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Early Evolution of (): Insights from Phylogeny Biogeography, and Comparative Ecology Author(s): W. Scott Armbruster Source: Annals of the Missouri Botanical Garden, Vol. 81, No. 2 (1994), pp. 302-316 Published by: Missouri Botanical Garden Press Stable URL: http://www.jstor.org/stable/2992100 Accessed: 14-10-2016 12:16 UTC

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This content downloaded from 132.198.50.13 on Fri, 14 Oct 2016 12:16:01 UTC All use subject to http://about.jstor.org/terms EARLY EVOLUTION OF W. Scott Armbruster2 DALECHAMPIA (EUPHORBIACEAE): INSIGHTS FROM PHYLOGENY, BIOGEOGRAPHY, AND COMPARATIVE ECOLOGY'

ABSTRACT

Dalechampia contains over 120 and occurs throughout the lowland tropics of Asia, , and the New World. Most species in both the Old and the New World secrete terpenoid resin from large glandlike aggregations of bractlets in the pseudanthial inflorescences (blossoms) and are pollinated by that collect resin for use in nest construction. Using comparative chemical, morphological, and ecological data and phylogenetic analyses, I attempt to ascertain the early evolutionary and biogeographic events that led to the present distribution of species, character states, and pollination systems throughout the tropics. Available evidence suggests the originated in western Gondwana or in the mid Cretaceous or early Tertiary, respectively, and spread throughout the tropics by the rafting of land masses, or by migration across higher latitudes when they had subtropical climates, or both. There is some evidence for two migrational events between the Old and New Worlds. The original pollination system may have involved pollination by pollen-collecting or by fragrance-collecting male euglossine bees. The origin of pollination by resin-collecting bees appears to have been a consequence of a preadaptation (exaptation): the earliest Dalechampia apparently used triterpene resins to defend flower parts against attack by herbivores and/or microbes, and resin secondarily assumed the role of pollinator reward. The mutualistic relationship with resin-collecting bees may have originated independently in the Old and New Worlds.

Trans-oceanic disjunctions of similar spe- record. The development of powerful computer- cies have intrigued plant biologists since the earliest assisted methods of phylogeny reconstruction, how- botanical explorers began to report them. We have ever, now makes it realistic to attempt retrospective long wondered how such disjunctions arose, when analysis of ancient biogeographic and evolutionary and how dispersal occurred, and how populations processes in the absence of a fossil record (see evolved in isolation from each other. Disjunctions Donoghue, 1989). The field of vicariance bioge- create natural evolutionary experiments in which ography represents one such approach in its at- two or more populations of similar genetic stock tempt to use analyses of phylogenetic relationships evolve independently in response to local environ- of several independent taxa as an aid to ascertain- mental conditions. An interesting challenge is to ing the processes that affected the distribution of unravel the history of disjunctions and reconstruct those taxa (see review in Humphries & Parenti, the evolutionary events that have occurred since 1986). the isolation of plant populations. In the present paper I consider four questions Research on this topic has rarely proceeded about the early evolutionary and biogeographic beyond the phase of description of the distributions events that affected the members of the pantropical of disjunct sister taxa and their taxonomic rela- euphorb genus Dalechampia: (1) Where and when tionships. This is because research on historical did the genus originate? (2) What series of events phenomena, especially those as ancient as the events led to the present geographical distribution of spe- creating trans-oceanic disjunctions, is extremely cies, character states, and pollination systems? (3) difficult, and until recently required a detailed fossil What was the original pollination system in the

' I thank M. Huft and G. L. Webster for organizing the symposium that elicited this contribution, D. Lees and L. D. Otero for generously providing me with unpublished data, and M. E. Edwards, G. Levin, P. M. Richardson, and an anonymous reviewer for comments on earlier versions of this manuscript. Research was supported by grants BSR- 8509031, BSR-9006607, and BSR-9020265 from the National Science Foundation (USA) and a grant from the National Geographic Society. 2 Department of Biology and Wildlife and Institute of Arctic Biology, University of Alaska-Fairbanks, Fairbanks, Alaska 99775-0180, U.S.A.

ANN. MISSOURI BOT. GARD. 81: 302-316. 1994.

