Pa/aeobo/{[Ilisl 5 J (2002) 1- J I 0031-0174/2002/1-11 $2.00
An argument for the origins of heterospory in aquatic environments
R.K. KARl AND DAVID L. DILCHER2
I Birbal Salwi InSlilUle of Palaeobolany, 53 University Road, Lucknow 226 007, India. JFlorida Museum of Natural HiSlory, Universily of Florida, Gainesville FL 32611-7800, U.S.A. Email: [email protected], fax: 1-352-392-2539
(Received 29 June 200 I: revised version accepted 20 August 2002)
ABSTRACT
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INTRODUCTION Salvinia and Awl/a, as an effective means of reproduction. Four of these genera are aquatic while Selagill~l/ais widely llETEROSPORY is found today in the Lycopsida in distributed from moist forest floors to seasonally dry h Clubmosses Horsetails Ferns Seed-plants +0 Ma B.P. ~ E ® 0, ,, 300 11. .J Step 1°1 Pteropsida West ?10 ffi Q= ~ "'"ClI IViuI Lycopsida 340 •U 0) II CladoxyJopsida 360 I CD f\]0 =ClI 380-1=Q Zosterophyllopskta > ~~ *Questionable Identity +Questionable monophyly of des«ndanl class =ClI 'i: ITracbeopbyu s. LI 420 ~.2 ~ Fig. I-Tentative non-numerical phylogeny of all tracheophyte classes. showing putative ancestor-descendant relationships and divergence daleS: note ihat the class-level radiation occurred within the Devonian. Stippling indicates the minimum number of potentially independent origins of heterospory: (I) some Barinophytales. (2) all Selaginellales and Rhizomorphales. (3) some Equisetales, (4) some Sphenophyllales (doubtful), (5) some Stauropteridales, (6) all Salviniales, (7) all Marsileales, (8) some Filicales (e.g.. Plaryzoma*), (9) some Aneurophytales. (10) some Archaeopteridales, ?all Protopotyales, all Cecropsidales. (11) some Noeggerathiales. Note that the Gymnospermopsida inherit heterospory from their putative progymnospermopsid ancestor. Open circles indicate probable aquatic, open squares indicate possible aquatic (modified from Bateman & DiMichele, 1994). KAR & DILCHER-AN ARGUMENT FOR THE ORIGINS OF HETEROSPORY IN AQUATIC ENVIRONMENTS :l PRI GEDSIEGEM~ElF GIVFRASFAMCARB could be considered possible that the potential to capture a new dispersal strategy which increased out-crossing was an important driving force in evolution ofheterospory in or near ~.,~-o'O,",c,"b aquatic environments. The megaspores and microspores when @I9~~~~;~~;:!ci released in the water could drift freely mixing microspores and a megaspores from diverse populations of the same species and after fertilization further drifting to areas distant from either parent population where the new sporophyte generation would ~, then mature. The data for consideration of such a hypothesis 1°0 is presented here. b In this paper we are addressing only questions of initial 0 morphological changes that were driven by selection pressures as mentioned by Tiffney (1981). We suggest these selection pressures were directed by the potential for increased out it c crossing encouraged by heterospory in aquatic environments. We do not carry this argument further to include modifications of heterospory that might have carried these further to the evolution of the seed habit or seed-like habit (Bateman & DiMichele, 1994) or prepollen so common in the later Paleozoic 0 d seed land plants as discussed by Poort et al. (1996). During the Middle Devonian (Givetian), there were many new innovations in land plants (Banks, 1968; Chaloner & ~ Sheerin, 1979; Gensel & Andrews, 1984). By this time, some land plants, such as Aneurophyton had attained an arborescent e habit that included the production of secondary tissue and major branching systems. Heterosporous taxa were present at a) homospory b) inrenncdiaIC this time, some which must have been the precursors of seed c) heterospory d) naked megaspore with 3 aboned spores plants (Stewart, 1983). The seed habit represented an important c) seed innovation in the evolution of plants and became the normal habit of the various groups of vascular plants that were to Fig. 2-Diagrammalic record of the time of first appearance of differ become the dominant vegetation on the earth (Fig. 2). ent types of reproductive structures in Devonian fossil plants. Early Devonian spores were simple with a trilete mark, a. Sporangia with spores of same size (e.g., in Cooksonia). b. mostly azonate with smooth, apiculate or spinose Sporangia with spores of two sizes (e.g., in Cluzleuria). c. Spo ornamentation (Traverse, 1988). Early Devonian genera (Figs rangia with mega- and microspores (e.g., in Archaeopleri.