditions.

With the establishment of the Nostoc symbiosis, Gunnera was able to invade poor, sandy soils, such as the waterlogged, sandy-paludal habitat where G herteri grows today (cf. Osten, 1932). This ability to thrive in poor soils may have been aided by an additional symbiosis with mycorrhizae, although this has been reported only from the highly derived G petaloidea (Koske et al., 1992). Some species radiated onto permanently damp sand dunes (e.g., as in Misandra, Ostenigunnera, and some species of Milligania), while others remained on stream banks (Perpensum and some species of Milligania and Misandra). Once the constraint of soil nutrients was overcome through mutualism, the clade appears to have evolved toward larger size in plants and leaves, which could have been advantageous in overtopping competition. The availability of sunlight in open, disturbed areas, as along waterways, may have aided this directionality.

Movement toward tropical zones would have made available more areas with moisture levels conducive to the radiation of subgenus Gunnera, especially the Pseudo-Gunnera-Panke clade. Although increasing leaf size would have been selected for in warmer climes, smaller, more densely foliate forms were probably favored in the colder, austral zones. High transpiration rates may have restricted near-equatorial populations to higher altitudes (Bader, 1961; Jarzen, 1980) where areas of landslides as well as cliffs provided islands of open habitat for colonization. Increasingly sturdy and erect stems that produced leaves only near the apex (i.e., the pachycauls of Panke), as well as thick petioles, would have been necessary to support massive leaves that provided yet more photosynthetic area. At the same time, such stems were useful in resisting burial due to slumping and alluviation. The subgenus Pseudo-Gunnera developed an alternative strategy for coping with frequent burial in tropical mountains (where it is found today in New Guinea) through the production of numerous stolons and the ability to produce adventitious roots from leaves. The increasingly thick and succulent petioles in the line leading to G. manicata acquired thorns or hardened processes, perhaps in response to large herbivores.

D. IMPLICATIONS FOR MACROSYSTEMATICS: A HERBACEOUS RADIATION OF EUDICOTS?

No evidence was noted in this study of a compound-leafed ancestry for Saxifraga, Chrysosplenium, or Gunnera. The taxa with which these genera grouped in cladograms were consistently groups with simple leaves, such as Pachysandra. This raises the possibility that this group represents a distinct "rosid" radiation separate from much of the traditional subclass Rosidae with its possible sapindopsoid or cunoniaceous origins (Hickey & Wolfe, 1975; Takhtajan 1980, 1983; Cronquist, 1981; Dickison, 1989). This conclusion is similar to that implied by recent genetic analyses (Soltis et al., 2000, 2003; Angiosperm Phylogeny Group, 2003; Hilu et al., 2003). A number of the apomorphies linked Gunnera and Saxifragaceae in the cladistic analyses. These include low rank, palinactinodromous leaves that lacked fourth and higher order veins or freely ending veinlets and possessed chloranthoid teeth. Such leaves are reminiscent of those of early angiosperm fossils and represent character states that may precede the evolution of the trochodendroid hamamelids (cf. Hickey & Doyle, 1977; Taylor & Hickey, 1992). Further research may identify a more basal outgroup for the Gunneraceae-Saxifragaceae clade.

The tricolpate pollen of some Saxifragaceae, as well as that of Gunnera, suggests that they occupy a basal position among eudicots in light of evidence for the monophyletic origin of tricolpate pollen (Doyle & Hotton, 1991; Chase et al., 1993; Crane et al., 1995; Sytsma & Baum 1996; Hoot et al., 1999; Soltis et al., 2000, 2003). Dickison (1989) suggested that among the plesiomorphies shared by rosids and basal hamamelids are trilacunar, three-trace nodes that may be related to the three-veined petiole of the basal Saxifragaceae-Gunneraceae. Although Dickison saw the rosidhamamelid ancestor as having several ovules per locule, recent phylogenetic and anatomical studies suggest that primitive carpels may have been unilocular (Taylor & Hickey, 1992; Crane et al., 1995; Hickey & Taylor, 1996; Taylor & Kirchner, 1996). If so, then unilocular taxa like the tricolpate Gunnera, Chrysosplenium, or the tricolporate Astilbe, may fall near the base of the rosid-hamamelid clade, or the "core eudicots" (sensu Soltis et al., 2003). There is increasing evidence for an herbaceous ancestry for the eudicots (Donoghue & Doyle, 1989; Doyle & Hotton, 1991 ; Taylor & Hickey, 1992; Hickey & Taylor, 1996), which may therefore warrant the placement of herbaceous groups near the base of the eudicots. Paleobotanical considerations of eudicot origins need to incorporate a search image of small, low-rank herbaceous leaves like those of the subgenus Ostenigunnera and the genera Chrysosplenium and Saxifraga.

VI. Conclusions

Gunnera has long proved difficult to place systematically. The same consistent suite of fertile characters that so well designates the monogeneric Gunneraceae has offered little evidence for direct comparison with other taxa. The very simple flowers have led to superficial comparisons with groups such as Haloragaceae and Balanophoraceae, which may represent convergence through reduction (cr. Hooker, 1856). On the other hand, leaves vary greatly within Gunnera, and the study of leaf architecture provides a robust data set both for examining the phylogenetics within Gunnera and for determining its higher-order affinities. Ontogenetic evidence within Gunnera is congruent with a phylogenetic trend that sees species with large, elaborately veined leaves develop from ancestors having small, poorly organized leaves. The resultant hypothesis of Gunnera phylogeny is congruent with the biogeographical distribution of its subgenera and with the separation times of the Gondwana continents (Figs. 16, 19). It seems that the ecological range of Gunnera and its two major clades, the Prorepens clade and the Megaphyll clade, was fully established during its early radiation by the Turonian and has remained remarkably consistent. Thus Gunnera palynofossils should prove to be useful environmental indicators even in the distant past.