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genus, and how did the early diversification of grance-collecting male euglossine bees (: pollination systems occur? (4) How, when, and ) (Armbruster & Webster, 1979; Arm- where did the novel mutualism with resin-collecting bruster et al.,, 1989; Armbruster et al., 1992). bees arise? Using the cladistic method of phylogeny These bees apparently use fragrances as precursors reconstruction, I develop explicit hypotheses ad- in the biosynthesis of sex pheromones (Dressler, dressing the four historical questions. I evaluate 1982; Whitten et al., 1989). Several species in the hypotheses by considering independent data on the Neotropics and in Madagascar appear to pro- the relationships between the and their her- duce no reward for pollinators other than pollen; bivores and pollinators. these species are pollinated by pollen-collecting bees and (Armbruster et al., 1993). Species of Dalechampia are found throughout NATURAL HISTORY AND DISTRIBUTION OF the lowland tropics of Asia, Africa, and the New DALECHAMPIA World, although the greatest diversity is expressed Dalechampia is distinctive within the Euphor- in South America (Fig. 1). Species bearing resin biaceae: the ca. 120 species have pseudanthial glands (and pollinated by resin-collecting bees) are inflorescences (blossoms) in which usually 3 pistil- by far the most widespread; they occur in every late flowers and usually 4-16 staminate flowers major region where Dalechampia is found, except are united into subterminal and terminal cymules, Madagascar. Those species pollinated by male eu- respectively. Close examination of the Dalecham- glossine bees are necessarily restricted to the Neo- pia inflorescence, however, indicates that its ar- tropics, because euglossines are endemic to the rangement is probably homologous to that of the New World. Species lacking the resin gland and inflorescences of and (although pollinated by pollen-seeking insects are most di- in these taxa the inflorescences are not pseudan- verse in Madagascar, but are also found in northern thial, i.e., do not function as single pollination units South America and southern Central America. as in Dalechampia) (Webster & Webster, 1972). Several authors have concluded that the gland- These three taxa are also similar in habit. Unlike less species found in Madagascar form the most most other euphorbs, Tragia and Plukenetia com- basal species group in the genus (Michaelis, 1924; prise viny species and Dalechampia comprises Magin, 1987), while Webster & Armbruster (1991) mostly viny species. Tragia and Dalechampia are considered the glandless species of northern South also similar in having urticating, crystaliferous tri- America (sect. ) to form probably chomes of virtually identical morphology (Webster the most basal group. It is possible that the Mad- & Webster, 1972). For these reasons, Webster agascan and South American glandless species, (1994) has recently proposed that Dalechampia which share numerous characteristics, form a sin- be included in tribe Plukenetieae (with Tragia and gle basal monophyletic or paraphyletic cluster of Plukenetia) rather than isolated in its own tribe as species. This raises the possibility that Dalecham- in earlier treatments (e.g., Webster, 1975). The pia has a complex biogeographic history, with striking similarities among these three genera and multiple migrations among the continents and in- their inferred close relationship make it possible to dependent evolution of the mutualism with resin- use, with considerable confidence, Tragia and Plu- collecting bees in the Old and New World tropics kenetia as candidate outgroups in the phylogenetic (Armbruster & Mziray, 1987). Alternatively, if the analyses described below. resemblance between Madagascan species and Despite the relatively uniform blossom mor- members of section Rhopalostylis is the result of phology in Dalechampia, there is considerable homoplasy (character convergence and/or rever- variation in the reproductive biology. Most species sals), there may be no reason to reject a very simple in both the Paleotropics and Neotropics offer resin biogeographic history involving an origin in the as a pollinator reward and are pollinated by female New or the Old World, followed by dispersal to the or worker bees that collect resin from a variety of other hemisphere. plant sources and use it in nest construction (Cam- Armbruster & Mziray (1987) proposed four al- merloher, 1931; Armbruster & Webster, 1979; ternative dispersal hypotheses that could explain Armbruster, 1984; Armbruster & Mziray, 1987). the present distribution of Dalechampia species: The resin is secreted by a cluster of modified bract- (1) recent long-distance dispersal of species among lets (the "resin gland") associated with the sta- continents, (2) migration across mid- to high-lati- minate flowers (Webster & Webster, 1972). About tude land bridges during the Tertiary, when these a dozen species in the New World offer fragrances latitudes had subtropical climates, (3) a nearly con- as a pollinator reward and are pollinated by fra- tinuous western Gondwanan distribution in the mid

This content downloaded from 132.198.50.13 on Fri, 14 Oct 2016 12:16:01 UTC All use subject to http://about.jstor.org/terms J., ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~

FIGURE 1. Approximate distribution and number of species of Dalechampia in the Paleo- and Neotropics.

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to late Cretaceous disrupted by subsequent conti- polarize characters and specify ancestral character nental drift, and (4) distribution of primitive Dal- states, and the outgroups were eliminated. These echampia in South America, Africa, and Mada- procedures left unaltered the relative positions of gascar by continental drift, followed by extinction Old and New World taxa. of primitive species in Africa and a second migra- Iterative cladistic runs were conducted to de- tion (either by long-distance dispersal or migration termine the sensitivity of cladistic results to initial via higher latitudes) of more derived species be- assumptions about character reversibility (Table 2). tween South America, Africa, and Asia. Circum- I varied the assumption of character reversibility stantial evidence they provided supported the sec- (reversible vs. irreversible between plesiomorphic ond, third, and fourth hypotheses, but not the first. [primitive] and apomorphic [derived] states) for They did not attempt to identify the site of origin each of three selected characters, and in all possible of the genus nor the direction dispersal events. The combinations of the three characters. purpose of the present study is to use phylogenetic I then examined each of the numerous maxi- analyses of the New and Old World species to mally parsimonious trees to determine the simplest refine these biogeographic hypotheses and specify biogeographic and evolutionary scenarios that could possible sites of origin of the genus, directions of explain the distribution of taxa, character states, dispersal, pollination ecology of the earliest species, and pollination systems and were consistent with and the site(s) of origin of the novel mutualism the tree. This was accomplished by manually map- with resin-collecting bees. ping distribution and pollination ecology data onto each tree using the parsimony assumption (see PHYLOGENETIC INFERENCE Maddison & Maddison, 1992).

METHODS

RESULTS To reconstruct phylogenetic relationships among Old and New World species of Dalechampia, I When all characters were assumed reversible, conducted cladistic analyses on a data set of 46 cladistic analysis of the set of 34 taxa yielded 436 morphological characters (Table 1) from 25 neo- equally parsimonious trees (120 steps, consistency tropical, 4 African, and 3 Madagascan species of index [CI] = 0.47). The large number of equally Dalechampia and representatives of two sister parsimonious trees reflects instability in the place- genera, Tragia and Plukenetia, to serve as possible ment of a few similar taxa (Fig. 2). The gland outgroups (Appendix). The species of Dalecham- characteristics, pollination ecology, and geograph- pia were chosen to represent the major species ical distribution of the various ancestral taxa (nodes groups in the genus. I used the heuristics algorithm of the tree) were inferred by parsimony from the of PAUP 3.0 (see Swofford, 1993) on a Macintosh distribution of these characteristics across the ex- microcomputer to find the shortest trees. In this tant taxa (Maddison & Maddison, 1992). "Map- analysis ancestral states were not specified (i.e., ping" of characteristics onto the consensus tree characters were not polarized). Instead, PAUP de- allowed inference of the history of these ecological termined the ancestral states through global par- and biogeographic features. Despite the abundance simony (Maddison et al., 1984), selecting the more of equally parsimonious trees, the evolutionary and parsimonious of the two sister taxa to be the out- biogeographic implications of this cladistic analysis group. I used MacClade 3.0 (see Maddison & Mad- generally supported Hypothesis 1 (Table 3): Dal- dison, 1992) to explore alternate tree topologies, echampia originated in the Neotropics or western analyze character evolution, assess tree congru- Gondwana, and the earliest species were initially ence with alternative biogeographic hypotheses, and pollinated by either fragrance-collecting male eu- produce graphics. glossines or pollen-collecting insects (Figs. 2, 3). After an initial run with the full set of taxa Dalechampia evolved a mutualistic (pollination) (including the sister genera), I eliminated all but relationship with resin-collecting bees in the Neo- one member of each stable, well defined lade of tropics, and relatively recently in the genus's evo- neotropical species and all but two of the very lutionary history a resin-reward species colonized similar taxa in the paraphyletic section Rhopalo- Africa. More recently, there occurred a migration stylis. This reduced the number of New World from Africa to Madagascar. The colonists of Mad- taxa to 11 and Old World taxa to 4. The decreased agascar apparently evolved pollination by pollen- number of taxa greatly reduced PAUP run time collecting bees and/or beetles just after they col- on the computer. To further reduce run times the onized Madagascar. results of the initial cladistic analysis were used to Cladistic analysis of the reduced set of taxa