\). d. Megaspore tetrad: one large. presumed fertile, three small pre 3, 4) such as Refusotriletes, Calamospora, Lopholrileles, sumed abortive (e.g., in Cysrosporiles). e. Radiospermic Acanthot riletes, Punctali sporites, Apiculatispori s, (Archa/!osperllla) and platyspermic (SperlllolirllU.I'j seeds (modi Leiotriletes and Emphanisporites are examples of these early fied from Chaloner & Sheerin 1979). spores (Banks, 1968). Large spores of 150-200 ~m,some pseudosaccate and some zonate, are known from the Middle that many megaspores and microspores of the Middle Devonian Eifelian and Givetian stages (Owens & Richardson, Devonian had morphological features that suggested that they 1972; Richardson, 1974; Turnau, 1986). At that time we also were dispersed in fresh water and demonstrated parallel see several spores with bifurcate processes such as morphological features with those megaspores and Ancyrospora, Hysfricosporites, Perotriletes, Nikitinsporilcs microspores of the aquatic ferns that evolved about 240 mi IIion and Dicrospora while there are some genera that have small years later during the Lower and Upper Cretaceous. It is bifurcate processes such as Densosporites devonicus and obvious from the paleobotanical record presented by Bateman Rhabdosporites langii. In the Late Devonian (Frasnian) & DiMichele (1994) (Fig. I) that heterospory has evolved continental and marginal marine facies, there often is dominance repeatedly in various major groups of plants at various times of spore genera with grapnel like processes. Pseudosaccatel during the history of land plant evolution. camerate spores are also found as common elements in these We suggest that the major stimulus for the initial evolution assemblages (Figs 3,4). Richardson (1969) observed that 50% of heterosporous reproductive systems in plants is to of the palynological assemblage from the Middle Old Red accommodate out-crossing in an aquatic environment. In such Sandstone of the Orcadian Basin, Scotland consists of an aquatic environment, a two dimensional dispersal system Ancyrospora and Rhabdosporites langii. Abundance of is available in which out-crossing is encouraged. Therefore, it Ancyrospora, Hyslricosporiles and Rhabdosporifes langii 4 THE PALAEOBOTANIST Series or Stage Banks, 1980 McGregor, 1977 Richardson, 1974 Post Famennian Tn Ib f------Tn la r-----?-----. V. nilidus Rhacophyton f------Assemblage - zone VII V.pllsil/ites FAMENNIAN f------f- -- S:Je.EJ1EP!!JIJ!!-- Archaeopleris L. crishfer Assemblage - zone VI f------FRASNIAN oplivus - bullalus ------~------Svalbardia Triangulailis GIVETIAN Assemblage - zone V f------f------Densosporites devonicus - orcadensis Hyenia devonicus ElFELIAN Assemblage - zone IV .....------Rhabdosporiles langii velala - langii Acinosporiles ------1-----.------acanlhomammillalus Grandispora Calyplosporiles UPPER annulailis - biomailis - proteus lindlarensis f------Psilophylon sexlanlii EMSIAN 1------'------Emphanisporiles annulalus LOWER Assemblage- zone III caperalus - emsiensis .....------Dibolisporiles cf gibberosus STEGENlAN ------~------r------Zoslerophyllum Emphanisporiles micrornatus Assemblage - zone II micrornatus - prOleus GEDINNIAN Sireelispora newportensis ------1------Cooksonia . Synorisporiles PRIOOLIAN Assemblage - zone I chulus - ? vermiculala tripapillatus KAR & DILCHER-AN ARGUMENT FOR THE ORIGINS OF HETEROSPORY IN AQUATIC ENVIRONMENTS 5 was also noticed in the Frasnian freshwater deposits of New according to the author may exhibit the beginning of biometric York State (Richardson, 1969). In the Famennian Stage of the heterospory. Late Devonian, a progressive decrease of the spores with Chaloner (1967) showed, in a series of histograms. a bifurcate processes, pseudosaccus and zona is observed (Fig. progressive increase in maximum spore size througQ the Early 4). and Middle Devonian and then a gradual segregation into Dilcher et af. (1992) advocated that the bifid, anchor like small spores and large spores and thus the commencement of processes and the apical prominence (acrolamella) found in heterospory (Fig. 7). The overall picture according to Chaloner these heterosporous Middle-Late Devonian spores were (1967) seems to be consistent with a progression from a phase produced in order to increase the potential to entangle and beginning early in the Devonian with a low degree of hold megaspores and microspore masses in close proximity heterospory and continuing later in the Middle and Late while the spermatozoa were released (Fig. 5). Also they Devonian to a much more pronounced size di fference between mentioned there might be some increase in volume ratio which microspores and megaspores. According to Sussex (1966) the would provide necessary buoyancy in the water. The presence fossil record suggests that there was an early and widespread of bifid processes in the Palaeozoic acritarchs (e.g., occurrence of heterospory in almost all the major groups of Micrhystridium shillelOllellsis, Polygollium gracilis), land plants. By the Late Devonian or Early Carboniferous Mesozoic, Tertiary (e.g., Acholllosphaera ramulifera, Lepidostrobus, Sigillariostrobus, Pleurollleia, Lepidocarpoll. Homotrybliul1l telluispillOSlllll) and Recent dinoflagellates, Mazocarpon and Miadeslnia of Lycopsida; Palaeostacllya Cretaceous (Arcellites) and Tertiary aquatic heterosporous and Calamostachys of Sphenopsida; Archaeopteris, hydropterideae as well as the extant Salviniaceae all Lagenostoma and Trigonocarpus of Pteropsida and many demonstrate similar functional morphologies. This is probably other plants as well had attained heterospory. related to the fact that many of these microspores and Cichan et al. (1984) considered that the term heterospory megaspores accomplished their fertilization in water. The has traditionally been used to describe plants that ha ve spores observation of Taylor et al. (1980) of the presence of smaller of two different sizes (morphological heterospory). However, microspores between the spines, or in the apical prominence because of the consistent correlation in extant plants between (acrolamella) of the megaspore Nikitillsporites calladensis, a bimodal distribution in spore size and the production of and of Winslow (1962) on the presence of smaller endosporic dioecious gametophytes, this term has also come ArchaeoperisacClts grains associated with Nikitillsporites, to denote a particular pattern of reproduction (biological as in extant Azo/fa, provides additional support for this heterospory). To ascertain whether or not a plant is contention. Archaeoperisaccus and NikitillSporites are mostly heterosporous (in the biologically heterosporous sense), small confined to Frasnian and according to McGregor (1979) are and large spores must be germinated and correlations between restricted to north of the palaeoequator (Fig. 6). Marshall & spore size and archegonial versus antheridial production Allen (1982) noted the simultaneous occurrence of four larger observed (Cichan et al., 1984; Bateman & DiMichele, 1994). and smaller species of Auroraspora and two species of a similar Platyzonza (Tryon, 1964) is the first example of a dioecious nature in Rhabdosporites from the Devonian sediments of condition in a heterosporous, terrestrial plant where the spores Shetland. Turnau and Karczewska (1987) also observed that of two different sizes are found and the small spores bear the nearly all the large spore species described by Fuglewiez and antheridia while the larger spores produce archegonia. Prejbisz (1981) from the Middle Devonian of Poland are DiMichele et ai. (1989), however, think that the gametophytes associated with smaller but otherwise similar spores. These of Platyzoma lack colonizing capabilities and that the life cycle genera are Apiculiretusispora, Biharisporites, Corollispora, is not comparable to heterosporous species with endosporic and Grandispora. The spores of the smaller size class are gametophytes. The ecological constraints inherent in the life themselves relatively large and their mean ranges from 90-207 history of Platyzoma make it an unlikely candidate for J.lm.Turnau and Karczewska (1987) suggest the reason for the evolutionary intermediate. DiMichele et af. (1989) advocated size increase of the isospores was to enhance the nutritional heterochrony to explain the independent evolution of capability for the developing gametophyte. They also heterospory in most lineages of the lower vascular plants. postulated that in the course of development of heterospory, Galtier (1964), Brack (1970) and Brack-Hanes (1978) endospory preceded size differentiation and presumably sex suggest that in fossil plants, where developmental studies are differentiation (Fig. 7). Similarly, spores of one sporangium of not possible, a biological definition of heterospory can only Fairone/fa reported by Gerrienne (1996) from the Early be applied in cases of morphological heterospory where mature Devonian of Belgium have size ranges from 37-210 11m.This gametophytes bearing either antheridia or archegonia are found preserved within the spore wall. In the cases when micro- ./ " Fig. 3-Showing the comparison of tentative megafossil generic assemblage zones in Devonian with palynological zones suggested by McGregor (1977), Richardson (1974) and Banks (1980) (after Banks. 1980). 6 THE PALAEOBOTANIST S GED. SIE. EMS. ElF. GIV. FRA FAM. Punctalisporiles Ambitisporiles LopbotriIeles - LeiolrileleS Calamospora Retusotriletes Granulatisporiles Emphanisporites Chelinospora TrileileS Bullatisporites Dictyotriletes Stenozoootriletes Samarisporites Lycospora Cirratriradites Murospora Camptozonotriletes Auroraspora Rhabdosporites Planisporites AcantholriJetes Apiculatisporis Cyclogranisporites Dibolisporiles VenucosisporileS Camptotriletes Convolutispora ReticuJatisporites Pezforosporites Densosporiles VallatisporileS Cadiospora Craspedispora Archaeozonotriletes Tholisporites Perolrililes Calyptosporites , GrandiSJlOr8 Geminospora Diaphanospora Ancyrospora CorystisporileS AnapiculatisporileS HystricosporileS Acinosporites Phyllothecotrileres Raislriclcia BiharisporileS Apiculiretusispora Spinozonotriletes Leiozonotriletes Aneurospora Cincl1lr3sporites Lophozonotrileres DiatomozollOuiletes HymenozonolriJetes Cymbosporites Nikitinsporites Archaeotriletes Enigmophytospora Brocliouiletes Reliosporites Camerozonotriletes Triangul.atisporiles CysIOSporiles • Lagcnorsporites Lagenicula Archaeoperisaccus Azonomonoletes Knoxisporites Canthospora Pulvini5pola KAR & DILCHER-AN ARGUMENT FOR THE ORIGINS OF HETEROSPORY IN AQUATIC ENVIRONMENTS 7 60 DiMichele (1994) suggest a spore size of200 11mis sufficient to designate megaspores as probably containing archegoniate- .c ri .,; 50 bearing gametophytes. • co co Unfortunately, the contents of dispersed spores from the co co 0 0 Devonian are not preserved and the parent plants of the co .. E E 40 Devonian spores with bifurcate processes, and most of the other megaspores, are not known. Balme and Hassell (1962). '0 POlonie (1965), Banks (1968) and Gensel (1980) detailed ill silu 0 30 0 spores of Devonian plants. According to Gensel (1980) spores described from the Devonian sporangia consist of 30 genera 20 and 40 species. She concluded that spore morphology seems A I B I c 0 E I I to be similar between the various species of some genera e.g.. megaspore species PsiLophyton, Pertim and Archaeopteris. Sometimes di fferent genera may have the same type of spores e.g., TelraxyLopleris Fig. 5-Givelian and Fransian megaspore species with apical promi and ReLlimia. Also, plants of quite different affinities have nence. a.p.h. = apical prominence height. e.d. =equatorial di ameter (modified from Allen. 1972). more or less similar types of spores e.g., Krilhodeophyloll, Cooksonia, CrassipariataLis and PsiLophyloll producing spores assigned to ApicuLiretusispora. and megagametophyte development are imperfectly known, Protobarinophyton and Barinophyton are exceptions they infer that biological heterospory was probably present because the in situ spores of these two genera are small and based upon a correlation with living plants. In cases where large spores (Cichan el aL., 1984). Both these genera exhibit the contents of the spores are not preserved, the precise nature intrasporangial heterospory, i.e., the spores within a single of the large and small spores is uncertain because the difference sporangium conforms to a bimodal size. According to Cichan in spore size may merely have been incidental and not el al. (1984) microspores of Prolobarinophyloll significant in a biological sense (Sussex, 1966). Bateman and pennsylvanicum are 30-42 11mand the megaspores are 410-560 Fig. 6-Geographical distribution of ArclUleoperimc('f(s (black squares) and Nikitin.l'poriles· (white squares) (modified from Streel el al., 1990; map modified from Scotese & McKerrow. 1990). ./ " Fig. 4-A table showing the first and last appearance of Devonian spore genera (modified from Chaloner, 1967). 8 THE PALAEOBOTANIST packed minute grana. The smaller spores, on the contrary, are 60 triangular in outline and ornamented with baculi, coni, etc. (Gensel & Andrews, 1984). The size range of the megaspore,', 0 l0- t» of Chaleuria cirrosa falls far below 200 J.lm, a conventional C size often used to mark heterospory in dispersed spores (PI. g, 40 1). '0 I I Mio - Taylor and Brauer (1983) considered that BarinophYlon l0- t» citrulliforme might be regarded as a transitional stage in the .0 20 E evolution of heterospory because the spores already differ in ::J Z size, wall structure and most importantly sexual expression but are still found in the same sporangium. Cichan el al. (1984) considered that in plants with spores distinct in size as well as (Sd) Ge. Si. Em. Ei. Gi. Fr. Fa. (Wes.) structure, there is a strong possibility that biological heterospory was also present. They thought that differential Fig. 7-A histogram showing the numbers of those genera which con sporoderm ultrastructure in conjunction with dimorphic spore tain species with a mean size exceeding 200 11mas megaspores (mega) in contradistinction to miospores (mio) (modified from size might potentially be a more viable indicator of heterospory Chaloner, 1967). than differences in spore size alone. Using such evidence they suggest that Prolobarillophyton pennsylvaniculII and B. citrulliforme were biologically heterosporous. In the extant J.lm.The microspores of Barinophylon cilmlliforme are 30-50 lycopods some species of Selaginella have micro- and J.lm and the megaspores are 650-900 J.lm. The sporangia of megaspores in the same sporangium. The same phenomenon Chalellria cirrosa (Andrews el al., 1974) also produce two was recorded by Goswami and Arya (1970) in !soetes pallIii kinds of spores. The smaller ones are 30-48 J.lmin size whereas and by Mondal (]978) in !soeles corolllandelilla. the bigger ones range from 60-156 J.lm and both types are The most characteristic feature of the megaspore of produced in the different sporangia. The larger spores are Protobarinophyton pennsylvanicum and BarillophvlOll subcircular-circular in shape and sculptured with closely citrulliforme is the wall structure. Both of them are spongy .' :'::~\.:~;.~-'~'. . I..;. • .!l..". ( • ' ...",t.,. '-.to' ''''''~'~~ "."f "". ._ . .. .. - ....-. ".~ .1 ~.\ . . \. 8 PLATEl Chalet/ria ,.irro.l"G. A. One single sporangium x 45 B. A presumed megaspore x 640 C. A presumed microspore x 64() (afler c Andrews er al., 1974) KAR & DILCHER-AN ARGUMENT FOR THE ORIGINS OF HETEROSPORY IN AQUATIC ENVIRONMENTS 'J and in P.pcnl1sylvanicum SEM study reveals a porous surface comprehensive understanding of the ecological significance layer while the subsurface layer is alveolate and seems to be of each organism. Such ecological context consists of an composed of superposed sheets of wall matelial with numerous understanding of the ways in which present day organisms oval/circular lacunae. In B. citrulliforlllc, the sporoderm layer function within their ecosystems, how their external ch'aracters of the megaspore is loosely arranged giving a spongy and physiology are adapted to their lives and the way in which appearance. The microspore wall of B. citrullifonnc has a their morphology fits the environments. The spongy wall homogeneous sporoderm and the microspore wall of P. structure of the megaspores of Azalla, Salvinia and Marsilca pcnl1sylval1icum is also different from that of the megaspore provide buoyancy in aquatic environments. Thus it may also (Taylor & Brauer, 1983; Cichan ct al., 1984). The spongy be postulated that the same character found in megaspore wall structure of P. pcnnsylvaniculll and B. Protobarinophyton and Barinophyton megaspore walls were citrulliformc shows some similarity to the megaspore wall adapted to the same kind of environment. In the opinion of structure of Azalia, Salvinia, lsoetcs, Marsilca, as well as Dodd and Stanton (1990), the analogy of morphologrcal Sclaginclla. Fitting (1900), Pettitt (1966), Fowler and Stennett similarities for individual entities or populations can be Wilson (1978), Lugardon and Husson (1982) and Zhiyan (1983) regarded as a valid argument for environmental interpretations observed several layers of spongy sporoderm in the that are time independent. Lorenz (1974) advocated that megaspore wall of Azalia where the sporopollenin elements whenever we find two kinds of life that are unrelated to each forming the ektexine have ramifying rod lets. Pettitt (1966), other with a similarity in form it is probably caused by parallel Lugardon (1973) and Lugardon and Husson (1982) also adaptations to SImilar environmental pressures. When we recorded fairly comparable sponginess in the megaspore wall correlate the megaspore wall structure of Protobarinophyton of lsoctcs and Marsilca. Similar differences between the pcnnsylvanicum and Barinophyton citrulllformc with the wall microspore and megaspore wall structure found in P. structure of megaspores of living heterosporous aquatic ferns pcnnsylvanicum and B. citrulliformc were also observed in and lycopods, we have to assume that these heterosporous the microspore and megaspore walls of Azalia, Salvinia, Devonian plants also lived in an aquatic environment. This Marsilca, lsoctcs and Selaginclla by Pettitt (1966), Stainer raises the possibility that heterospory may have originated in (1967), Lugardon (1972) and Lugardon and Husson (1982). An aquatic environments. DiMichele ct al. (1989) reasoned that exception to this observation is found in the wall structure of the heterosporous sexual system is most advantageous in the microspores and megaspores of Archacoptcris. Here the aquatic and semi-aquatic habitats because these exhibit wall structure in both microspores and megaspores found in physical conditions more consistently favourable for the the microsporangia and megasporangia in organic connection release of sperm and eggs. They further suggest that in such have similar wall features. Pettitt (1966) thinks the spores of environments the heterosporous species may have a distinct Archacoptcris cf. jacksonci was not far advanced from a advantage over homosporous forms. homosporous stage and the wall structure of the microspores Allen and Friend (1968) and Banks (1968, 1975) wrote and megaspores had not differentiated much beyond that of about the palaeoecology and palaeogeography of the the common ancestral isospore type. Devonian. According to them, when vascular plants appeared The spongy wall structure of the megaspores found in on land all the continents were joined to form a megacontinent Protobarinophyton and Barinophyton of the Devonian and and there may have been only about 2% oxygen in the extant Azalla, Salvinia, Marsilca, lsoctcs and Sclaginclla is atmosphere. In the uplands there were abundant metamorphic indeed very striking. Except for Sclaginclla, all are aquatic rocks and a predominance of mechanical over chemical heterosporous water plants. Dilcher ct al. (1992) have weathering. The earliest land plants seem to have occupied postulated that the presence of grapnel like processes in extant chiefly mud flats. However, Banks (1975) assumed that the aquatic Azalla, and in aquatic megaspores Arccllitcs and Rhynia chert flora of Emsian age is a good example of an Ariadnacsporitcs from the Late Cretaceous suggests that the inland intermontane bog (Fig. 6). Dineley (1979) remarked that heterosporous genera, Ancyrospora and Hystricosporitcs from as much as 85% of the surface of the earth was covered by the Middle and Late Devonian, also had an aquatic habit. water during Middle-Late Devonian time in addition to the While the megaspores of Protobarinophyton and presence of continental ice in the south polar region. None Barinophyton are devoid of bi fid processes, the spongy nature the less, the volume and the area covered by Devonian of the megaspore wall, which is comparable to the extant sediments are greater than those of other Palaeozoic systems megaspore walls of Azalla, Salvinia, lsoctcs and Marsilca (Raup, 1976). Gregor (1970) calculated that about 1.5 cubic strongly suggests that they had an aquatic habit also. kilometers of sediment accumulated per year during this period, Differences between the microspore and megaspore wall which is more than double that of the Cambrian, Ordovician or structure of these plants may also suggest such a habit. Carboniferous periods. According to Dineley (1979) this seems Dodd and Stanton (1990) assumed that to reflect the vigour of the geological cycle during the palaeoenvironmental reconstruction depend upon a Devonian. In North Atlantic, Devonian sedimentation took 10 THE PALAEOBOTANIST place widely and rapidly with thick greywackes and associated Andrews HN, Gensel PG & Forbes WH 1974. An apparently clastic rocks, cherts and volcanics. In north-west Europe heterosporous plant from the Middle Devonian of New BlUnswick. Russian platform volcanic activity was in full swing during Palaeontology 17: 387-408. Balme BE & Hassell CW 1962. Upper Devonian spores from the Early-Middle Devonian. In northern Asia, several cratonic Canning basin, Western Australia. Micropaleontology 8: 1-28. blocks collided and fused and stabilization was in progress Banks HP 1968. Devonian plants. In: Moore RC (Edilor) during the Devonian (Dineley, 1979). This turmoil in a vast Developments, trends. and outlooks in Paleontology. Journal of area was perhaps responsible for one of the three great Paleontology 42: 355-356. Phanerozoic phases of extinction of marine invertebrate life Banks HP 1975. Early vascular land plants: proof and conjecture. mostly referred to as Frasnian - Famennian mass extinction Bioscience 25: 730-737 (McLaren, 1970; Cooper, 1977). Obviously, such Banks HP 1980. Floral assemblages in the Siluro-Devonian. In: Dilcher palaeogeographical and palaeoecological conditions were not D & Taylor T (Editors)-Biostratigraphy of fossil plants: congenial for the plants to thrive in the terrestrial realm. The Successional and paleoecological analyses: 1-24. Dowden. marginal lacustrine environment where Ancyrospora, Hutchinson and Ross Inc., Stroudsburg, PA. Bateman RM & Dimichele WA 1994. Helerospory: The most iterative Hystricosporites and Rhabdosporites langii are found in key innovation in the evolutionary history of the plant kingdom. abundance could easily harbour and nourish the megaspores Biological Review 69: 345-417. at the cradle of their evolution. Brack S 1970. On a new structurally preserved arborescent lycopsid fructification from the Lower Pennsylvanian of North America. SUMMARY American Journal of Botany 57: 317-330. Brack-Hanes S 1978. On the megagametophytes of two The hypothesis is proposed here that aquatic lepidodendracean cones. Botanical Gazelle II: 412-428. environments have provided plants with the potential to Chaloner WG 1967. Spores and land-plant evolution. Review of Palaeobotany and Palynology I: 83-93. develop a heterosporous mode of reproduction. Heterospory Chaloner WG & Sheerin A 1979. Devonian macrotloras.ln: House has occurred independently in several groups (clades) of MR, Scrutton CT & Bassett MG (Editors)-The Devonian vascular land plants at different times ranging from the Middle System. Special Paper. Palaeontology 23: 145-161. Devonian to the Crelaceous. Many of the extant heterosporous Cichan MA, Taylor TN & Brauer OF 1984. Ultrastructural studies plants, that had their origins in these early times, are still1iving of in situ Devonian spores: Protobarinophyton pennsylvanicllll1 in aquatic environments. An aquatic environment provides Brauer. Review of Palaeobotany and Palynology 41: 167-175. increased potential for out-crossing between microspores and Cooper P 1977. Palaeolatitudes in the Devonian of Brazil and the megaspores and provides a safe environment in which to Frasian-Famennian mass extinction. Palaeogeography disperse microspores and megaspores. The heterosporous Palaeoclimatology Palaeoecology 21: 165-207. Dilcher DL, Kar RK & Dettmann ME 1992. The functional biology plants that gave rise to seed plants and heterosporous land of Devonian spores with bifurcate processes - a hypothesis. In: plants owe their origins to aquatic ancestries. Yenkatachala BS, Dilcher DL & Maheshwari HK (Editors) