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DECEMBER I99O MEMOIRS OF THE NEW YORK BOTANICAL GARDEN 64:21V224

The Origin of the -The Evidence from Morphology

Wrrlnu R. AwoeRSoN

Abstract

ANoensoN, W. R. (University of Michigan , North University Building, Ann Arbor, MI 48109-1057, U.S.A.). The origin of the Malpighiaceae-The evidence from morphology. Mem. New York Bot. Gard. 64: 210-224. 1990. The Malpighiaceae are a of some 1200 flowering , of which 850/oare neotropical and the rest paleotropical. Their habits and are very diverse, especially in the , while the are relatively uniform. Calyx glands in most neotropical secrete oils gathered by polli- nating bees, but the glands present on the of four genera in the , where the oil-bees that visit malpighs do not occur, produce sugary similar to that produced by the anatomically similar extrafloral nectaries found on foliar organs in both hemispheres. The in most Malpighiaceae is based on single-flowered units, but in ten neo- tropical genera those units may be cymules. Among diverse types the ancestral condition seems to be colporate. A hypothetical ancestor based on characters that hardly vary supports Engler's view that the Trigoniaceae and Vochysiaceae are the families closest to the Malpighiaceae. An analysis utilizing them as outgroups leads to the conclusion that the likeliest ancestral character-states (inflorescence of cymules, colporate pollen, and dry dehiscent fruits) are heavily concentrated in the New World subfamily Byrsonimoideae, hence my "American" hypothesis that the family originated in the New World in effective isolation from the Old World. I contrast that with Vogel's "Gondwanian" hypothesis, based on the structural and functional similarity of Old World calyx glands to extrafloral nectaries; he proposed that the family originated before the breakup of Gondwanaland and the New World species acquired their oil-producing calyx glands after separation from their Old World relatives. I discuss some of the problems inherent in these hypotheses, and conclude with the hope that new molecular data will enable us to break the impasse imposed by the limitations of the morphological evidence.

Dedication to pursue that interest. During my three years at New York, and subsequently at The University Almost twenty years ago, in 197l,I completed of Michigan, I have had the opportunity to study my Ph.D. and accepted a research position at the and describe the wonderful series of collections New York Botanical Garden. Although my doc- from northern amassed by Bas- toral thesis treated a of the Rubiaceae, my sett Maguire and his collaborators. That treasure real interest since undergraduate days had been continues to provide material and inspiration for york the Malpighiaceae, and I was hired at New my research, and I am often moved to consider 2r0 I eeol ANDERSON: ORIGIN OF THE MALPIGHIACEAE 2tl

