Proc. Natl. Acad. Sci. USAVol. 93, pp. 11713-11717, October 1996Evolution

Zoidogamy in fossil gymnosperms: The centenary of a concept,with special reference to prepollen of late Paleozoic conifersRUUD J. POORT*, HENK VISSCHER*, AND DAVID L. DILCHERt*Laboratory of Palaeobotany and Palynology, Utrecht University, Budapestlaan 4, 3584 CD, Utrecht, The Netherlands; and tPaleobotany Laboratory,Florida Museum of Natural History, University of Florida, Gainesville, FL 32611

Contributed by David L. Dilcher, August 2, 1996

ABSTRACT This year is the centenary of the surprisingdiscovery in 1896 of zoidogamy in extant cycadophytes andGinkgo. But by coincidence, also in the same year, the conceptof prepollen was introduced. The morphology of prepollen wasconsidered justification for the probable production of motileantherozoids in extinct gymnosperms. In this paper, thehistory of the prepollen concept is briefly outlined. It isemphasized that, in addition to well-known examples inpteridosperms and cordaitaleans, a prepollen condition alsooccurred among late Paleozoic conifers.

Toward the end of the 19th century, it was generally assumedthat seed plants, both extant and extinct, were uniformlycharacterized by siphonogamy. This fertilization mechanisminvolves formation of a pollen tube, a tubular outgrowth of themicrogametophyte through which immotile gamete cells ornuclei are delivered to the archegonia. The mechanism isfundamentally different from zoidogamy, the fertilization bymeans of motile antherozoids, which can be observed inspore-bearing plants.As early as 1887, the possibility of zoidogamy in extinct

gymnosperms was mentioned by the French palaeobotanistRenault (1), but this view attracted little attention. Then in1896, a century ago this year, the assumption of uniformsiphonogamy in gymnosperms was definitively shown to be afalse concept. By remarkable coincidence, the presence ofzoidogamy was independently discovered in both recent and infossil plants in the same year.

Zoidogamy in Gymnosperms

In 1896, the Japanese botanists Hirase and Ikeno publishedtheir classic notes on the discovery of the production ofantherozoids in Ginkgo biloba (2) and Cycas revoluta (3). In thesame year, Renault published the text of his monumental workon Carboniferous and Permian plant fossils from France (4).By studying pollen grains present in pollen chambers ofpteridospermous and cordaitalean ovules, Renault interpretedthe supposedly internal cellular structure of the pollen as amulticellular microgametophyte. He hypothesized that thesecells could have produced motile antherozoids rather thandeveloping pollen tubes.The discoveries of Hirase and Ikeno surprised the interna-

tional botanical community and had an immediate and tre-mendous impact on the comparative analysis of reproductivebiology in gymnosperms. Fertilization by means of motileantherozoids soon became universally recognized as the fun-damental reproductive strategy of all extant cycadophytegenera, as well for Ginkgo. Zoidogamy provided a functionalexplanation for the presence of the pollen chamber, long sinceknown in the ovules of these taxa. The function of the pollentube in these taxa had to be regarded as exclusively nutritive,

because it serves as a haustorial organ to digest the tissues ofthe nucellus and provide nutrients for the developing motileantherozoids.

Similar to those in extant cycadophytes and Ginkgo, thecommon presence of pollen chambers in ovules of late Paleo-zoic gymnosperms already had been well documented (5).Following Renault's observations, the study of the fossilizedcontent of pollen chambers received considerable attention.Supposedly multicellular structures in pollen grains and avariety of small bodies were interpreted as fossil evidence forthe production of antherozoids (6-8). Indirectly, but moreconvincingly, zoidogamy was suggested on the basis of themorphology of the pollen wall. Following studies by Kidston(9), it gradually was realized that some pteridosperms pro-duced pollen with the overall morphological organization ofmany isospores or microspores of pteridophytes. A commonfeature is the presence of a proximal aperture. In modernheterosporous pteridophyte spores, this aperture splits open,permitting the protrusion of the antheridia-bearing gameto-phyte. This is true also in heterosporous lycopsids, whichrelease internally produced antherozoids through a proximalaperture (10). Hence, functional interpretation of similarapertures in fossil gymnospermous pollen suggested zoid-ogamy (11)

Prepollen

At present, fossil gymnospermous pollen characterized byproximal apertures and absence of distal specializations indic-ative of the production of a pollen tube is known as prepollen.The prepollen concept is intimately linked with zoidogamy.This year, we are at the centenary of the concept. In 1896,Renault coined the termprepollinies for large pteridospermousand cordaitalean pollen, characterized by a supposed multi-cellular microgametophyte and assumed to be indicative ofzoidogamy (4). He considered this pollen to be intermediatebetween pteridophyte spores and cycadophyte pollen, al-though he was unaware of the discoveries of Hirase and Ikeno.The termprepollinies was used infrequently until it was revivedand anglicized by Schopf (12, 13).

In the 1970s, the prepollen concept was elaborated byChaloner (14), and further comments were contributed byJonker (15, 16). More importantly, basic morphological andultrastructural information became available, confirming thepresence of functional proximal sutures in prepollen, includingthe huge (up to 0.5-mm-long) pollen types of medullosaleanpteridosperms for which Renault had used the term prepolli-nies (17). As a result, prepollen is currently defined as "themicrospores of certain extinct seed plants characterized byproximal apertures and presumed proximal germination,rather than the distal, equatorial or other typical apertures ofseed plant pollen grains" (18). Prepollen thus representspollen that had not yet developed the capacity to producepollen tubes (Fig. la).

In the definition of prepollen, emphasis is given to thefunctional interpretation of the proximal aperture in the pollen

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The publication costs of this article were defrayed in part by page chargepayment. This article must therefore be hereby marked "advertisement" inaccordance with 18 U.S.C. §1734 solely to indicate this fact.

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a b

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FIG. 1. Scheme of zoidogamous (a and b) and siphonogamous (c)fertilization strategies of conifer pollen; outer pollen wall omitted. (a)Prepollen condition; release of motile antherozoids through proximalaperture; no outgrowth of pollen tube; relatively large size (latePaleozoic). (b) Pollen grains with proximal release of motile anthero-zoids; distal outgrowth of a haustorial pollen tube with an exclusivelynutritive function (late Paleozoic and early Mesozoic). (c) Pollengrains with distal outgrowth of a pollen tube functioning as a carrierfor immotile gamete cells or nuclei to migrate to the archegonium(Mesozoic to Recent).

wall rather than to multicellular structures. At present, thereis a strong and justified reluctance to accept early records ofmulticellular microgametophytes in some (pre)pollen. Notablyin permineralized material, effects of fossilization are a likelyexplanation for pseudocellular structures (19, 20). The earlyrecords of fossilized antherozoids need to be reconfirmed. Yetthere is a subsequent record that justifies the link betweenprepollen and zoidogamy. In pollen present in the pollenchamber of the medullosalean ovule Pachytesta and corre-sponding to Renault's and Schopf's prepollen, two cells thatclosely resemble the immature paired antherozoids of moderncycadophytes were detected (21).

It is obvious that the fossil prepollen by definition contrastswith the two pollen categories that are functionally recognizedin extant gymnosperms: (i) pollen with a distal aperture(leptoma) for the outgrow of a pollen tube with an exclusivelynutritive function (release of motile antherozoids is not bypreformed apertures but by wall decay; zoidogamy of cycado-phytes, Ginkgo), and (ii) pollen with a leptoma for the outgrowof a pollen tube that also serves as a carrier for immotilegamete cells or nuclei (siphonogamy of all other gymnospermtaxa; Fig. lc). The combination of the exclusively fossil pre-pollen with the two extant pollen categories provides a 3-foldsubdivision that is frequently followed to illustrate, in a generalsense, progressive change in the reproductive strategy ofgymnosperms (22).There are some controversies regarding the functional in-

terpretation of the morphology of fossil pollen grains that arecharacterized by the presence of both proximal and distalapertures. Many such pollen grains have been described aspalynological form-genera based upon dispersed pollen fromlate Paleozoic and early Mesozoic sediments. Well-knownexamples are pollen types corresponding to the form-generaJugasporites, Lueckisporites, and Triadispora. Considering theproximal aperture to be a vestigial feature, such pollen some-times has been regarded as indicative of siphonogamy. Incontrast, by neglecting the leptoma, similar forms have beennamed prepollen. In fact, this distinctive fossil pollen may becompared functionally with the pollen of extant cycadophytesand Ginkgo. In contrast to this extant pollen, where anthero-

zoids are released by wall decay, in the fossil pollen zoidogamyis supported morphologically by the presence of a preformedsuture in the proximal wall (refs. 23 and 24; Fig. lb).A more difficult problem to solve is the functional inter-

pretation of fossil pollen characterized by the presence of aleptoma but without any indication of a proximal aperture.Such pollen grains are likely to have produced pollen tubes, butit remains impossible to decide whether they represent zoid-ogamous or siphonogamous plants. Even the unique discoveryof a fossil pollen grain with a well-preserved branched pollentube (25) remains inconclusive. This particular grain is regu-larly cited to be indicative for siphonogamy in the late Paleo-zoic. However, other criteria, such as the presence of a pollenchamber in the corresponding ovules, strongly suggests zoid-ogamy. It should be realized that the origin of pollen tubes andsiphonogamy are separate evolutionary steps (24, 26). Anadditional problem in the interpretation of apertures in fossilgymnosperm pollen. is the possibility of the presence ofdistinctive apertures (proximal, distal, or equatorial) that arenot related to pollen tube formation or the release of anthero-zoids, but to harmomegathy, i.e,. the process by which pollengrains change in shape to accommodate variations in thevolume of the cytoplasm caused by changing hydration.As far as prepollen is concerned, a wealth of morphological

and ultrastructural data is now available for a variety of pollentypes, found in situ in polleniferous organs of lyginopteridaleanand medullosalean pteridosperms (17, 27-42). Although notalways explicitly cited as prepollen, these studies firmly con-firm a prepollen condition in the Lyginopteridales and Medul-losales. Pollen of other pteridosperms is frequently character-ized by only a distal aperture. This also applies to pollen of anumber of cordaitalean taxa. However, a prepollen conditionis also evident in some cordaitalean pollen types, such as theform-genus Felixipollenites (28, 38, 42, 43).The distinctive morphological and ultrastructural characters

of pteridosperm and cordaitalean prepollen have now at-tracted wide attention. However, despite conclusive evidence,it is not yet been generally appreciated that pollen of some latePaleozoic conifers could qualify as prepollen as well.

Prepollen in Late Paleozoic Conifers

Modern conifers are siphonogamous. Except for apparentlyinaperturate forms in the Taxales, conifer pollen is well knownto be characterized morphologically by a distal leptoma (44).One can recognize a wide variety in the overall shape of thepollen, even within a single family. In a number of genera ofthe Pinaceae and Podocarpaceae, for example, pollen has twolateral and distally inclined expansions of the outer wall(sexine). These expansions may be hollow (saccate) or some-times filled with spongy sexinous structures (protosaccate orsaccoid). In other families, such differentiations are lacking.Regardless of these variations, the pollen tube develops inmost modern conifer pollen (except Taxales) from the distalleptoma. In all modern conifers, the pollen tube functions asa carrier or transport system for the gamete cell or nucleus tomigrate to the archegonium and the egg cell before fertiliza-tion occurs.

Also, late Paleozoic and Mesozoic conifers are usuallyregarded as siphonogamous. In his monograph on Paleozoicconifers, Florin compared saccate or saccoid fossil coniferpollen with presumed modern counterparts (45). Yet pollenwith both proximal and distal apertures was known or sus-pected to be produced by fossil conifers. Such pollen (Juga-sporites) was described, for example, from polleniferous conesof the late Permian conifer Ullmannia (46, 47). In 1984,uniform siphonogamy in extinct conifers was challenged.Again by coincidence, a prepollen condition for coniferouspollen was reported from two independent sources.

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Proc. Natl. Acad. Sci. USA 93 (1996) 11715

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FIG. 2. Prepollen of late Carboniferous/early Permian Walchiaceae (form-genus Potonieisporites, known from the genera Walchia, Ernestio-dendron, and Otovicia). (a) Proximal face of specimen showing aperture. (X435.) (b) Section subparallel to longest axis; thick outer wall (sexine)with alveolate infrastructure; no indications of the presence of an aperture at the distal (lower) side. (x 1600.) (c) Section subparallel to short axis;inner wall (nexine) strongly folded due to compression; thick outer wall (sexine) with no indications of a distal aperture. (x 1600.)

A detailed study of the genus Ortiseia from the UpperPermian of North Italy, and a reevaluation of the generaWalchia and Ernestiodendron by Clement-Westerhof (48) ini-tiated the development of a natural concept of the Walchi-aceae (48-52), the most prominent conifer family of the latePaleozoic Euramerican floral province. One of the novelelements in this reevaluation is the concept that walchiaceouspollen represents prepollen. Light-microscopic and scanningelectron microscopic studies of in situ pollen from pollenifer-ous organs of Ortiseia demonstrate the presence of a proximalaperture. No evidence was found for the additional presenceof a leptoma that could support outgrowth of a pollen tube.Moreover, on the basis of detailed cuticular analysis, it was

deduced that corresponding ovules are likely to possess pollen/archegonial chambers.By studying permineralized ovuliferous cones described as

Lebachia lockhardii from the Upper Carboniferous of Kansas,Mapes and Rothwell (53, 54) arrived at similar conclusions.The ovules are characterized by a pollen chamber. Uncom-pressed pollen grains preserved in pollen chambers have thecharacteristics of prepollen. Scanning electron microscopyreveals the proximal aperture, whereas a light-microscopicsection indicates absence of a distal leptoma.