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TABLE 1. Characters and character states used in TABLE 1. Continued. phylogenetic analyses. The "0" character state is the ancestral condition, as determined by global-parsimony 33. Pollen shape: 0 = prolate; 1 = subspherical. outgroup analysis. * indicates character was not used in 34. Seed surface: 0 = smooth; 1 = rugulose; 2 = the phylogenetic analysis. tuberculate. 35. Seed shape: 0 = round; 1 = 3-angled; 2 = lentic- 1. Nature of proximal involucral bract: 0 = stipuli- ular; 3 = slightly flattened. form; 1 = involucral. 36. Petiole of proximal involucral bract: 0 = present; 2. Nature of distal involucral bract: 0 = stipuliform; 1 = absent. 1 = involucral. 37. Pollen exine: 0 = reticulate; 1 = psilate. 3. Position of proximal involucral bract: 0 = separated 38. Relative size of pistillate sepals in fruit: 0 =

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TABLE 2. Consequences of varying initial assumptions of reversibility of characters upon the biogeographic/ evolutionary conclusions drawn from the most parsimonious trees obtained by cladistic analysis of the reduced list of Dalechampia taxa. Numbers indicate biogeographic/evolutionary hypothesis(es) with which the most parsimonious trees were consistent (see Table 3). Numbers in parentheses indicate the proportion of maximally parsimonious trees consistent with each hypothesis.

In combination with character

Character assumed irreversible Alone 20 41 17, 20

17. Fusion of staminate bracts 2 (96%)' 3 (60%)2 3 (100%)3 4 (3%) 2, 3 (33%) 3, 4(1%) 5(4%) 2, 5 (4%)

20. Presence of resin gland or its vestige 3 (60%)2 - 3 (100%) 3 3, 5 (33%) 5 (4%) 2, 5 (4%)

41. Presence of sterile arms in staminate 3 (100%)3 3 (100%)3 pleiochasium

None 1 (100%) -

IN = 252 equally parsimonious trees. 2 N = 114 equally parsimonious trees. 3N = 42 equally parsimonious trees. 4N = 50 equally parsimonious trees.

though the shift to the connate condition may not 252 maximally parsimonious trees, 96% of which be expected to occur frequently, it seems even less supported HI (Table 2). In this hypothesis, Dale- likely that the connate involucre would split up into champia originated in the Neotropics or western the "correct" number of bractlets, in the arrange- Gondwana, a glandless stock colonized the Paleo- ment that recreates the original relationship be- tropics (by the breakup of Gondwana or migration tween bracts and pleiochasial arms. Thus if there via higher latitudes), the mutualism with resin- is homoplasy in this character, it seems more likely collecting bees originated in the Neotropics, fol- to reflect convergence than reversal. lowed by one or more additional colonizations of The assumption of irreversibility was applied to the Old World from the New by gland-bearing each of these characters in turn and in all possible (resin-producing) species (Fig. 6). combinations. The cladograms from the seven dif- All other assumptions and combinations of as- ferent runs generated hypotheses 3, 2, 5, and 4 sumptions of irreversibility of characters yielded in order of frequency (Tables 2, 3). By far the shortest trees that supported H3 either all or most most commonly supported hypothesis was H3, with of the time (Table 2). Thus it appears that the H2 a distant second. For example, the assumption most likely biogeographic/evolutionary hypotheses that a sterile pleiochasial arm cannot readily be- are H., H1, and H2. Which of these one favors come fertile again resulted in 42 equally parsi- depends not only on whether one assumes char- monious trees that all support H3: Dalechampia acters in general are reversible or irreversible, but originated in the Neotropics or western Gondwana, also on which particular character or combination a glandless lineage colonized the Paleotropics (by of characters are assumed irreversible. Assump- the breakup of Gondwana or migration via higher tions about the irreversibility of certain characters latitudes), mutualisms with resin-collecting polli- have stronger effects on biogeographic conclusions nators evolved separately in the Old and New than others. That is, assumptions of irreversibility Worlds, followed by recolonization of the Neotrop- of certain characters appear to be dominant, in ics by Old World gland-bearing (resin-producing) their effects, over others. The "pecking order" species, extinction of the glandless species from apparent in Table 2 is Character 41 > Character most of Africa, and their persistence in Madagascar 20 > Character 17. (Fig. 5). All of the phylogenetic hypotheses derived from The assumption that the fusion of staminate the cladistic analyses lead to two basic conclusions. bracts is irreversible, when taken alone, produced (1) Dalechampia originated in the Neotropics or

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) z = < 0 o < < D < = 2WU w Ir <2)j