Leaf architecture and its ontogeny in Gunnera strongly suggest a relationship with the lower, herbaceous Saxifragaceae (Figs. 12, 13). For this reason we support placement of Gunneraceae in the order Saxifragales (as recognized by Takhtajan, 1983, 1997). The sister relationship with Saxifragaceae has implications for the evolutionary polarization of traits within that family. This implies a much greater antiquity for Saxifragaceae than has previously been proposed (Savile, 1975; Benton, 1993; Soltis et al., 2001a, 2001b). Both the pollen record and paleobiogeography indicate that the Gunneraceae was well established by the Turonian (93 Ma), so the ancestors of modern Saxifragaceae should be sought in some prior age. Gunnera represents one of yet another of the evolutionary directions taken by a basal herbaceous angiosperm radiation that included the eudicots beginning in the early-mid Cretaceous.

IX. Appendix: Characters and Character States

Characters and character states for the data matrix (Table IV) used to produce the cladograms are set forth below. Discussion is provided for those taxa showing more than one state, or when additional explanation is warranted. Leaf architectural characters and their states are mostly derived from Hickey (1973, 1979). Additional character states are defined and, if derived from another source, the citation is given after the character state description. For those characters for which data are not based on the authors' own study, citations follow the character-state descriptions.

A. FOLIAR MORPHOLOGY: FORM

1. General laminar form: (0) elliptical; (1) ovate; (2) obovate; (3) reniform, distinguished from ovate in that the width of the leaf exceeds its length; (4) orbicular, distinguished from elliptical by having width and length approximately equal.

2. Apex: (0) acute; (1) obtuse; (2) rounded; (3) acuminate; (4) embayed, with indentation at the apex equal to, or greater than, one-third of the leaf length.

3. Base: (0) decurrent to sublobate; (1) lobate; (2) truncate to cordate; (3) rounded; (4) lobate-auriculate, having ear-shaped lobes of the lamina developing toward the petiole and partially enclosing the lobate base.

4. Lobes or akroteria: (0) lobes absent, akroteria only present as marginal teeth; (1) lobed, akroteria indented one-quarter of the distance to the midvein; (2) pedate, having two orders of lobes or akroterion pairs; (3) having primary akroteria as large, convex-convex teeth, with secondary akroteria as marginal teeth: akroteria are indented generally less than one-quarter of the distance to the midrib and therefore do not qualify as lobes.

For discussion of the terms in these character states, see the section "Systematic Leaf Architecture of Gunneraceae" above, and Fig. 3. Gunnera brephogea is borderline between states 2 and 3, with some specimens falling into either character state. This demonstrates the arbitrariness of the division into distinct categories of what is in fact an evolutionary, and probably ontogenetic, spectrum. Gunnera brephogea has been coded as state 2, because this strengthens its position as intermediate between the "pedate" and "orbicular" lineages of the subgenus Panke.

5. Margin: (0) serrate; (1) crenate, or dentate, with one order of teeth; (2) dentate in two orders; (3) dentate in three or more orders; (4) dentate with secondary akroteria as broad, first-order teeth, the margins of which bear higher-order akroteria that resemble teeth in venation but lack sinuses; thus the margin of the broad, first-order teeth is essentially repand; (5) entire.

States 1 and 2 are merely points along a spectrum of marginal form in Gunnera. In order to assign this state, leaves were assumed to have a single order of teeth unless a substantial majority of teeth were associated with second-order teeth. Thus the existence of small numbers of secondary teeth does not warrant assignment to state 2.

In Gunnera pilosa and G. talamancana, high-order teeth are incipient (state 4). They are apparent by their glandularity and venation pattern but project barely, if at all, beyond the margin. These repand margins have a tendency to be revolute.

6. Tooth form, first-order teeth: (0) acuminate-convex (type D 1); (1) convex-convex (type Al); (2) straight-straight (type B2); (3) convex-concave (type C1); (4) acuminate-acuminate (type A4); (5) concave-concave (type C3); (6) Disanthus N/A; (7) Cnestis N/A; (8) acuminate-straight (type D2).

In determining tooth form, only that portion of the leaf margin separated from other teeth by sinuses was considered.

B. VENATION CHARACTERS

7. Primary venation type: (0) pinnate; (1) actinodromous; (2) palinactinodromous, but with basal origination of three primaries; (3) acrodromous.

Palmate and pinnate venation types can intergrade and thus represent points along a morphocline. This is particularly evident in the subgenus Milligania. For this reason, character 8, state 2 (below) includes pinnately veined leaves.

8. Mode of origination of lateral primaries or basal secondaries: (0) three distinct veins in the petiole; (1) basal with lateral primaries forming a margin along a lobate base; (2) basal, with only one vascular bundle visible in the petiole, including pinnately veined leaves with a pair of strong, basally originating secondaries; (3) suprabasal; (4) Griselinia N/A; (5) Aucuba N/A; (6) Cnestis N/A.

9. Course of midrib: (0) straight, unbranched; (1) straight, reticulating, becoming indistinct from higher-order veins; (2) midrib lacking (i.e., dichotomizing from the base); (3) straight, trichotomous approximately halfway toward the apex, or with oppositely arising secondaries forming a virtual trichotomy; (4) straight, dichotomizing once below the apex; (5) straight, dichotomizing twice below the apex.

10. Number of agrophic veins present on each side of lamina: (0) absent; (1) 1; (2) 2; (3) 4; (4) 5 or 6; (5) N/A, true pinnate venation.

11. Primary vein development (including agrophic veins in craspedodromous leaves): (0) marginal; (1) reticulate; (2) Trochodendron N/A (A); (3) Ampelopsis N/A; (4) Griselinia N/A; (5) Disanthus N/A; (6) Proserpinaca N/A; (7) Lopezia N/A; (8) Aucuba N/A; (9) Cnestis N/A.

12. Secondary vein, type and course: (0) brochidodromous; (1) semicraspedodromous; (2) craspedodromous, branched or sinuous, includes reticulate; (3) craspedodromous or marginal, recurved; (4) craspedodromous or marginal, uniformly curved.

13. Secondary vein, angle of origination: (0) moderately acute, 45[degrees]-65[degrees]; (1) narrowly acute, <45[degrees]; (2) widely acute, >65[degrees].

14. Variation in angle of secondary origination: (0) upper veins more obtuse; (1) uniform; (2) upper veins more acute; (3) angle irregular.

15. Tertiary pattern: (0) reticulate-orthogonal; (1) reticulate-random; (2) percurrent.

16. Quaternary course: (0) orthogonal; (1) random reticulate; (2) ramified admedial; (3) fourth order lacking.

17. Quintenary course: (0) fifth-order veins absent; (1) random; (2) orthogonal.

18. Marginal veins: (0) looped; (1) incomplete.

19. Areolation: (0) imperfect; (1) well developed; (2) incomplete.

20. Areole shape: (0) quadrangular; (1) irregular.

21. Freely ending veinlets: (0) simple, linear or curved; (1) branched once; (2) branched more than once; (3) veinlets lacking; (4) veinlets occasional.

The absence of freely ending veinlets in Gunnera was noted by Palkovic (1974). In leaves of the larger species, particularly in subgenus Panke, veinlets are found in a small minority of areoles.

22. Alveolarity of laminar tissue: (0) none or slightly prominent major veins; (1) subalveolar, with prominent veins on abaxial surface; (2) alveolar.

This character refers to the texture of the leaf formed by prominent veins and surrounding impressed areas of laminar tissue on the abaxial surface. On the adaxial surface, the veins are highly impressed and around small hills of laminar tissue, which thus appears colliculate. Alveolarity within Gunneraceae is distinctive in this character because prominent or impressed veins include the penultimate vein order present (e.g., the fifth or sixth order), whereas in other taxa that sometimes show alvaeolarity, accentuation of the veins is usually restricted to the third (or fourth) order; e.g., Vitaceae, Platanaceae. The presence of pseudo-colleters (character 39 below) in many species of Gunnera greatly exaggerates their alveolarity.

23. Leaf rank (Hickey, 1977: appendix; Hickey & Taylor, 1991): (0) first rank; (1) low second rank ([2r.sup.0]-[2r.sup.1); (2) high second rank ([2r.sup.2]-[2r.sup.3]); (3) third rank.

This character represents the general organizational regularity of the leaf. It is significant because it makes less likely the derivation of very irregularly veined leaves from highly ordered leaves under normal mesic conditions. Because Gunneraceae show a broad spectrum of rank, from the low first-order leaves of Gunnera herteri to the highly reiterative venation of subgenus Panke, this character should elucidate trends toward greater or lesser rigidity in venation pattern. In general, leaf rank tends to reflect the general size of the leaf within Gunnera.

24. Crystalline inclusions in leaf tissue: (0) absent; (1) sandy; (2) druses; (3) raphides, as well as other forms; (4) framboids.

For a discussion of oxalate crystals in Saxifraga, see Gornall (1986). Druses are reported for Gunnera herteri by Mattfeld (1933).

C. MARGINAL TEETH, GLANDS, AND SINUSES

25. Glands: (0) on teeth; (1) on teeth and in sinuses; (2) marginal; (3) absent.

26. Apical termination of marginal teeth: (0) tylate; (1) tylate with dark-staining apical process; (2) foramenate; (3) simple; (4) papilose; (5) spinose; (6) Cnestis N/A; (7) Disanthus N/A.

27. Principal vein: (0) central and direct; (1) eccentric, running to one side of the axis of symmetry of the tooth; (2) Disanthus N/A; (3) Cnestis N/A.

28. Termination of principal vein: (0) tapered; (1) bulbous; (2) truncate; (3) splayed; (4) Cnestis N/A; (5) Disanthus N/A.

29. Suite of veins associated with the principal vein of the tooth: (0) no admedial, conjunctals and accessories only; (1) admedial and conjunctals only; (2) admedial, conjunctals, and one order of reticulate accessories; (3) admedial, conjunctals, and reticulate accessories in more than one order; (4) admedial, conjunctals, and freely ending accessories; (5) admedial and freely ending accessories, true conjunctals lacking; (6) Disanthus N/A; (7) Cnestis N/A.