how impoverished my career would have been fleshy and dry, and dry dehiscent fruits that may if Bassett had not had the vision, determination, be unwinged, bristly, or variously winged. The and force of personality to do what he did in the winged mericarps are mostly of two types, that Guayana Highland. It is thus with admiration in which each mericarp has its principal wing and appreciation for his extraordinary achieve- dorsal (hereafter referred to as banisterioid) and ments that I dedicate this paper to Bassett Ma- that in which the principal wings are lateral (hi- guire. raeoid). In the Old World genera the fruits are always dry and winged, and with one exception Background Information they dehisce into samaras resembling the two principal samara types found in the New World. The Malpighiaceae are a medium-sized family On that basis Niedenzu (1928) assigned all the oftropical and subtropical flowering plants, com- Old World genera to two tribes, Banisterieae prising some 1200 species assigned to 66 genera. (those with banisterioid samaras) and Hiraeeae About 850/oofthe speciesoccur in the New World, (those with hiraeoid samaras); each tribe was and the balance in the Old World. With two dominated by a large number ofNew World gen- exceptions, no genus or species occurs in both era having similar fruits. I have long felt that hemispher es.S t igmap hy II o n ovatum (Cav.) Nied., Niedenzu applied his characters too me- a and Atlantic coast species of a large chanically, thereby creating several very artificial American genus, has been collected several times groupings of genera. My recognition of the whol- in western . leona(Cav.) Exell ly American subfamily Byrsonimoideae (1977) is a well-established species of western Africa, was a first step in correcting those excesses.The but only with difficulty can it be distinguished Byrsonimoideae have fruits that are indehiscent from its closest relatives in the Caribbean and or dehiscent and fleshy or dry, but none are bris- on the Atlantic coast of Central and South Amer- tly or winged. That paper did not address the ica, H. platyptera DC. and H. multiflora (DC.) problem of the relationships of the Old World Hochr. The rest of Heteropterys, a genus of some Malpighiaceae, which has been complicated 100 species,is entirely American. All writers who somewhat since the time of Niedenzu by the de- have considered these two disjunctions agree that scription of (Ardnes, 1946), a they have probably resulted from dispersal from of Madagascar with a most peculiar winged but Atlantic America to western Africa in geologi- indehiscent fruit. cally recent times. I would be willing to go further All Malpighiaceae are perennials. In they and suggest that at least the may include herbaceous stems from a thickened base, have been introduced into Africa accidentally by of all sizes, small to large , and twin- humans in the last several centuries. The I/e/- ing varying from slender and subherba- eropterys was described from Africa rather early ceous to woody that reach the tops of the (Cavanilles, 1790), but even that was long after tallest rainforest trees. No member of the sub- regular transatlantic travel began, and I cannot family Byrsonimoideae is a ; all are trees or help wondering whether I1e teropterys leonamight shrubs. Both twining and erect habits are found also be a recent transplant from America. In any among the non-byrsonimoids of both New and case, those two paleotropical plants can be ex- Old Worlds, but the great majority ofthose many cluded from further discussion here, and when I species are vines. refer below to the Old World Malpighiaceae my In the New World most species of Malpighi- comments will not apply to Stigmaphyllon ova- aceae bear large paired multicellular abaxial tum or Heteropterys leona. glands on four or all five of the sepals (Fig. 5C, While the flowers of the Malpighiaceae are D). Although they are outside the , those rather uniform, the fruits are extremely diverse glands are accessible to bees visiting the flower (Anderson, 1979b). For that reason, since the because the clawed leave a space through time of Linnaeus fruit characters have furnished which the bee can reach. In a landmark mono- the most important bases for recognizing genera graph, Vogel (I97 4) showed that those calyx and for grouping those genera in tribes and sub- glands, which he called elaiophores, produce oils families. In the New World the full range of fruit that are gathered by female anthophorine bees types occurs, including indehiscent fruits, both of the tribe . Lobreau-Callen (1989) 2r2 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor. 64 has recently confirmed his findings by analyzing The oil-bees that pollinate most New World the secretions from the calyx glands of several Malpighiaceae do not occur in the Old World genera, although she did find traces of in (Vogel, 1974). Almost no one seems to have pub- addition to a preponderance of lipids. I have lished good field observations on the suggested(1979b) that the reason the flowers of of Old World Malpighiaceae, but the large size neotropical Malpighiaceae are so uniform, in of their anthers suggests that they reward their genera that are very diverse in habit and fruit, is with pollen. Since the oil-bees are not that their evolution has been constrained by their available, it is not surprising that most Old World dependence on oil-bees for pollination. Most Malpighiaceae lack calyx glands. According to members of the Byrsonimoideae have ten calyx the descriptions of Niedenzt (1928) and Ardnes glands, two on each of the five sepals. Most non- (1950, 1954) only four genera bear calyx glands. byrsonimoids in the New World have only eight In , which has hiraeoid samaras, most calyx glands, on the four lateral sepals; the an- species have one very large elongated gland, borne terior , which is inaccessible to the bee when on the commissure between the two posterior she is oriented toward the posterior "flag" , sepals and decurrent onto the . Four of is eglandular in those species. A moderate num- the 27 species of Hiptage have one to several ber ofNew World Malpighiaceae lackcalyx glands small glands, and two have an eglandular calyx. completely, and are presumably pollinated by is a genus of some 25 species, most bees for which the only reward is pollen. of them endemic to Madagascar. According to Most genera and species of Malpighiaceae, in Ardnes (1950) some of them have the calyx al- both the New and Old Worlds, bear multicellular ways eglandular but most bear 1-10 small ca- glands on various foliar organs-vegetative lycine glands in at least some populations. The , reduced inflorescence leaves, , and 29 species of and its closely related bracteoles. These glands are usually borne on the segregateRhinopterys have banisterioid samaras or the abaxial surface of the lamina; in and small calyx glands varying in number from one species ( corueae Cuatr. & Croat) none to ten and in position from commissural they occur on the adaxial surflace, and in to (apparently) abaxial and paired (A. ferrugineus several byrsonim o tds (Lo p h a nt her a spp., Sp ach - Engler, fide Niedenzu, 1928: 264). Vogel (1974 ea spp.) one or both of the bracteoles may 66-67) has investigated the anatomy of the calyx terminate in a large stalked gland (Fig. 5A, C). glands tn Hiptage benghalensls (L.) Kurz andAc- It is common for field botanists to observe ants ridocarpus smeathmannii (DC.) Guill. & Perr. removing the nectar from the glands on young and reports that it is similar to that of neo- leaves and bracts of Malpighiaceae, so it comes tropical elaiophores and extrafloral nectaries in as no surprise that when those secretions have both hemispheres; in details he finds the paleo- been analyzed (Vogel, 1974: 64; Lobreau-Callen, tropical calyx glands to be more like extrafloral 1989: 82) they have proved to be rich in sugars nectaries than neotropical elaiophores. On the and lacking the oils present in the secretions from basis of those structural similarities he considers neotropical elaiophores. Although these extraflo- the Old World calyx glands to be homologous ral nectaries are very diverse in size (less than with elaiophores and extrafloral nectaries, in spite 0.5 mm to 4 mm or more in diameter) they are of the fact that they are usually not paired. On quite similar in their basic anatomy to each other the same pages Vogel cites previous work indi- and to the elaiophores found on the sepals of cating that the gland of H ipt age benghale nsis pro- most neotropical Malpighiaceae (Vogel, 1974: duces a sugary nectar and is therefore not an 64). The extrafloral nectaries often occur as paired elaiophore as defined by Vogel. He himself in- structures borne abaxially and near the base of vestigated the calycine secretions in Acridocarpus leaves and bracts, in a position analogous to the smeathmannii and found abundant production position of neotropical elaiophores on sepals. On ofa nectar rich in sugarsand lacking lipids. These the basis of those structural and positional sim- results have been confirmed recently for the same ilarities, Vogel (1974: 64-69; 1990) has asserred two speciesby Lobreau-Callen (1989). that the two kinds of glands must surely be de- In most Malpighiaceae each flower is borne on velopmentally and evolutionarily homologous, a pedicel, subtended by two bracteoles borne at in spite of their different secretions. the apex of a , which is in turn sub- r 9901 ANDERSON: ORIGIN OF THE MALPIGHIACEAE 2r3