Further morphological and ultrastructural studies (55) haveconfirmed the prepollen condition of in situ and dispersedwalchiaceous pollen. Meanwhile, Lebachia lockhardii had been

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FIG. 3. Pollination model for late Paleozoic prepollen-bearing conifers (after refs. 51 and 52). (a) Portion of an ovuliferous cone with airflowpattern indicated by curved arrow. (b) Capture of prepollen by a pollination droplet at the top of the micropyle. (c) Enlargement of (b), showingprepollen absorbed by pollination droplet. (d) Retraction of droplet into micropyle. (e) Prepollen inside pollen/archegonial chamber where releaseof motile antherozoids takes place through the proximal aperture of the prepollen grains.

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11716 Evolution: Poort et al. ~~~~~Proc. Nati. Acad. Sci. USA 93 (1996)

applied to typify the Emporiaceae (54). The presence ofprepollen has now become part of the diagnosis of two latePaleozoic conifer families. The coniferous prepollen typesrecognized so far correspond to (or resemble) the late Paleo-zoic form-genera Nuskoisporites and Potonieisporites (Fig. 2).

In the Lower Permian of Argentina, dispersed pollen (Can-nanoropollis) that has been associated with the Ferugliocla-daceae (56) might show a prepollen condition, but furtherstudies are required. On the other hand, the presumed pres-ence of prepollen in the late Permian Majonicaceae (57) hasto be rejected. In situ pollen corresponds to the form-genusLueckisporites and incudes forms with both proximal and distalapertures. Similarly, the coniferous families Ullmanniaceae(late Permian) and Voltziaceae (Triassic) produced pollen(Jugasporites and Triadispora) that apparently had developedthe capacity to form distal haustorial pollen tubes (46, 47, 58).In contrast to the siphonogamy in extant conifers, thesefamilies were still characterized by zoidogamy. Consequently,conifers represent the only group of gymnosperms in which thethree functional steps in pollen evolution can be recognized(Fig. 1).

Coniferous prepollen is characterized by a single, monosac-cate or monosaccoid, expansion of the sexine. Despite therelatively large size of the prepollen grains (up to 300 atm), theoverall shape of this differentiation is likely to indicate windpollination (45, 52, 55). Both in the Walchiaceae and theEmporiaceae, the ovules are inverted, with a downward-projecting micropyle. This would suggest a pollination dropmechanism for facilitating the entry of prepollen in the pollenchamber (51-54). The presence of such a mechanism issupported by an observed cluster of prepollen at the tip of thenucellar beak of an ovule of the walchiaceous genus Otovicia(51, 52). Noting the occurrence of prepollen in the genus, thereconstructed pollination mechanism for Otovicia may serve asa model of the pollination biology of Walchiaceae and Em-poriaceae (Fig. 3).

Conclusions

In conclusion, we emphasize that during the late Paleozoic,zoidogamy was the rule rather than the exception among allmajor gymnosperm groups, including the conifers. Prepollen-bearing plants gradually became extinct during the Permian.The most recent known genus with prepollen, the coniferOrtiseia, did not survive the ecological crisis at the Permian-Triassic transition (55, 59). However, possibly as a paralleltrend in a variety of late Paleozoic gymnosperms (24, 26), thecapacity to form haustorial pollen tubes had already developedand zoidogamous taxa could continue to dominate gymno-sperm plant life during a considerable part of the Mesozoic. Itis not yet possible to estimate accurately when siphonogamyoriginated, or when and why this reproductive strategy startedits rise to dominance over zoidogamy. Yet we have to begrateful that there are still a few "living fossils" that havesurvived the progressive elimination of zoidogamous plants.Fossil pollen may help to hypothesize on the waxing andwaning of zoidogamy, but we first needed the pollen of Cycasand Ginkgo to reveal, a century ago, that the very concept ofzoidogamy among gymnosperms is not a hypothesis but areality.

We thank Hans Kerp, Han Van Konijnenburg-Van Cittert, WilliamDiMichele, Gar Rothwell, and William Stern for helpful comments.This work was supported by The Netherlands Organization for Sci-entific Research and The Netherlands Life Science Foundation. Thisis Netherlands Research School of Sedimentary Geology publicationno. 960901 and University of Florida Contributions to Paleobiologyno. 477.

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