30. Conjunctal veins: (0) joining and fusing with the principal vein, opposite; (1) joining and fusing with the principal vein, alternate; (2) incipiently connivent, with only a few strands merging; (3) connivent with the principal (i.e., running alongside it and splaying or ending concurrently in tooth epithem); (4) convergent but remaining separate; (5) only one conjunctal, joining; (6) "vitioid" tooth venation, in which alternate conjunctals split just before meeting the principal vein, with the admedial portion of the conjunctal joining the principal while the exmedial portion connives; (7) Cnestis N/A; (8) Disanthus N/A; (9) Griselinia N/A.

Although character state 0 occurs in a minority of modern Cercidiphyllum leaves, it is indicated as the ancestral state in the fossil record (see the discussion in the text). However, recoding our cladistic matrix for this character would not affect the placement of Cercidiphyllum.

31. Strength of the admedial: (0) same order as the principal vein; (1) lower order than the principal vein; (2) N/A Disanthus; (3) N/A Cnestis; (4) absent.

32. Sinus shape: (0) angular; (1) rounded; (2) rounded sinuses between first-order teeth, sinuses between the higher order lacking; (3) N/A Disanthus; (4) N/A Cnestis.

33. Source of sinus venation: (0) conjunctal; (1) branch from conjunctal; (2) combinations of conjunctal and its branch; (3); combination of conjunctal and admedial; (4) convergent, thickened, merging admedials; (5) combination of admedial and branch from admedial; (6) combination of branches from admedial and conjunctal; (7) branch from admedial; (8) Disanthus N/A; (9) Gunnera pilosa N/A; (A) Gunnera talamancana N/A.

D. EPIDERMAL CHARACTERS

34. Epidermal cell morphology (Dilcher, 1974): (0) elongate cells and deeply undulate outline; (1) isodiametric, pentagonal-hexagonal, straight to round walls; (2) hexagonal with straight walls, interspersed with irregularly shaped, sinuously walled cells.

35. Trichomes (Theobald et al., 1979): (0) absent; (1) unicellular; (2) uniseriate, multicellular; (3) multicellular-stellate; (4) multiseriate.

36. Trichome placement: (0) on the margin only; (1) on the lower surface veins and the margin; (2) on veins of both surfaces and margin; (3) on veins of both surfaces, margin, upper surface, and areoles; (4) on the veins and areoles of both surfaces, plus the margin; (5) on the veins, areoles, and sinuses; (6) Gunnera herteri N/A; (7) Trochodendron N/A; (8) Tetracentron N/A; (9) Cercidiphyllum N/A; (A) Aucuba N/A; (B) Disanthus N/A; (C) Ascarina N/A; (D) Hamamelis N/A; (E) Chrysosplenium N/A; (F) Griselinia N/A; (G) on the petiole only; (H) Myrothamnus N/A.

37. Petiolar processes: (0) thoms or processes lacking; (1) thorns or processes present. This character does not include trichomes. Thorns on the petioles of Panke species often extend onto the primary veins.

38. Colleters, circular glandular processes emerging from laminar tissue of the leaf's upper surface, at the intersection of fourth- and fifth-order veins, secretory: (0) absent; (1) present.

Colleters are unique to the Gunnera subgenera Panke and Pseudo-Gunnera and have been discussed by numerous authors (Solereder, 1908; Palkovie, 1974; Mora-Osejo, 1984; Wilkinson, 1998).

39. Pseudo-colleters, conical, nonglandular processes emergent from the upper surface of leaf tissue in the midst of areoles or subtended by seventh- or higher-order venation: (0) absent; (1) present.

These have often been noted as a variant form of colleter (Solereder, 1908; Palkovic, 1974; Mora-Osejo, 1984), but because these are not glandular they are not true colleters (cf. Wilkinson, 2000).

E. POLLEN

The sources for characters 38 through 47 are as follows: Gunnera (Praglowski, 1970; Jarzen, 1980; Jarzen & Dettmann, 1989), Proserpinaca (Praglowski, 1970); Ascarina (Walker & Walker, 1984), Aucuba (Chao, 1954), Griselinia (Heusser, 1971) Cercidiphyllum, Trochodendrales, Hamamelidaceae (Zavada & Dilcher, 1986; Hufford & Crane, 1989; Endress, 1993a, 1993b, 1993c); Platanus (Kubitzki, 1993a); Lopezia (Patel et al., 1984); Saxifraga (Erdtman, 1966; Ferguson & Webb, 1970); Chrysosplenium (Heusser, 1971; Gupta & Sharma, 1986); Cnestis (Dickison, 1979), Vitaceae (Erdtman, 1966); Myrothamnus (Zavada & Dilcher, 1986; Kubitzki, 1993b; Wanntorp et al., 2004). In some cases character states were based on photographs in the above publications.

40. Form: (0) monosulcate; (1) tricolpate; (2) bicolpate; (3) tricolporate; (4) triporate; (5) periporate.

41. Protruding apertures: (0) absent; (1) present.

42. Pollen size: (0) medium (2540 [micro]m); (1) small (10-24 [micro]m); (2) large (>40 [micro]m).

43. Aperture shape: (0) elliptic furrow (i.e., aperture termini round); (1) lenticular (i.e., aperture termini pointed); (2) circular.

The potential systematic utility of this character is noted by Hufford and Crane (1989).