FIG. 1. Inflorescence types in the Malpighiaceae. A. Raceme of dichasia; known in the Trigoniaceae and postulated for the Malpighiaceae; the inflorescence diagrammed here is more elaborate than that of lactescens,the only malpigh in which dichasia occur. B. Raceme of cincinni; known in l0 genera of neotropical Malpighiaceae. C. Pseudoraceme (raceme of I -flowered cincinni); this and condensed derivatives of it are present in all other Malpighiaceae, comprising 56 genera, and in some species in 4 of the genera that show condition B. I interpret evolution of these as a reduction series proceeding from A to C. tended by a single (Fig. 1C). In all or some simplest way to summarize the diversity in the speices of ten neotropical genera one finds cy- family's pollen is to say that it is either colporate mules instead of the one-flowered units de- with equatorial pores and colpi at right angles to scribed above. The difference consists in the fact the equator (or some obvious variant on that that one of the two bracteoles subtends a theme), or porate with the pores mostly non- comprising a peduncle, two bracteoles, and a equatorial and the ectoapertures variously ori- pedicellate flower; one of those two bracteoles is ented and modified, or lost completely. Figure 2 in turn fertile, and so on, resulting in a cincinnus shows examples oftricolporate (A & B) and tetra- of 2-10 flowers (Figs. 1B, 5,A.,C). Those genera colporate (C) , as well as two very different are , Blepherendra, , Byrso- porate pollens, one with ectoapertures (D) and nima, , Glandonia, Lophanthera, one without them (E). Lowrie's figure 3.2 is re- Mcvaughia, Spachea, and Verrucularia. ,\lI of produced here (Fig. 3) as a nice summary of the those except Barnebya belong to the subfamily bewildering diversity in the family's pollen. As Byrsonimoideae (Anderson, I97 7, 1979 a). In one that shows, Lowrie considered tricolporate pol- byrsonimoid species (Lophanthera lactescens len to be ancestral in the family and all other Ducke) the cymules are often dichasia instead of types to have been derived from it, ultimately. cincinni. i.e.. both bracteoles subtend flowers in- Lobreau-Callen (1983) also summarized the pol- steadof only one (Fig. lA). Barnebyaisan anom- len of Malpighiaceae as either "colpor6es" or alous genus of uncertain affinities (Anderson & "por6s" and assumed that colporate pollen was Gates, l98l; Lowrie, 1982). All other neotrop- ancestral in the family. The reason for their ical Malpighiaceae, and all paleotropical species, agreement on this point is obvious when one have as the ultimate units of the inflorescence considers the distribution of pollen types in the single flowers instead of cincinni. fossil record and in extant families ofthe Rosidae The pollen of the Malpighiaceae is extremely (Walker & Doyle, 19751'Cronquist, l98l:521\. diverse, and I cannot begin to do justice to that Tricolporate pollen is common in both, while diversity here. For descriptive treatments see the bizarre "porate" types of pollen shown in Lowrie (1982) and Lobreau-Callen (1983 and Figure 2 are scattered; indeed, at least some of earlier papers cited therein, especially 1967). The the grains found in the Malpighiaceae are prob- 2t4 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN lvor. 64 ably peculiar to this family. Tricolporate pollen of the plants and their bees across the widening or types clearly derived from it (syntricolporate, Atlantic. I speculated that the Old World Mal- parasyntricolporate, and tetracolporate) are found pighiaceae, all with wind-dispersed samaras, de- in all genera of the wholly New World subfamily scended from two or more New World Malpigh- Byrsonimoideae, and polycolporate pollens (pores iaceae that were dispersed from west to east, and and colpi 5-8) occur in the New World genera further that in the Old World, where oil-bees Dinemagonum, , , and were not present, the elaiophores degenerated . In the Old World syntricolporate into the calyx glands still present in some species pollen is found only in Acridocarpus and its seg- or were eventually lost. Implicit in my specula- regate Rhinopterys (Lowrie, 1982', Lobreau-Cal- tion was the assumption that the ancestral Mal- len, 1967, 1983). According to Lobreau-Callen pighiaceae had unwinged fruits ill-adapted to (1983), Brachylophonhas "colporate" pollen; she long-distance dispersal, and it was not until more did not say how many pores and colpi are pres- dispersible samaras evolved that the family suc- ent, and Lowrie did not see material of that ge- ceeded in crossing the gap from New World to nus. Lowrie (1982) and Lobreau-Callen (1967, Old. These ideas had been summarized earlier 1968) both reported Rhyncophora to have by Raven and Axelrod(L974) on the basis of my tricolporate pollen, but in her 1983 paper Lob- personal communications to Peter Raven. reau-Callen described it as "inapertur6" (p.814) Ardnes (1957) also suggestedthat the center without explaining her change in opinion. I am of origin of the Malpighiaceae was the area in assuming that the earlier reports, including her Brazll, the Guianas, and Venezuela where the 1968 drawing, of tricolporate pollen in Rhyn- Malpighiaceae are most numerous and diverse. chophorawere correct. All other Old World Mal- While it is intuitively tempting to equate center pighiaceae, as well as the majority of New World ofdiversity with place of origin, the idea has been Malpighiaceae, have various kinds of "porate" generally discredited and will receive no further pollens considered derived by both Lobreau-Cal- consideration here. len and Lowrie. Lobreau-Callen (1983: 876, 879) My conviction that the Malpighiaceae origi- thought that, for the most part, the porate pollens nated in the neotropics has always depended on of the Old World are more similar to each other the distribution of the character-states that I con- and to the colporate pollens of both hemispheres sider to be ancestral in the family. I have made than they are to the porate pollens of the New passingreference to this relationship (e.g., 1981: World. She derived the Old and New World por- 22-23;1983), and Cronquist cited personal com- ate pollens independently from tricolporate an- munications from me (198I 771), but I have not cestors. Lowrie (pp. 32t-323) agreed that most elaborated my reasoning in print, which led Vo- porate Old World pollens are coherent in mor- gel (1990) to assume, erroneously, that my hy- phological groups that reflect their geography, pothesis rested upon the distribution of calyx but he related two of those groups loosely to two glands. I shall correct that misimpression here. New World groups with porate pollen, and he The neo-orthodoxy of cladism would dictate placed one anomalous Old World genus (Fla- that I polarize characters by comparing the char- bellaria) within one otherwise neotropical sub- acter-states in the Malpighiaceae with those found group. in appropriate outgroups. While I find it impos- sible to achieve that ideal fully, I agree that in Hypotheses of the Origin of the making this kind of argument one should at least Malpighiaceae be explicit about one's reasons for asserting that any character-state is relatively plesiomorphic or THE "AMERICAN"Hyporrtrsrs apomorphic, and that much I shall do. The Malpighiaceae are morphologically rather I have suggested (1979b) that the Malpighi- isolated-there are no transitional forms or ob- aceae originated and diversified in the neotrop- viously closest sister taxa. Every plant I have ics, in a close coevolutionary relationship with studied was either clearly assignable to the family New World oil-bees, presumably after the sep- or readily excludable from it. (The only group aration between South America and Africa was about which I have ever had the slightest doubt sufficiently great to prevent the ready migration is the Brazilian genus .) It seems to me r9901 ANDERSON: ORIGIN OF THE MALPIGHIACEAE 215

FIG. 2. Pollens of neotropical Malpighiaceae.A & B. Lophanthera longifolia (H.B.K.) Grisebach, x 3500 (Prance26646). C. Mcvaughia bahiana W. R. Anderson, x 2500 (Anderson11740).D. Janusia occhioniiW. R. Anderson, xlTOO (AndersonI I 151).8. BunchosiadecussifloraW. R. Anderson, x 1500(Sl/va & Brazdo 60612). 2r6 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor. 64

sYNrRlcoLPoRArE "2""tt ,--eQLYPoRArsrQAscAGNlolD (/\\q> \.."/r,i (\\ ('".o.)',. -l- --l_,/ ' I r "|\) I AcoLpArE A colpoD,oRAr"coLPoDroRAr A .1'I(D 1A) ,A(-') (')'"""' O -:^ / d" colPt ).- \."fDcolPt\^."fD I I ./'' I ;-ur. d,' a-"Jl @-C,-,?-L=]-o ,/ cLoNoDtoro I BANISTERIO|D DERIVED CUBOIOAL

FIG.3. Lowrie's summary of pollen typesin the Malpighiaceae,with all typesderived from the tricolporate condition.From figure3.2in Lowrie(1982:38). that the appropriate method for selecting one or whorled or subopposite leaves, and a very more closest outgroups is to describe the "ur- few have them alternate. malpigh" and then compare that description to 6. Leaves unlobed-mostly; some Stigmaphyl- families that have been suggestedas putative rel- lon spp. have lobed leaves. atives. Below I list the character-states that I 7. Leaf margins entire-always; some are pseu- would expect to find in such an ancestor, on the dodentate at insertion of glands, cilia, or basis of their ubiquity or near-ubiquity in extant bristlelike hairs. Malpighiaceae. For each character I have added 8. Stipules present-mostly; much reduced in qualifying comments as to that character-state's some, to occasionally lacking. occurTence. 9. Multicellular extrafloral nectaries present- mostly; absent from a few species or genera. I. Habit perennial-always. 10. Flowers hermaphroditic-mostly. 2. Habit woody-mostly; a few have minimal lI. Sepals 5-always. . 12- Petals 5-always. 3. Hairs unicellular-always. 13. Petals clawed-mostly. 4. Hairs 2-armed-mostly; a few have basi- 14. l?-mostly; fewer in a few species fixed hairs, but most are clearly secondarily or genera; very rarely more. so with some hairs showing a rudimentary 15. Extra- and intrastaminal nectaries lack- second branch as a basal spur; three other- ing-always. wise dissimilar clades ( spp., Byr- 16. Carpels -l-mostly; 2 in a few clades; very sonima spp., and Thryallis) have hairs with rarely 4. more than 2 arms. 17. Styles as many as carpels-mostly; rarely 5. Leaves opposite-mostly; a few taxa have fewer. l 9901 ANDERSON: ORIGIN OF THE MALPIGHIACEAE 217

18. Styles distinct-mostly; coherent or connate which to reject immediately. The source of most in a few clades. of my morphological data was Cronquist (1981). 19. I per carpel-always, except where I also consulted the monograph of Trigoniaceae aborted; never 2 or more. by Lleras (1978) and studied specimens of Tri- 20- lacking in mature -al- goniaceae and Vochysiaceae in the University of ways, as far as I know. Michigan Herbarium.

Bentham and Hooker (1862) placed the Mal- Ge o grap hic al D ist ribut io n pighiaceae near the families that have often been grouped as Geraniales and Linales. The plant Both Trigoniaceae and Vochysiaceae occur described above as our "urmalpigh" is most un- principally in the neotropics, but there are two like the former (Oxalidaceae, , Bal- species of the former and one of the latter in the saminaceae, Tropaeolaceae, and Limnantha- Old World. If numbers count, outgroup com- ceae), so they are easy to eliminate from parison would favor a New World origin for the consideration as candidate outgroups. Most of Malpighiaceae, but caution is in order. The two the Linalean families also differ significantly from paleotropical Trigoniaceae (Humbertiodendron my urmalpigh; for example, the Humiriaceae and T r i g o n i ast ru m) have uniovulate locules more have an intrastaminal disk, endospermous seeds, like those ofMalpighiaceae than most New World usually five carpels, one style, mostly more than Trigoniaceae, and the fruit is a schizocarp with ten stamens, and often toothed leaves. The clos- three samaras that are impressively reminiscent est fit among the Linalean families is the Ery- of the fruit in the neotropical malpigh genus,Bar- throxylaceae, although its alternate leaves and nebya. endospermous seeds weigh heavily against choosing it as closest sister group. Habit The competing view, since the time of Engler (1897), has been that the families closest to the Both outgroups include trees, shrubs, and Malpighiaceae are the Trigoniaceae and Vochys- woody vines, although the latter are rare in the iaceae. Takhtajan (1980), Cronquist (1981), Vochysiaceae. Therefore, one cannot on the basis Dahlgren (1983), and Thorne (1983) all agreed of strict outgroup comparison specify the ple- that the families closest to the Malpighiaceae are siomorphic habit in Malpighiaceae. I confess to the Trigoniaceae, Vochysiaceae, Polygalaceae, an intuitive bias in favor of viewing vines as and Krameriaceae, with the first two generally derived from shrubs, but it is clear that woody favored. Comparing my urmalpigh with the data vines can give rise to shrubs and even small trees, I can gather about these families, I have to agree as tn spp. in central Brazll, so it is that the Trigoniaceae and Vochysiaceae do seem not impossible that a woody vine was ultimately to be the two families most like the Malpighi- ancestral to all the Malpighiaceae, even the large aceae, although both differ significantly from the trees of the Byrsonimoideae. plesiomorphic malpigh characters. Thus in Tri- goniaceae there are intrafloral nectaries, there is Inflorescence only one style, and the seeds are endospermous. In Vochysiaceae there is only one style, the ovules I believe that the single-flowered units found are mostly two or more per carpel, and the sta- in most Malpighiaceae have been derived from mens are never as many as ten. Nevertheless, at several-flowered cymules. That sequence is di- this time those two families, and especially the agrammed in Figure 1. It is based on Besseyan Vochysiaceae, seem to be the best candidates for reductionism-the belief that reduction is evo- closest sister taxa to the Malpighiaceae. lutionarily easier to achieve than elaboration, es- Now that we have reinvented Engler's wheel, pecially once a certain point ofno return has been can we polarize characters that vary within the passed, in this case the ability to make cymules Malpighiaceae? Only a few, as it turns out, but of more than one flower. Secondarily elaborated I shall do what I can, using a combination of inflorescences are common in the Malpighiaceae, outgroup and ingroup arguments and identifying but they consist of branched inflorescences com- them as such so that cladistic purists will know posed of many single-flowered units. In the 2r8 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor. 64