Hz e- T 1J C-CL D l5J c< 0cn = c0 ca- I

z~~~~~~~~ \\\\\\\\ > o < ETRPC

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M< I Iequivocal

FIGURE 2. Consensus tree for set of 32 Dalechampia species and two candidate outgroups (Tragia and Plukenetia) based on assumption that all characters are reversible. Taxa with unstable arrangements in the 436 maximally parsimonious trees are indicated by polytomies (points of branching of more than two taxa).

western Gondwana. (2) The earliest species were SPECIALIST HERBIVORES ON DALECHAMPIA pollinated by pollen-collecting insects or fragrance- There are several genera of nymphalid butter- collecting male euglossine bees. Uncertainty re- flies whose larvae appear to be specialist folivores mains as to when and in which direction dispersal on New and Old World Dalechampia. The phy- between the Old and New Worlds occurred. logenetic relationships among the New and Old World may give us some clues about TESTS OF HYPOTHESES the history of their and their host plants' migrations There are several sources of independent data among the Neotropics and Paleotropics. that could be used to evaluate the biogeographic/ Assuming that specialist Dalechampia folivores evolutionary hypotheses generated by phylogenetic feed only on Dalechampia, one can make several analyses. These include information on the rela- specific predictions about the phylogenetic rela- tionships among specialist herbivores on Old tionships between those of the New and Old Worlds, and New World Dalechampia, the chemical de- depending on the biogeographic scenario used to fense systems that Dalechampia uses against her- account for their present distribution. (1) If the bivores, details of pollination biology of Old and initial dispersal of Dalechampia from the New New World Dalechampia, and morphological de- World to the Old occurred by long-distance dis- tails of the resin gland of Old and New World persal after the continents achieved close to their species. present positions, the herbivores in the

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cn < ?c < < I z (D w ( = < a: < < ? fi Oj _ -

C /)W < ZyC/) _j mL.1. ( M0

C/) < r z < 0 0 PLE-O LECIN INSECTS

TreeLength: 1 17 POLLINATION

LZPOLLEN-COLLECTING INSECTS

RESIN-COLLECTING BEES

FRAGRANCE-COLLECTING BEES

equivocal

FIGURE 3. Same cladogram as is in Figure 2, with pollination systems mapped onto the branches.

Old and New Worlds should be completely unre- tinuous population of the herbivores to also disperse lated. This is because it is extremely unlikely that into the Old World. (3) If the initial dispersal from both host plant and herbivore would have become the New World to the Old occurred by a continuous established in the Paleotropics by long-distance dis- population being split into two or more populations persal from the New World, and the Old World by the rafting apart of the continents (the breakup herbivore fauna would more likely be the result of of Gondwana) in the Cretaceous, the Old and New members of the local butterfly fauna evolving to World herbivores should again be sister taxa, but feed on Dalechampia. (2) If the initial dispersal not as closely related as in the second scenario. from the New World to the Old occurred by mi- There is some ecological information available gration of a semi-continuous population stretching on butterfly herbivores that feed on Dalechampia across and Europe or Asia in the (Table 4; see Armbruster, 1983; Armbruster & early to mid Tertiary, when these continents had Mziray, 1987; DeVries, 1987). Unfortunately there subtropical climates, the butterfly herbivores in the is not yet detailed information available on their Old World should be closely related sister taxa of phylogenetic relationships. The systematic (Table the New World species. This is because a semi- 4) and phylogenetic information that is available continuous population of host plants across the indicates a close phylogenetic relationship between higher latitudes should have allowed a semi-con- Old and New World taxa, possibly forming two

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TABLE 3. Five most parsimonious biogeographic hy- World could be derived from Tragia-feeding an- potheses derived from the cladistic analyses under varying cestors. In this case phylogenetic relationships assumptions about character reversibility. among lepidopteran herbivores may yield insights into the biogeographic history of Tragia, but not H1. The genus and the resin-collection mutualism of Dalechampia. originated in the New World, with a subse- quent migration to the Old World from the EVOLUTION OF THE RESIN REWARD SYSTEM New and the loss of the resin-collection mu- tualism in Madagascan taxa. How likely is it that an unusual pollination sys- H2. The genus originated in the New World or tem such as pollination by resin-collecting bees western Gondwana; an initial migration (or could have originated more than once within Dal- rafting) to the Old World from the New echampia? Elsewhere in the plant kingdom it has was followed by the evolution of the resin- apparently originated only one other time, in Clusia collection mutualism in the New World, and (Guttiferae) (Armbruster, 1984). Therefore, it seems then by a second migration to the Old at first highly unlikely that pollination by resin- World by gland-bearing species. collecting bees would have arisen multiple times in H3. The genus originated in the New World or western Gondwana; an initial migration (or the genus. Any biogeographic scenario invoking rafting) to the Old World was followed by this would also seem improbable. Consideration of the independent evolution of the resin-col- how the system arose, however, makes multiple lection mutualism in Old and New Worlds, origins of the relationship seem more probable. followed by a migration of gland-bearing species to the New World from the Old. TABLE 4. Provisional phylogenetic classification and H4. The genus and the resin-collection mutualism host-plant associations of lepidopteran herbivores feeding originated in the New World, followed by a on Dalechampia and related genera. Systematic rela- migration of gland-bearing species to the tionships and host plant information from Jenkins (un- Old World, loss of the mutualism in Mada- published manuscript), Armbruster & Mziray (1987), gascar, and finally recolonization of the Ackery (1988), Otero (1990), and D. Lees (unpublished New World by gland-bearing species. data). H5. The genus and the resin-collection mutualism

originated in the New World, followed by Neotropics Paleotropics two or more migrations of gland-bearing species to the Old World and subsequent recolonization of the New World by gland- Subfamily Eurytelinae bearing species. Tribe Neptini Neptis (T', A, others)

Tribe Eurytelini Biblis (T) Byblia (D, T, P) groups with vicariant genera in both areas (Jenkins, Mestra (T, D) Mesoxantha (T) unpublished manuscript; Armbruster & Mziray, Neptidopsis (D, T) 1987; Otero, 1990; Ackery, 1988). This obser- Ariadne (T, R, D, vation generally supports the predictions of the Te, Ac) hypotheses of early Dalechampia "migration" by Eurytela (T, R, D, Te) continental drift and migration in the Tertiary via Tribe Epicaliini higher latitudes. It does not support the hypothesis Hamadryas Sallya (D, T, others) of recent long-distance dispersal (see Armbruster (D, T) & Mziray, 1987, for additional discussion). Thus Ectima (D) the evidence from the relationship among the lep- Panacea (D??) Batesia (D??) idopteran herbivores of the Old and New Worlds Catonephele supports the hypotheses that show a fairly early (A, D, V) colonization of the Old World from the New. Myscelia (D, Ad) The observation that many of the lepidopterans Nessaea (P, A) that feed on Dalechampia may sometimes also Tribe Dynamini feed on Tragia (Table 4), however, raises another Dynamine (D, T) possibility. It is possible that Tragia and its her- Abbreviations for host plants: A = Aichornia, Ac = bivores achieved a pantropical distribution prior to , Ad = Adelia, D = Dalechampia, P = Plu- Dalechampia. If this were true, then the lepidop- kenetia, R = Ricinus, T =Tragia, Te = Tetracarpium, terans now specializing on Dalechampia in the Old V = Veconcibea.

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2 < C/) 0 2 J0 W U)~~~ 0 0 L W S D E E C] nZL > 11 C P 7 C/) 0 0 _ 0 D 0 < < j M C Ct) 0 LL C/) H Cl) Ir L 0L 0 0 03 0 0 0 0 0 0 0 0 0 0 U U a U

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FIGURE 4. Consensus tree for the simplified set of taxa, assuming that all characters are reversible. The figure shows the species distribution mapped onto the cladogram and origins of the mutualism with resin-collecting bees ("resin mutualism" = RM). Taxa with unstable arrangements in the 50 maximally parsimonious trees are indicated by polytomies.

In all Dalechampia species that reward polli- Species of Dalechampia identified in cladistic nating bees with triterpenoid resins, the secretory analyses as diverging early in the evolution of the bractlets are clustered into a glandlike structure in genus do not use resin-collecting bees as pollinators, the staminate subinflorescence. Comparative mor- although they do produce resins from inflorescence phological studies of gland-bearing and non-gland- bractlets. Character mapping indicates that the bearing species show that the bractlets of the gland common ancestor of the rest of the genus also had are homologous to those that subtend the staminate this feature. This suggests that resin secretion in flowers (and cover them in bud) in glandless species the genus first arose as a way of protecting repro- (Armbruster, unpublished obs.). The bractlets also ductive tissues from attack by insect herbivores or secrete the same mixture of oxygenated triter- microbes. Its presence in the inflorescence set the penes, even though the compounds play no role in stage for resin-collecting bees to visit flowers to pollination. These bractlets and their resinous se- collect the resin for nest construction. These bees cretions would instead appear to play a role in secondarily assumed the role of pollinators. The defending the staminate flowers from depredation plant, in response, evolved higher rates of resin by herbivorous insects or microbes. Also consistent secretion, and the bractlets became organized into with this idea is that some of the same compounds a gland from which the resin could be collected are also secreted by glands along the margins of more efficiently. Thus the resin reward system young leaves, stipules, and/or sepals of many Dal- probably evolved from a preadaptation (exapta- echampia species, where they appear to play a tion). Because the preadaptation was apparently role in defending those parts from herbivores (Arm- "in place" very early in the evolution of the genus, bruster, Howard & Debevec, unpublished data). it was probably present in the first Dalechampia

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MADAGASCAR

equivocal

FIGURE 5. Consensus tree for the simplified set of taxa, assuming that all characters are reversible except character 41 (see Table 2), which was assumed irreversible. The figure shows the species distribution mapped onto the cladogram and origins of the mutualism with resin-collecting bees ("resin mutualism" = RM). Taxa with unstable arrangements in the 42 maximally parsimonious trees are indicated by polytomies.

to arrive in the Old World, as well as in the New Cremophyllum have resin glands composed of a World species. This is confirmed by the secretion single concentric whorl of resiniferous bractlets de- of "defense" (non-reward) resins by many of the rived from three pleiochasial arms. The gland-bear- Madagascan species as well as several members of ing species of the Old World and most of the more section Rhopalostylis. Thus the stage would have derived species of the New World have resin glands been set similarly in both the Paleotropics and composed of two rows of nearly parallel platelike Neotropics for the evolution of the mutualism with bractlets which are apparently derived from four resin-collecting bees. Resin-collecting bees were pleiochasial arms. The two forms of gland are con- probably already present in both the Paleo- and sistent with two origins of the resin gland. The Neotropics (Michener, 1979). It thus seems not so distribution of the two gland types is consistent with unlikely that the resin-collecting mutualism might the phylogeny that supports biogeographic Hy- have originated independently in both places. pothesis 3: one migration to the Old World, a Another observation is consistent with two sep- separate origin of the resin gland in the Old and arate origins of the resin gland and resin-reward New Worlds, followed by a recolonization of the system. If the resin gland originated independently New World by species bearing the Old World gland more than once, we might expect to see subtle type (Fig. 5). differences in the structure of the gland. If the There are two final aspects of the pollination resin glands throughout the genus were of identical ecology that may have bearing on our biogeograph- structure, it would suggest a single origin of the ic hypotheses. First, if Dalechampia had tight gland. There are actually two distinct kinds of resin relationships with resin-collecting pollinators prior gland. Members of sections Dioscoreifoliae and to its colonization of the Old World (as it apparently

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< < Cl) 0 0 < LL ~~~~~~~~LL Z ?0 2 2 2 D 11 0 C) 0 F C) Cl) I 0 L_ 0 0 0 0 0 o 0 0 0 0 0 U E

DISTRIBUTION /III NEOTROPICS

AFRICA

MADAGASCAR

FIGURE 6. Consensus tree for the simplified set of taxa, assuming that all characters are reversible except character 17 (see Table 2), which was assumed irreversible. The figure shows the species distribution mapped onto the cladogram and origins of the mutualism with resin-collecting bees ("resin mutualism" = RM). Taxa with unstable arrangements in the 252 maximally parsimonious trees are indicated by polytomies.

did with lepidopteran symbionts), and it colonized abandoning pollination by resin-collecting bees and the Old World by some mode other than long- reverting to pollination by pollen-collecting bees distance dispersal, we might expect to see sister and beetles. This is surprising because pollination genera of bees visiting Dalechampia on either side by resin-collecting bees appears to be a very suc- of the Atlantic as we observed in the . cessful pollination system, as evidenced by its abun- We do not see this; there are not close phylogenetic dance in the genus (some 80% of Dalechampia relationships between the major pollinators in the species are pollinated in this way). If this occurred, New World and the Old. The most likely candi- we could expect there to be some disadvantage to dates, Hypanthidium on neotropical Dalecham- pollination by resin-collecting bees in Madagascar. pia and Pachyanthidium on South African Dal- There might actually be such a disadvantage; ac- echampia (Steiner & Whitehead, 1990; cording to C. D. Michener (pers. comm.), except Armbruster & Steiner, 1992), are not particularly for tiny Trigona spp., which are often too small close within the (C. D. Michener, pers. to be effective pollinators (see Armbruster & Mzi- comm.). This suggests dispersal between continents ray, 1987; Armbruster, 1988), resin-collecting bees either was long-distance over oceanic barriers to are notably uncommon in Madagascar. bees, or occurred prior to the evolution of the resin mutualism (consistent with H3 but not HI), or some- DISCUSSION AND CONCLUSIONS how occurred without the bees "following" the plant. In this study I have tried to illustrate the ad- A somewhat surprising feature of HI is that vantages it of using the results of cladistic analyses has the Dalechampia that colonized Madagascar to develop and refine hypotheses about the bio-

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geographic and evolutionary history of extant or- America in the late Cretaceous/early Tertiary, ganisms for which there are no detailed fossil rec- evolved a mutualism with oil-collecting bees (based ords. However, many uncertainties remain, and it on oil secretion by calyx glands), and more recently is essential to explore through iterative analysis the colonized the Paleotropics, where the mutualism consequences of making different assumptions about was lost (Raven & Axelrod, 1974; Anderson, 1979). character evolution. The use of molecular data to A recent re-evaluation of floral morphology of infer phylogeny may solve some of the problems Malpighiaceae by Vogel (1990) leads to an alter- and uncertainties illustrated here, but even molec- native conclusion: the Malpighiaceae originated in ular phylogenies often may be ambiguous (see San- western Gondwana in the mid-Cretaceous, and con- derson & Donoghue, 1989). Tests of phylogenetic tinental drift resulted in primitively glandless spe- and historical hypotheses using independent data cies occurring in both the Paleotropics and Neo- (such as information on symbionts) are necessary tropics. One (or several?) lineage(s) in the Neotropics if we are to progress beyond the stage of hypothesis evolved a mutualism with oil-collecting bees, and, generation. later, members of this advanced lineage recolonized In the present study, I used cladistic results to the Paleotropics (Vogel, 1990). This scenario is generate and refine several hypotheses explaining similar to Hypotheses 2 and 3 for Dalechampia: the present distribution of Dalechampia species the presence of species with predominately ple- and their pollination systems. Three competing hy- siomorphic character states in the Old and New potheses seem most likely, and independent data Worlds is explained by a widespread, possibly are needed to distinguish among these. In partic- Gondwanan distribution of Dalechampia during ular, information on the genetics and development the mid-Cretaceous to early Tertiary. The close of flowers and inflorescences would be valuable, similarity of some of the derived species of the Old because the phylogenetic and biogeographical in- and New Worlds is explained by a second trans- ferences made were sensitive to assumptions about Atlantic dispersal event in both Malpighiaceae and the reversibility to the primitive character states Dalechampia. It will be interesting to see if ad- of certain inflorescence characters. ditional evidence continues to support these earlier Independent ecological information was used to origins and more complex biogeographic scenarios evaluate the likelihood of the hypotheses generated for Dalechampia, Malpighiaceae, and possibly oth- from phylogenetic information. Data from insect er plant groups. herbivores and pollination of Dalechampia best support Hypothesis 3. The evidence, however, does

not exclude Hypotheses 1 or 2. Hypothesis 1 de- LITERATURE CITED pends on the assumption that all morphological ACKERY, P. R. 1988. Hostplants and classification: A characters can revert to their primitive stages. review of nymphalid butterflies. Biol. J. Linn. Soc. Whether this is realistic remains to be determined. 33: 95-203. It appears that Dalechampia originated in the ANDERSON, W. R. 1979. Floral conservatism in neo- Neotropics or western Gondwana. The earliest spe- tropical Malpighiaceae. Biotropica 11: 219-223. cies of Dalechampia probably employed fra- ARMBRUSTER, W. S. 1983. Dalechampia scandens. Pp. 230-233 in D. H. Janzen (editor), Costa Rican grance-collecting male euglossine bees or pollen- Natural History. Univ. Chicago Press, Chicago, Il- collecting insects as pollinators. The mutualism with linois. resin-collecting bees may have evolved separately 1984. The role of resin in angiosperm polli- in the Old and New Worlds (Hypothesis 3), or may nation: Ecological and chemical considerations. Amer. have evolved only in the New World (Hypotheses J. Bot. 71: 1149-1160. 1988. Multilevel comparative analysis of mor- 1 and 2). phology, function, and evolution of Dalechampia The simplest biogeographic scenario is proposed blossoms. Ecology 69: 1746-1761. in Hypothesis 1: Dalechampia originated in the & W. MZIRAY. 1987. Pollination and herbi- New World, evolved a mutualism with resin-col- vore ecology of an African Dalechampia (Euphor- biaceae): Comparisons with New World species. Bio- lecting bees there, and subsequently colonized Af- tropica 19: 64-73. rica and Asia, and most recently, Madagascar, & K. E. STEINER. 1992. Pollination ecology where the mutualism with resin-collecting bees was of four Dalechampia species (Euphorbiaceae) in lost. This explanation is similar to explanations of northern Natal, South Africa. Amer. J. Bot. 79: 306- the dispersal history of a number of plant groups 313. & G. L. WEBSTER. 1979. Pollination of two (Raven & Axelrod, 1974). For example, the usual species of Dalechampia (Euphorbiaceae) in Mexico explanation of pantropical distribution of the Mal- by euglossine bees. Biotropica 11: 278-283. pighiaceae is that the group originated in South , A. L. HERZIG & T. P. CLAUSEN. 1992. Pol-

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lination of two sympatric species of Dalechampia WHITTEN, W. M., A. M. YOUNG & N. H. WILLIAMS. (Euphorbiaceae) in Suriname by male euglossine bees. 1989. Function of glandular secretions in fragrance Amer. J. Bot. 79: 1374-1381. collection by male euglossine bees (Apidae: Euglos- , S. KELLER, M. MATSUKI & T. P. CLAUSEN. sini). J. Chem. Ecol. 15: 1285-1295. 1989. Pollination of Dalechampia magnoliifolia (Euphorbiaceae) by male euglossine bees (Apidae: APPENDIX. List of specimens studied. Euglossini). Amer. J. Bot. 76: 1279-1285. , M. E. EDWARDS, J. F. HINES, R. L. A. MAHUNNAH D. aristolochiifolia HBK: Armbruster et al. 87-128, & P. MUNYENYEMBE. 1993. Evolution and polli- 87-136 (ALA); Chavez 3067 (MO); Cook & Gilbert 1022 nation of Madagascan and African Dalechampia. (F); Dillon & Turner 1703 (F, MO); Gentry et al. 44120, Research and Exploration 9: 430-444. Hudson 1192, Hutchison & Wright 3852 (MO); Mac- CAMMERLOHER, H. 1931. Bliten Biologie I. Gebriider Bride 3802 (F); Sagastegui et al. 8455, Stein & Todzia Borntraeger, Berlin. 2064 (MO); Stork & Horton 10093, Stork et al. 10563 DEVRIES, P. J. 1987. The Butterflies of Costa Rica and (F); Vargas 131, Woytkowski 5720, 6564, 6834 (MO). Their Natural History. Princeton Univ. Press, D. attenuistylus Armbruster: Armbruster et al. 87-153, Princeton, New Jersey. Armbruster 93-01 (ALA). DONOGHUE, M. J. 1989. Phylogenies and the analysis D. canescens HBK: Armbruster & Herzig 85-119, 85- of evolutionary sequences, with examples from seed 127 (ALA); Haught 1832, Plowman & Vaughan 5354 plants. Evolution 43: 1137-1156. (F); Webster & Armbruster 23651 (ALA). D. capensis DRESSLER, R. L. 1982. Biology of the orchid bees (Eu- Spreng.: Armbruster & Steiner 90-202, Armbruster et glossini). Annual Rev. Ecol. Syst. 13: 73-94. al. 90-203 (ALA); Bayliss 5294, Coetzee 1328, Dahl- HUMPHRIES, C. J. & L. R. PARENTI. 1986. Cladistic strand 1952, Germishuizen 233, Huntley 79, Kemp 760, Biogeography. Clarendon, Oxford. Kerfoot K7301, Strey 11185, Zeyher 245 (MO). D. MADDISON, W. P. & D. R. MADDISON. 1992. MacClade. caperonioides Baill.: Webster et al. 25245 (ALA). D. Sinauer, Sunderland, Massachusetts. chlorocephala M. Denis: Armbruster et al. 90-151; Dorr , M. J. DONOGHUE & D. R. MADDISON. 1984. & Koenders 2987, 2987A, 3024 (ALA, MO). D. cle- Outgroup analysis and parsimony. Syst. Zool. 33: matidijolia Baill.: Armbruster et al. 90-148 (ALA); Croat 83-103. 29424, 30130, 31463, 32153 (MO). MAGIN, N. 1987. The pseudanthium of Dalechampia D. dioscoreifolia Poepp.: Armbruster 79-212, Arm- and its systematic significance. XIV International bruster et al. 85-117, 87-139 (ALA); Beekman 59, Feuil- Botanical Congress, Berlin. [Abstract.] let 417 (CAY); Gentry 6365 (ALA, MO); Gentry et al. MICHAELIS, P. 1924. Blutenmorphologische Untersu- 18696 (MO); Granville et al. 7292 (B, CAY, MO, P); chungen an den Euphorbiaceen. Bot. Abh. 3: 1- Guanchez & Huber 4742 (ALA, VEN); Maas et al. 2226 150. (CAY, U); Oldeman 2067 (CAY, MO, NY, P); Oldeman MICHENER, C. D. 1979. Biogeography of the bees. Ann. B.3227 (CAY, NY, U); Poncy 89 (ALA); Proctor et al. Missouri Bot. Gard. 66: 277-347. 27384 (F); Raynal-Roques 20006 (CAY); Revilla 1710 OTERO, L. D. 1990. Estudio de algunas caracteres para (MO). su uso en la clasificaci6n de Eurytelinae (Lepidoptera: D. ficifolia Lam.: Hatschbach 44381 (F); Webster et Nymphalidae). Bol. Entomol. Venez. 5: 123-138. al. 25007, Webster & Armbruster 25101, 25161 (ALA). RAVEN, P. H. & D. I. AXELROD. 1974. Angiosperm D. fragrans Armbruster: Armbruster & Herzig 85-101 biogeography and past continental movements. Ann. (ALA, NY); Armbruster & Herzig 85-104 (ALA); Maas Missouri Bot. Gard. 61: 539-673. et al. 2320 (MO); Mori et al. 8693 (NY, P). SANDERSON, M. J. & M. J. DONOGHUE. 1989. Patterns D. heteromorpha Pax & Hoffm.: Armbruster 77302, of variation in levels of homoplasy. 