44. Nonapertural exine sculpturing (Walker & Walker, 1984): (0) reticulate, beaded, spinulose, or verrucate; (1) reticulate, smooth, without tectal spinules; (2) tectum with insular protrusions; (3) rugulate, imperforate, with viscin threads; (4) psilate; (5) clavate.

45. Nonapermral exine structure (Walker & Walker, 1984): (0) tectate perforate to semitectate; (1) tectate imperforate; (2) intectate.

46. Columellae and foot layer: (0) both present; (1) both absent.

47. Nonapertural exine lumina: (0) polygonal; (1) round; (2) Proserpinaca N/A; (3) Lopezia N/A; (4) Aucuba N/A; (5) Griselinia N/A; (6) Saxifraga N/A; (7) Pachysandra N/A; (8) Myrothamnus N/A.

48. Apertural sculpturing: (0) smooth to finely verrucate; (1) coarsely granulate; (2) pore, no sculpturing.

49. Endexine: (0) thick, under apertures only; (1) endexine throughout, thickened under apertures; (2) endexine throughout, not thickened under apertures; (3) endexine absent under apertures.

50. Pollen maturity at shedding: (0) 2-celled state; (1) 3-celled state.

F. MISCELLANEOUS, REPRODUCTIVE, AND ANATOMICAL CHARACTERS

51. Growth habit: (0) cauline herb, with bifurcating axis, opposite, axillary leaves without stolons; (2) tree or shrub; (3) pachycaul; (4) rhizomatous herb, with leaves basal; (5) woody vine (Schindler, 1905; Ohwi, 1965; Spongberg, 1972; Cronquist, 1981; Webb & Gornall, 1989; Endress, 1993a, 1993b, 1993c; Heywood, 1993; Kubitzki, 1993a, 1993b). (Note the absence of state 1 for this character, both here and in the matrix in Table IV.)

52. Stolons: (0) absent; (1) present.

We have coded all stolons the same, despite indications that stolons in Misandra and Milligania differ from those of Pseudo-Gunnera, because the latter are not subtended by foliose leaves and lack adventitive root primordia (see the discussion in the text).

53. Symbiotic Nostoc cyanobacteria: (0) absent; (1) present.

The Nostoc symbiosis is unique to Gunnera among angiosperms (Bergman et al., 1992).

54. Sieve-element plastid types: (0) plastids containing starch crystals only (S-type); (1) plastids containing proteins (P-type)(Behnke, 1981, 1986, 1991).

55. Stipules: (0) present; (1) absent.

Gunnera possesses axillary scales, called "ligules" or "rhizome scales" (Schindler, 1905), which are sometimes considered to be stipulate (cf. Cronquist, 1981, 1988). However, MoraOsejo (1984) argued for their derivation from reduced leaves and did not consider them to be stipules. Examination of the ligules in G. chilensis suggests that they may represent developmentally reduced leaves. Study of the minute "ligules" in the smaller and presumably more primitive species indicates that they are indeed cataphylls (Wanntorp et al., 2003).

56. Ovule: (0) orthotropous, bitegmic; (1) anatropous or hemianatropous, bitegmic; (2) anatropous, unitegmic (Davis, 1966; Palkovic, 1974; Orchard, 1975; Corner, 1976; Cronquist, 1981; Dahlgren & Thorne, 1984; Webb & Gornall, 1989; Kubitzki, 1993b).

57. Embryo-sac development: (0) monosporic, 8-nucleate (Polygonum type); (1) tetrasporic, 16-nucleate (Peperomia type); (2) Oenothera type; (3) bisporic (Allium type). Same sources as for character 56.

58. Nucellus: (0) crassinucellar; (1) tenuinucellar. Same sources as for character 56.

59. Endosperm development: (0) nuclear; (1) cellular. Same sources as for character 56.

60. Number of seeds per fruit: (0) 1; (1) many. Same sources as for character 56.

61. Flowering habit: (0) all flowers hermaphroditic; (1) monoecious (mixture of unisexual and some hermaphroditic flowers); (2) dioecious (Scbindler, 1905; Ohwi, 1965; Meijden & Caspers, 1971; Spongberg, 1972; Palkovie, 1978; Cronquist, 1981; Lowry & Robinson, 1988; Webb & Gornall, 1989; Endress, 1993a, 1993b, 1993c; Heywood, 1993; Kubitzki, 1993a, 1993b; Takhtajan, 1997).

62. Inflorescence type: (0) panicle or compound spike; (1) spike or raceme; (2) dense racemose head; (3) corymb; (4) solitary flower; (5) cyme. Same sources as for character 61.

Platanus has been coded as a panicle on the basis of the likely derivation of its inflorescence (Kubitzki, 1993a). Myrothamnus is also considered a reduced panicle (Kubitzki, 1993b). Chrysosplenium often has a single flower, but, because some species have compound inflorescences of the corymb type (Ohwi, 1965), we have coded this as basic to the genus, assuming that the solitary flowers are a reduced derivative.

63. Embryo shape: (0) straight, cylindrical; (1) undifferentiated or with slight cotyledons; (2) with two lobes, obcordate. Same sources as for character 61.

64. Phyllotaxis: (0) opposite; (1) alternate; (2) whorled.

65. Sessile, cauline leaves (sometimes improperly called "ligules" on Gunnera): (0) absent; (1) like other leaves, but smaller and sessile; (2) small, straplike; (3) small, shieldlike; (4) budlike; (5) pinnatifid to laciniate.

Study indicates these to be cataphylls (Mora-Osejo, 1984; Wanntorp et al., 2003); cf. character 55 above.

VII. Acknowledgments

The authors gratefully acknowledge Britt Wheeler, administrative assistant, Division of Paleobotany, Yale Peabody Museum, for preparing and proofreading the manuscript. Special thanks are due to Linda Klise, collections manager of the division, for her assistance with nomenclature and proofreading.

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DORIAN Q FULLER

Institute of Archaeology

University College London

London WC1H 0PY, England

AND

LEO J. HICKEY

Department of Geology & Geophysics

Yale University

New Haven, CT 06520-8109, U.S.A.
Table 1 Affinities of Gannera proposed or
implied by various authors

Proposed Source(s)
affinity

Haloragaceae/ Bentham & Hooker, 1865; de Candolle, 1868;
 Haloragales Engler & Prand (Peterson, 1893);
 Schindler, 1905; Hutchinson, 1973;
 Cronquist, 1981; Heywood, 1993
Urticales Jussieu, 1789; Battling, 1830; Endlicher, 1837
Arialaceae Lindley, 1846
Umbellales Gibbs, 1974
Onagraceae Gray, 1854; Gibbs, 1974;
 Doyle & Scogin, 1988a, 1988b
Vitaceae Behnke, 1981; Thorne, 1992
Cornaceae Thorne, 1992
Connaraceae Behnke,1986
Eucryphiaceae Behnke,1986
Balanophoraceae Hooker, 1856; Hansen, 1980; Mabberley, 1993
Saxifragaceae Huber, 1963; Takhtajan, 1980, 1983;
 Dahlgren, 1983; Doyle & Scogin, 1988a,
 1988b
Hamamelidaceae Chase et al., 1993
Cercidiphyllaceae Chase et al., 1993; Sytsma & Baum, 1996
Platanaceae Chase et al., 1993
Trochodendrales Chase et al., 1993
Myrothamnaceae Hoot et al., 1999; Soltis et al., 2000,
 2003; Wanntorp et al., 2001, 2002

Table II
The division of Gunnera species into
subgenera following different authors

 Maclaughy, Mattfeld, Meijden and
Schindler, 1905 1917 1933 Caspers, 1971

Milligania (9 spp.) Milligania Milligania Gunnera
Misandra (3 spp.) Misandra Misandra section:
 Misandra
Pseudo- Pseudo- Pseudo- section:
 Gunnera (1 sp.) Gunnera Gunnera Gunnera
 (including (including
 Perpensum) Milligania,
 Pseudo-
 Gunnera,
 Perpensum)
Per pensum (1 sp.) Perpensum
Panke (19 spp.) Pazzke Panke section: Panke
 Ostenigunnera Ostenigunnera
 (1 sp.,
 discovered
 1929)

Table III Specimens examined, including leaf
clearings and herbarium sheets

Family or Species Figure No. OTU
subgenus Gunneraceae

Milligania Gunnera eordifolia
 (Hook. f.) Hook f.
 G. dentata Kirk 4E, 5A GDEN
 G. monoica Raoul 3D, 9C GMON
 G. prorepens Hook. f. 4C GPRO
 G. strigosa Sol. (GSTR) 4D, 7C
 G. hamiltonii 1B, 4F GHAM
 Kirk ex W. Ham.

Misandra G. lohata Hook. f. 4A, 9D GLOB
 G. magellanica Lam 413, 4G GMAG

Ostenigunnera G. herteri Osten 1A, 5B, 7A GHER
Pankc G. brephogea 1F GBRE
 Linden et Andre
 G. chilensis Lam. 1C, 6C, 6D GCHI
 G. insignis Oerst. 5C, 6B, 8C, 9F GINS
 G. killipiania Lundell GKIL
 G. manicata Linden GMAN
 G. mexicana Brandegee GMEX
 G. petaloidea Gaudich
 G pilosa Kunth 1D, 8B, 8D (GPIL)
 G. talamancana H. GTAL
 Weber & L. E. Mora
Perpensum G. perpensa L. I E, 6A, 9B GPER

Pseudo-Gunnera G macrophylla Blume 3C, 8A, 9A, 9E GMAC

Other families

Aextoxicaceae Aextoxicon
 punctatum Ruiz & Pav.
Berberidopsidaceae Berberidopsis
 corallina Hook. f.
Buxaceae Pachysandra 10H, 11A PACH
 procumbens Michx.
Cercidiphyllaceae Cercidiphyllaun 10G CERC
 japonicum
 Siebold & Zuce.
Connaraceae Cnestis palala Merr. ONES
Cornaceae Aucuba japonica Thunb. AUCU
 Griselinia
 jodinfolia Taub.
 G scandens Taub. GRIS
Euchryphiaceae Eucryphia lucida EUCR
 (Labill.) Baill.
Haloragaceae Haloragis acutangula
 F. Muell.
 Loudonia roei Schltr.
 Proserpinaca l0A PROS
 palustris L.
Hamamelidaceae Disanthus DISA
 cercidifolia Maxim.
 Hamomelis virginiana L. 10D HAMA
 Liquidambar LIQU
 formosana Hance
Myrothamnaceae Myrothamnus
 moschata Baill.
Onagraceae Lopezia trichota 10B LOPE
 Schltr.

Penthoraceae Penthorum sedoides L.
Platanaceae Platanus 10E PLAT
Saxifragaceae occidentalis L.
 Astilbe
 japonica A. Gray
 Chrysosplenium 7F CHRY
 alternifolium L.
 C. grarvanum Maxim. CHRY
 C. griffithii CHRY
 Hook. f. & Thomas
 Jepsonia parryi
 (Torrey) Small
 Leptarrhena
 pvrifolia
 (D. Don) Ser.
 Lithophragma
 affinis A. Gray
 Mitella breweri A. Gray
 Peltiphyllum
 peltatum
 (Torrey) Eng.
 Saxifraga SAXI
 mertensiana Bong.
 S. (Micranthes) 7B, 7D, 11C MICR
 eriophora S. Watson
 S. (Micranthes) MICR
 nivalis L.
 S. sarmentosa L. SAXI
 Sullivantia
 oregana S. Watson
 Tolmiea menziesii
 (Pursh) Torrey &
 A. Gray
Tetracentraceae Tetracentron 10f, 11B TETR
Trochodendraceae sinense Oliv.
Vitaceae Trochodendron TROC
 ralioides
 Siebold & Zucc.
 Ampelopsis AMPE
 heterophylla Blume
 Vitis inconstans Miq. 10C VITI

Family or
subgenus Herbarium materials (a, b)

Milligania R. C. Gunn s.n. (YU)
 ex Herb Kirk 365 (US), NCLC 6923
 Fosberg 30750 (US), Fosberg 30777 (US), Fuller
 and Jones 310 (YU), Fuller and Jones 311 (YU),
 L. Cockayne 4537, NCLC 6900
 Fosberg 30731 (US); Walker 4869 (US), NCLC 6917
 Walker 4420 (US), NCLC 6918
 Fuller 95-1 (YU), NCLC 6927
Misandra Goodall 2303 (US), NCLC 69157; Moore 2062 (US)
 Banks and Solander (US): US 1232964, NCLC 6915
 Sleumer 1048 (US), NCLC 6916
Ostenigunnera Herter 226976 (US), NCLC 6914;
 anon. (US): US 2104785
Pankc B.T. 542 (NY), NCLC 6890;
 Bunting 11.674 (NY), Wiggins
 10993-A (NY)
 Bettreund 12556 (UC)
 Crosby 11436 (NY), Lent 277 (NY),
 Hill 17747 (NY), Gomez
 19719 (NY), Skog 1301 (US),
 Hickey 5031 (YU): Standley 37583 (?)
 Steyermark 49835 (US), NCLC 6919;
 Breedlove 9000 (US)
 Pabst 77112 (NY), Krapovickas
 23066 (NY), Reitz 2.669
 (US), NCLC 1870
 Martinez 3230 (CAS); Reisfield 1481 (NY),
 NCLC 6899; Neal and Harrt s.n. (YU)
 Ewan 16628 (US), St. John 20525 (NY),
 NYBG 6911; Pennell 2660 (US),
 Pennington 5508 (US), Barriga 13232
 (NY)
 Lent 118 (NY), NCLC 6912;
 NYBG 650206-04 (NY), NCLC
 6920; Rodriguez 437 (UC)
Perpensum Ash 2843 (US), NCLC 6922;
 Strey 7960 (US), Bourell 2731
 (CAS)
Pseudo-Gunnera Hoogland & Pullen 5591 (US),
 NCLC 6921; Barker 67544
 (US), Bartlett 8532 (US),
 Fuller and Doyle 216 (YU),
 Fuller and Doyle 217 (YU),
 Fuller and Doyle 219 (YU)

Other families

Aextoxicaceae Unknown (US): US 2343533, NCLC 503
Berberidopsidaceae Philippi s.n. (US): US 1391551, NCLC 967
Buxaceae Kearney 108 (US), NCLC 4655
Cercidiphyllaceae Nikko s.n.: US 1314386, NCLC 4115
Connaraceae Rock 769 (US), NCLC 263
Cornaceae Wilson 6440 (US), NCLC 2744
 Eyerdan 10530 (US), NCLC 3795
 Philippi 1084 (US), NCLC 3793
Euchryphiaceae Arthur 5111 (US), NCLC 3193
Haloragaceae McDonald s.n. (US): US 2634123, NCLC 1863
 Pritzel 836 (US), NCLC 1861
 Chandler s.n. (US): US 983503, NCLC 1869
Hamamelidaceae Wilson 7743 (US), NCLC 805
 Palmer 4441 (US), NCLC 6343
 Shimada and Tanaka 3298 (US), NCLC 816
Myrothamnaceae Decary 10246 (US), NCLC 826
Onagraceae Rose and Painter 6692 (US), NCLC 1908
Penthoraceae Burton s.n. (YU), NCLC 6717
Platanaceae Hickey s.n. (YU), NCLC 6344A
Saxifragaceae Nanokawa s.n. (US): US 206082, NCLC 3488
 Hall 3068 (US), NCLC 3530
 Togasi 702 (US), NCLC 3538
 Rock 4979 (US), NCLC 3539
 C.C. Parry s.n. (YU)
 M. McCluskey 117 (YU)
 Brewer 1146 (YU)
 Brewer 1679 (YU)
 Bolander 4986 (YU)
 Cusick 3321 (US), NCLC 3468
 Moran 15406 (US), NCLC 3458
 Coville and Kearney 1108 (US), NCLC 3466
 Tsu 1679 (US), NCLC 3508
 T. J. Howell s.n. (YU)
 Bolander 4792 (YU)

Tetracentraceae Oliver s.n. (US): US 596944, NCLC 184
Trochodendraceae Unknown (US): US 1271620, NCLC 174
Vitaceae Barnes 20191 (US), NCLC 172
 Li Hao-min 13169 (YU), NCLC 6452

(a) For specimens without collector numbers,
herbarium serial numbers are given after the colon,
if possible.

(b) Key: (CAS) = California Academy of Science;

(US) = U. S. National Herbarium;

(YU) = Yale Herbarium;

(NY) = New York Botanical Garden;

(UC) = University of California at Berkeley.

Table IV
Data matrix for phylogenetic analysis

OTUs Character states

 11111111112222222222333333333344444444445555555555666666
 12345678901234567890123456789012345678901234567890123456789012345

GHER 12000021101203130001300201030041000600010111000020001112121010200
GMON 10012012320200030001301201022011301200010011000020411112121010222
GSTR 10002012320200030001301201022011301200010011000020411112121010222
GDEN 10002002310310010001301101022011301400010011000020411112121020222
GPRO 10002002310300010001301001022011301200010011000020411112121020222
GHAM 10002001311310010001301001022001311400010011000020411112121020222
GMAG 32100022220212030010311011032011401100010011000020011112121020203
GLOB 12112012020202010010301011032011401100010011000020011112121020203
GPER 32100023331201001001402200032111121400010011000020001112121010200
GMAC 32400023330201002000422000032111121301?10011000020011112121010204
GKIL 42433523540422002010023000012211621311010011000020301112121000225
GINS 42433423540422002010423000012111621311010011000020301112121000225
GPIL 34424023430403002000423020012112921311110011000020301112121010225
GBRE 44433223440401002000423000002111621301010011000020301112121010225
GTAL 34424023430401002000023020012112A21311110011000020301112121010225
GMEX 42433223540422002010023000012211221311010011000020301112121000225
GMAN 44423423540421002000423000002211521311110011000020301112121000225
GCHI 44423423540222002010423000012211221311110011000020301112121010225
MICR 12000021101203110001300200030441102000010111000011400012010100221
CHRY 12000021101203130001300000030041000E0001011100001?000?I?000103200
SAXI 32202022100203130001300000020040114400010012106111410011000103221
PROS 00001202056210110001000204021301114500026122002021000001000011010
LOPE 0030130200702211001100230003130100110005122321323?200001210024000
TROC 03303002002010002101103003022110210700010111000120200011001101110
TETR 10201032001001001121102003032101210800010111000110200001?0?101110
PLAT 11011314010402201001223400032311113400010111000?2?200000?1?010010
CERC 10203132021001001121202002135400710900010000001120200001011122200
HAMA 01301002000411202121203402030011700D000101110??I?0200001000101010
DISA 10206612015020201122202227256823800B00010011000110200001000121010
CNES 003067060590210021112030363477349?140005001200?01?200111100020710
AMPE 1320180202300020210120301200261041220003100100?2??200101?00105010
VITI 13221412020001202101223002002611612G0003100100?2??200101?00100010
AUCU 00301306004101021122102200034111610A0005121430411?200112001023000
GRIS 1020130400BI00002121202235005411710F0003005110501?0?0?I2?01113000
PACH 100000140112001111011020020320101113000502?2107200000?11?01011010
MYRO 01001120000401140101001102030310010H00040125208220200001300120100

For taxa abbreviations, see Table III; for character
state definitions, see Appendix.

Table V
Pairwise patristic distances between outgroup
taxa and representative Gunnera species (a)

 GHER GPRO GLOB GPER GMAC GCHIL Mean

CHRY 0.177 0.516 0.516 0.452 0.541 0.694 0.482
MICR 0.277 0.492 0.554 0.462 0.562 0.677 0.504
PLAT 0.557 0.574 0.574 0.492 0.567 0.607 0.561
PACH 0.534 0.534 0.586 0.5 0.579 0.759 0.582
TROC 0.6 0.554 0.646 0.569 0.625 0.646 0.606
SAXI 0.508 0.538 0.615 0.6 0.625 0.754 0.606
TETR 0.571 0.603 0.635 0.524 0.629 0.73 0.615
GRIS 0.607 0.623 0.656 0.574 0.65 0.754 0.644
CNES 0.705 0.623 0.656 0.607 0.683 0.672 0.657
CERC 0.646 0.646 0.646 0.585 0.688 0.769 0.663
AUCU 0.641 0.672 0.688 0.562 0.667 0.781 0.668
HAMA 0.597 0.645 0.677 0.645 0.705 0.758 0.671
VITI 0.721 0.656 0.656 0.656 0.667 0.689 0.674
PROS 0.585 0.631 0.723 0.646 0.75 0.815 0.691
AMPE 0.738 0.639 0.672 0.689 0.75 0.787 0.712
DISA 0.708 0.677 0.708 0.692 0.797 0.815 0.732
LOPE 0.688 0.703 0.688 0.719 0.81 0.828 0.739
MYRO 0.569 0.677 0.708 0.661 0.734 0.831 0.697

(a) Abbreviations as in Table III.
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Publication:The Botanical Review
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Date:Jul 1, 2005
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