Vochysiaceae the inflorescence is usually a ra- glanduliferous species or genus, but I really would ceme ofcincinni, just like the inflorescence found not be ready to say that Coleostachys, for ex- in many neotropical Byrsonimoideae. In the Tri- ample, could not have retained the eglandular goniaceae one can find the same racemes of cin- calyx of an urmalpigh. Among the neotropical cinni (e.9., Trigonia virens Macbride) as well as Malpighiaceae with elaiophores (the vast major- various degrees of reduction in the cincinni, ter- ity), ten glands on five sepals seem likely to have minating in single-flowered units. One also en- preceded eight glands on four sepals. This is an- counters racemes of dichasid, e.8., in Trigonia other Besseyan argument. I assume that it was rugosa Bentham. Recall that dichasia occur in originally developmentally simplest to make five one byrsonimoid species, Lophanthera lactes- similar sepals, and that selection eventually (and cens. That is the condition I postulate to have perhaps repeatedly) favored the loss of glands been ancestral in the Malpighiaceae. I would from the front sepal where they were least ac- therefore claim that outgroup comparison sup- cessible to the bee and therefore least likely to ports my ingroup argument, but I admit that the justify the expense of making them. In this con- presence in the Trigoniaceae of inflorescences text it may be worth mentioning that it is com- with single-flowered units weakens that claim. mon for populations or species in very diverse Unlikely as it seems to me, it is possible that an genera to lose additional glands (e.9.,Lophanthe- ancestor with inflorescences constructed from ra spp., Heteropterys spp., spp.), and single-flowered units gave rise to descendants with when that happens it almost always involves loss cincinni and dichasia in both Trigoniaceae and of the glands that were adjacent to the anterior Malpighiaceae. sepal, which I interpret as a continuation of the same reduction trend in response to the same Calyx Glands kind of selection.

Neither the Trigoniaceae nor the Vochysiaceae Pollen have abaxial glands on the sepals, so the glands for which the Malpighiaceae are famous are In the preceding section I presented the opin- clearly an apomorphy of that family. Does that ions of Lowrie and Lobreau-Callen that tricol- mean that every malpigh with an eglandular ca- porate pollen is plesiomorphic in the Malpighi- lyx has the plesiomorphic condition? Surely not. aceae. I agree. Inasmuch as that consensus is Among the neotropical Malpighiaceae one finds based on the condition that is typical ofthe Rosi- eglandular calyces at every taxonomic level-in- dae it can be considered an outgroup argument. dividuals within populations and populations Closer to home, one finds that in the Vochysi- within species (e.9., spp., Heteropte- aceae the pollen is tricolporate, while in the Tri- rys spp.), species within genera (e.g., Banister- goniaceae it is 3-5-porate. iopsis, Byrsonima, Galp himia, ), eglan- dular genera with sister genera that have glandular Fruit calyces (e.9., Echinopterys), and isolated genera or clusters of genera with eglandular sepals(e.g., Outgroup comparison tells us little about the Coleostachys; Lasiocarpus and Ptilochaeta; fruit of the urmalpigh, but since the fruits in both Thryallis). While it may well be that among all Trigoniaceae and Vochysiaceae are always dry these taxonomically scattered casesthere lurks a and dehiscent (capsules or schizocarps) it seems species or genus that retains the plesiomorphic probable that the ancestral condition in the Mal- eglandular condition, it would be patently absurd pighiaceae was a dry fruit that was schizocarpic to suggestthat they a// show the eglandular con- or whose carpels were free from the beginning. dition through unbroken inheritance from an From these considerations I conclude that the eglandular ancestor. Moreover, I know of no way earliest Malpighiaceae had inflorescences com- to examine an eglandular calyx and state objec- posed of cymules. The first ones to have paired tively on the basis of its morphology alone calyx glands probably had them on all five sepals. whether it is primitively or secondarily eglan- The pollen was surely tricolporate, and the fruit dular. I would be willing to guess in caseswhere was almost certainly dry and either schizocarpic the eglandular plant were embedded within a or derived from free carpels. The distribution of l eeOl ANDERSON: ORIGIN OF THE MALPIGHIACEAE 219

iollen 3:4-colporate Rhynchophora

BLepharan^dra Burdachin Acmanthera Byrsonima Colnostachys Diacidin Pterandra I-ophanthera Spchw Acridocarpus Verrucularia Rhinopterys