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Gard. 55: 130-142. D. "mauesensis" sp. nov.: Murca Pirez 50 (VEN). D. WEBSTER, G. L. 1975. Conspectus of a new classifi- megacarpa Armbruster: Armbruster et al. 85-115, 87- cation of the Euphorbiaceae. Taxon 24: 593-601. 151 (ALA). D. micrantha Poepp.: Armbruster et al. 85- 1994. Synopsis of the suprageneric taxa of 113, 87-150, 87-156 (ALA); Byron & Coelho 443 (MO); Euphorbiaceae. Ann. Missouri Bot. Gard. 81: 33- Garcia-Barriga 14103 (NY); Gentry et al. 29955 (F); 144. Lindeman et al. 214 (U); MacRae & Ruiz 80 (F); Nee & W. S. ARMBRUSTER. 1991. A synopsis of 31877 (MO); Poeppig 2807 (P); Poeppig 7200 (MO); the neotropical species of Dalechampia (Euphorbi- Prance et al. 24587 (NY); Revilla 87 (F, MO, NY); aceae). Bot. J. Linn. Soc. London 105: 137-177. Rimachi 323 (NY); Schomburgk 783 (P); Spichiger & & B. D. WEBSTER. 1972. 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D. osana Armbruster: Burger & Liesner 7278, Burger Armbruster 77-305, 78-409 (ALA). D. shankii (Molina) & Gentry 8962, 9011 B, Gomez 19672, Liesner 1869, Huft: Armbruster 79-213, 91-102, Armbruster & Berg Utley & Utley 1214 (F). 85-128 (ALA); Cuatrecasas 21512, Davidson 6828, Shank D. parvibracteata Lanj.: Jenman 4088 (US); McDow- & Molina 4427, 4475, Standley & Valerio 48588 (F). ell & Gopaul 2264 (ALA, US). D. parvifolia Lam.: Arm- D. spathulata Baill.: Croat 20306, Poeppig 2380, Vigo bruster et al. 90-168, Armbruster & Steiner 90-195 6480, 7693 (MO); Williams 4189 (F). D. subternata (ALA). D. pentaphylla Lam.: Hatschbach 11840, Mexia Muell. Arg.: Armbruster et al. 90-144, 90-150, Arm- 4149, Regnelli 1051 (F); Webster et al. 25215 (ALA); bruster & Hines 90-158, 90-160, 90-162, 90-164 (ALA); Woytkowski 35147 (F). Croat 30708, 30744, 31022, 31065, Dorr 3050, Gentry D. scandens L.: Alexandre 227 (CAY); Armbruster & 11801 (MO); Gillespie 4180, 4181 (ALA, US); Lorence Herzig 85-107, 85-124, Armbruster et al. 87-103, 87- 2097 (MO); Miller & Keating 4527, Phillipson 2492, 107, 87-115, 87-140 (ALA); Benoist 835, 1262 (P); 3050 (ALA, MO). Billiet & Jadin 4332 (BM, CAY); Broadway 444 (US); D. tiliifolia Lam.: Armbruster et al. 85-108, 85- 111, Cremers & Hoff 10608, Feuillet 538, 2969 (CAY); Gen- 87-111, 87-125, 87-138, 87-141 (ALA); Barthelemy try & Revilla 16246, Gentry et al. 22702 (MO); Gillespie 145 (CAY); Broadway 631 (NY); Cremers 9429 (B, CAY, & Persaud 1046, Gillespie et al. 1654, 1655, 1781 (ALA, MO, NY, P, US); Feuillet 1754 (CAY, P); Forest Dept. US); Granville 6940 (B, CAY, P); Harrison 714 (K); Brit. Guy. 5978 (K, NY); Granville 260 (CAY, P, U); Harrison 1769 (K, NY); Hekking 1049 (U); Hitchcock Granville 265 (CAY); Hoff 5357 (B, CAY, NY, P, US); 16770, Irwin BG-71 (US); Irwin et al. 55831 (MO, NY, Mori et al. 15026 (CAY, P); Oldeman B-802 (CAY, U); U, US); Kappler 1888 (P, U); Lall 312 (U); Lanjouw & Picon et al. 1524 (ALA, VEN); Poncy 4 (P); Prevost Lindeman 1114, 1807 (NY, U); L.B.B. (J.T. Serringa) 1808 (CAY, U, US); Sagot 513 (P); Solomon 3248, 7586 12534 (U); Maas et al. 7222 (B, US); Prevost 1456 (MO); Webster & Armbruster 23712 (ALA). D. triphylla (CAY); Reitsma & Reitsma 852 (NY); Sagot 512 (BM, Lam.: Armbruster & Herzig 85-103 (ALA); Barreto 5058, P); Schomburgk 610 (BM); Service Forestier 3077 (U); Henschen 1052 (F); Webster & Armbruster 25182, Service Forestier 4328 (CAY, P, U); Skog et al. 7427 25189, 25218 (ALA). (CAY, NY, P, U, US); Solomon 8899 (MO); Solomon & Plukenetia spp.: Armbruster 78-420, Armbruster et Escobar 12486 (ALA, MO); Wachenheim 25 (P); Web- al. 85-106, 87-110, 87-113, 87-144, Webster & Arm- ster 24143 (NY, U); Webster & Armbruster 23508, bruster 23412 (ALA). 23523, 25105 (ALA). D. schippii Standley: Armbruster Tragia spp.: Armbruster et al. 90-146, Armbruster & 77-303, 78-416, 79-204 (ALA). D. schottii Greenm.: Hines 90-157, 90-159, 90-163 (ALA); Maas 6231 (MO).

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