Barnebya

32 Neut World genera Inflorescence of cymules in at least some species 12 Old World genera

Fruit dehiscent

FIG.4. Distribution of three plesiomorphic character-states among the genera of Malpighiaceae. New World genera are in italic, with the byrsonimoid genera bold. Old World genera are in Roman. Not shown are the four genera (all neotropical) that lack all three character-states: Bunchosia, , Malpighia, and, Thryallis.

these inflorescence, pollen, and fruit character- tropical subfamily Byrsonimoideae, all of which states among extant genera is shown in Figure 4. are trees or shrubs with colporate pollen; most No Old World genera have thyrsiform inflores- have ten calyx glands. Four genera have the in- cences, and only four have colporate pollen. florescence composed of single-flowered units in Rhynchophorahas an indehiscent fruit, and Ac- all speciesand six have the fruit indehiscent. The r i do car p us and Rh i nop t ery s hav e alternate leaves only three genera that show all three of the ple- and syncolporate pollen. In the New World, Bar- siomorphic character-states used to prepare Fig- nebya is the only non-byrsonimoid genus with ure 4 are Lophanthera, Spachea, and Verrucu- an inflorescence composed of cymules; its pollen laria. Spacheais derived in its breeding system- lacks ectoapertures, resembling that of Buncho- all three species investigated are functionally di- sia shown in Figure 2E. That leaves the neo- oecious (Anderson, 198 I : 4243.,Steiner. 1985). 220 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor. 64

Verrucularia hardly differs from Lophanthera, pighs descended from samara-bearing plants like but it is advanced in its complete lack of extraflo- those now in the neotropics is too simple, be- ral nectaries. Lophanthera spp. seem to come cause all such extant neotropical species have closest to fitting the picture constructed here of "porate" pollen, and it is unlikely that such pol- an ancestral malpigh, but even they are probably len reverted to the ancestral rosid condition three derived in their winged anthers and in having times in the Old World. There must have existed the colpi short-bifurcate at the tips in some spe- at one time New World Malpighiaceae inter- cies, including Z. lactescens. the species cited mediate between byrsonimoids with colporate above as the only member of the family known pollen and thyrsiform inflorescences and the to bear dichasia as well as cincinnt. Lophanthera present-day samara-bearing plants with derived is a genus of five species, four of them Amazo- pollen and inflorescences. Barnebya probably nian and the fifth endemic to lowland forests near represents such an intermediate, in which the rivers on both coasts of Costa Rica (Anderson, plesiomorphic inflorescence was retained asso- 1983).The latter, L. hammeliiW. R. Anderson, ciated with derived pollen and winged fruits. Such is illustrated in Figure 5. In the 1983 paper I a plant, but with tricolporate pollen, would be a suggestedthat the basic chromosome number of fine ancestor for Acridocarpus and Rhinopterys, the family is probably n:6, the lowest number one of the three Old World clades with colporate known. I cited previous counts of n: 6 tn Loph- pollen (Anderson & Gates, 1981). This kind of anthera lactescens and Galphimia glauce Cav., ad hoc reasoning could account for all the Old a fairly closely related byrsonimoid. Since then World malpighs with colporate pollen, but it suf- I have counted the chromosomes in Lophanthera fers from two weaknesses. One is that it postu- hammelii (voucher is Hammel 13339 : Schatz lates more independent introductions from the 1034, MICH) and Verrucularia glaucophylla Adr. New World, and while such are not impossible Juss. (voucher is Anderson 13704, MICH). In the more of them one has to postulate the less bothspeciesn:6. likely they become. The other weakness is that My purpose in this exercise has not been to this kind of explanation relies on hypothetical suggest that the urmalpigh is alive and well and intermediates no longer in existence, except for living in the Amazon. I am not so naive as to Barnebya. While some such intermediates be- believe that any taxon could be expected to pos- tween the neotropical clades must have existed, sess solely plesiomorphic character-states. But I prefer explanations that do not require one to Figure 4 and my discussion of it show that the construct hypothetical organisms, since that admittedly few such states that I can identify practice lends itself so readily to special pleading with confidence are heavily concentrated in the for pet hypotheses. Byrsonimoideae, which are wholly American. The other explanation that I can suggest for The simplest hypothesis consistent with these colporate pollen in the Old World is that my data is that the family originated in northern hypothesis that the family originated in isolation South America in effective isolation from the Old in the New World is wrong. The alternative would World. be that the Malpighiaceae evolved before the The great problem with my "American" hy- breakup of Gondwanaland, and that the three pothesis is that it does not readily account for Old World clades with colporate pollen have al- the presence of tricolporate pollen in three quite ways inhabited what are now Old World regions. separate lineages in the Old World. My earlier Like the byrsonimoids they simply retained a speculation (1979b) that all the Old World mal- plesiomorphic pollen type inherited from their

-, FIG. 5. Lophantherahammelii. A. Floweringbranch, x 0.5,with circle x 2.5.B. Stipules,x2.5. C. Cincinnus of two flowers, x 2.5, with bracteoleglands (righ| x 5. D. Flower, side view with posterior petal erect, x 2.5, with singlepetal x 3.5. E. Stamens,x 10, abaxial view left, adaxial view right. F. , x7.5, with tip of style (left) x15. G. Fruit, x3, with adaxial view of single mericarp (left) x4.5. H. Mericarp in longitudinal section,with intact seedin position, x 4.5. I. , x 4.5, sideview left, abaxialview right. Drawn by Karin Douthit, A-B from Grayum 2231A, C-I from Hammel 9397. Onernally publishedin Brittonia 35:39. 1983. 19eOl ANDERSON: ORIGIN OF THE MALPIGHIACEAE 221

e3 wTffi N { l'.F s- 1't i R--- Lh. ll ,/1i\

M 222 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor-.64 common ancestors. This is the "Gondwanian" I accept as a reasonable working hypothesis hypothesis, which Vogel has proposed on differ- Vogel's conclusions that all malpigh glands are ent grounds. Let us, therefore, turn our attention homologous and that calyx glands were derived to that hypothesis now. from extrafloral nectaries. However, it does not necessarily follow that the calyx nectaries in Old World malpighs could only have come directly Tun "GoNDwANIAN" HYPoTHESIS from extrafloral nectaries. Vogel cannot have it In his 1990 paper Vogel developed an ar- both ways-if all those glands are anatomically gument based on observations presented in his so similar that their homology is unquestionable, 1974 book. There he showed that all calyx glands then there is no reason why elaiophores that lost in the Malpighiaceae are anatomically similar to their ability to produce oil after migration to the extrafloral nectaries, from which he concluded Old World should not revert in structure to a that all calyx glands are homologous with ex- condition similar to that of their homologs. In- trafloral nectaries and that extrafloral nectaries deed, that is just what Vogel's conclusions would gave rise to calyx glands rather than the reverse. lead me to expect. Similarly, the fact that those He also showed that the calyx glands in the few glands produce rather than oil does not Old World genera that possessthem are anatom- mean they are not degenerate elaiophores. As ically and functionally more like extrafloral nec- Vogel said ( 1990: 140): "Why, and how, the tran- taries than like the calyx glands ofthe New World sition of nectaria to oil glands came about phys- Malpighiaceae. On that basis he concluded that iologically, is still open to debate. The occurrence the Old World malpighs lacking calyx glands are in some of small amounts of lipids on primitively eglandular, and that in those bearing the one hand, and that of sugar traces in some calyx nectaries they evolved directly from ex- floral oils on the other, suggestsat least that such trafloral nectaries, not through degeneration from a change was feasible." I agree, and if it was elaiophores inherited from New World ances- feasible once in one direction, the reverse would tors. In 1974 (pp. 242-243) he seemed equally have been even more feasible, because the ge- ready to accept either of two explanations for netic ability to make sugary nectar was not lost this situation: "Either the New World Malpigh- when the plants evolved the ability to produce iaceae stemmed from the predecessors of [pres- oil in elaiophores. Therefore, I cannot accept Vo- ent-dayl paleotropical [Malpighiaceae], and after gel's assertion that the calyx nectaries in Old isolation a general transmutation of their calyx World malpighs could not be degenerate elaio- glands to elaiophores and thus nuptial organs phores. His own evidence as to their homology occurred, or . . . the Old World groups must have makes that a reasonable possibility. This point already separated, as did also the American gen- is critical to the Gondwanian hypothesis of the era of today, [which] although otherwise already origin of the Malpighiaceae. In fact, it is Vogel's possessing their characteristic features, still had only real basis for that hypothesis. no oil glands, i.e., found themselves in a con- Vogel emphasized the structure and function dition which is still conserved in the afroasiatic ofthe Old World calyx glands while glossing over representatives" [my translation]. The first of the anomalous fact that they exist at all. After these two suggestions is orthogenetic and would going to some trouble (1990: 138) to demonstrate be most unlikely to command serious consid- (on the basis of position, not field observations) eration from most evolutionary biologists, so not that they cannot function to reward pollinators, surprisingly it was deemphasized in the 1990 pa- he could advance no plausible explanation for per, where instead Vogel developed the second why they should have evolved in what seem like- idea, concluding (p. 141): "Both groups of the ly to be three quite different clades (Acridocar- family evolved from a common ancestor prob- pus/Rhinopterys, H ipt age, and Trist el lateia). He ably already existing in Gondwanaland which offered only another orthogenetic speculation: bore unspecialized pollen flowers. This original "Apparently, an evolutionary propensity for the condition is still conserved in the paleotropic calyx to acquire these vegetative glands also ex- descendants whereas the neotropical ones ac- isted, a conceivable process considering the veg- quired elaiophores as an apomorphy after the etative provenance of the sepal ." When separation of the continent." that line of reasoning is weighed against the pos- r 9901 ANDERSON: ORIGIN OF THE MALPIGHIACEAE 223 sibility that some Old World malpighs bear de- much more receptive to the second suggestion, generate glands because their ancestors were because my own monographic studies of neo- American and bore elaiophores, the presence of tropical Malpighiaceae indicate that there has those glands in the Old World can be seen as been parallel evolution among those genera of at supporting the American hypothesis. Those Old least superficially similar fruits. I suspect that World calyx glands are as much of a problem for banisterioid and hiraeoid samaras represent the Gondwanian hypothesis as the presence of aerodynamically optimal designs, which have colporate pollen in the Old World is for the been achieved independently several times in the American hypothesis. New World, and the same may have happened Another, analogous difficulty with the Gon- in the Old World. On the other hand, I must dwanian hypothesis was not recognized by Vo- admit that some Old World samaras are very gel. Almost all Malpighiaceae have clawed pet- similar indeed to some New World samaras. als. The functional significance of those claws in Niedenzu was not without some grounds for al- neotropical malpighs with elaiophores was made lying Old World and New World genera. Not obvious by Vogel in his 1974 monograph-they having studied any of the Old World Malpighi- leave a space through which the bee can gain aceaein detail I am not prepared to speak further accessto the elaiophores. The fact that the petals to this problem, but for the moment the multiple are clawed in malpighs without elaiophores, in- convergences required by the Gondwanian hy- cluding those ofthe Old World, presents no prob- pothesis would seem to constitute something of lem for my hypothesis of an American origin of a problem. the family; I see it as simply a retained plesio- morphy. But if the Old World malpighs did not Where Do We Go from Here? have an American origin, what is the functional significance or the selective basis for their clawed I have emphasized the inflorescence and pol- petals? len and concluded that an American origin for Finally, it seems inescapable that the Gondwa- the Malpighiaceae is most likely. Vogel empha- nian hypothesis requires a great deal of parallel sized characteristics of the calyx glands and con- evolution of apomorphies, as Vogel admitted cluded that the family had a Gondwanian origin. (1990: 138-139): "Provided the current system Some data are inconsistent with or at least in- of the Malpighiaceae is correct, the New World convenient for each hypothesis, and it is possible branches of the tribes Hiptageae and Banister- that the truth lies in some other explanation, ieae, as well as the Byrsonimoideae and the Mal- perhaps one that combines elements of both hy- pighia affinity, have acquired elaiophores in in- potheses. At this point it seems best to seek ad- dependent parallel lines, as repeated apomorphies ditional data that might shed new light on the that commenced to develop soon after the iso- problem. Since we have exploited morphology lation from the Old World stock. . . . If the al- rather thoroughly and remain at a stalemate, I ternative possibility is true, namely that the ad- have decided to explore non-morphological data. vent of elaiophores was a single evolutionary Therefore, I have recently embarked on a study occurrence, reflecting monophyly of the Ameri- using molecular data, in collaboration with Mark can portion of genera, it renders the assumption W. Chase. We hope that the sequence of nucle- of intra-tribal connections between these and the otides in one DNA gene will give us paleotropical subtribes (as expressed in the cur- an improved basis for specifying a closest out- rent system) no longer tenable, and their (mainly group to use in polarizing characters within the carpological) coincidences would be a matter of Malpighiaceae. We shall also try to use restric- convergence." The first suggestion recalls Vogel's tion site analysis to group the genera within the 1974 orthogenetic speculation, quoted above in family, independently of the morphology that translation, and seems just as incredible now as seems so subject to homoplasy. Therefore, we it did then. Anything is possible, I suppose, but hope to follow this paper in the fairly near future I really cannot believe that the bizane and ele- with a new contribution to the discussion. and I gant suite of identical character-states found in cannot at this time predict the contents of that the oil-flowers of the New World Malpighiaceae report. If molecular techniques enable us to find evolved independently four or more times. I am a way out of the thicket of conflicting morpho- 224 MEMOIRS OF THE NEW YORK BOTANICAL GARDEN [vor-.64

logical data, they will demonstrate their power Cronquist, A. 1981. An integrated system of classi- and their value for traditional systematists. fication of flowering plants. Columbia University Press, New York. xviii * 1262 pp. Dahlgren, R. 1983. General aspects of angiosperm Acknowledgments evolution and macrosystematics. Nord. J. Bot. 3: rr9-r49. Engler, A. 1897. Preparation of this article was aided by Na- Ubersicht iiber die Unterabteilun- gen, Klassen,Reihen, Unterreihen und Familien grant tional Science Foundation BSR-8700340 der Embryophyta siphonogama.In A. Engler & to The University of Michigan. My wife, Chris- K. Prantl, Die natiirlichen Pflanzenfamilien II-IV tiane, helped me translate Dr. Vogel's German. (Nachtriige):341-357 . W. Engelmann,Leipzig. The SEM photographs in Figure 2 result in part Lleras,E. 1978. Trigoniaceae.Fl. NeotropicaMono- gr. 19: 1-73. from the efforts of Robert Naczi and Stuart Low- Lobreau-Callen,D. 1967. Contribution a l'6tude du rie, and I am especially indebted to the latter's pollen des Malpighiaceaed'Afrique. Pollen & doctoral thesis for my information on malpigh Spores9:241-277. pollen, and for Figure 3. Figure I is modified 1968. I,e pollen desMalpighiac6es d'Afrique from a drawing originally published in the Mem- et de Madagascar.Bull. Inst. Fondam. Afrique Noire 30, 56r. A, Sci.Nat. 1: 59*83. oirs of The New York Botanical Garden 32 (An- 1983. Analysede la r6partition g6ographique derson, 1981: 25), and Figure 5 was originally desMalpighiaceae d'aprds les caractdres du pollen published in Brittonia (Anderson, 1983). et de la pollinisation.Bothalia 14:871-881. 1989. l*s Malpighiaceaeet leurs pollinisa- teurs. Coadaptation ou co6volution. Bull. Mus. Literature Cited Hist. Nat. (Paris),Sect. B, IV, ll: 79-94. Lowrie, S. R. 1982. The palynologyof the Malpigh- Anderson, W. R. 1977119781.Byrsonimoideae, a new iaceaeand its contribution to family systematics. subfamily of the Malpighiaceae. Leandra 7: 5-18. Ph.D. Dissertation.University of Michigan, Ann 1979a. Mcvaughia, a new genus of Malpigh- Arbor. 354 pp. University Microfilms #82-24999. iaceae from . Taxon 28: 157-16I. Niedenzu,F. 1928. Malpighiaceae.In A. Engler,Das 1979b. Floral conservatism in neotropical PflanzenreichIV, 141: 1-870. Malpighiaceae. Biotropica 11: 219-223. Raven, P. H. & D. I. Axelrod. 1974. Angiosperm 1981. Malpighiaceae. In B. Maguire & col- biogeographyand past continental movements. laborators, The of the Guayana High- Ann. Missouri Bot. Gard. 6l:539-673. land-Part XI. Mem. New York Bot. Gard. 32: Steiner,K. E. 1985. Functionaldioecism in the Mal- 2l-30s. pighiaceae:The breedingsystem of Spacheamem- 1983. Lophanthera,a genusof Malpighiaceae branaceaCuatr. Amer. J. Bot. 72:1537-1543. new to Central America. Brittonia 35:3741. Takhtajan, A. L. 1980. Outline of the classification & B. Gates. 1981. Barnebya,a new genusof of floweringplants (Magnoliophyta). Bot. Rev. 46: Malpighiaceaefrom Brazil. Brittonia 33227 5-284. 225-359. Arines, J. 1946. Trois genresde Malpighiac6esnou- Thorne, R. F. 1983. Proposednew realignmentsin veaux pour la flore malgacheet pour la science. the angiosperms.Nord. J. Bot. 3: 85-117. Notul. Syst.(Paris) 12: 126-136. Vogel,S. 1974. Olblumen und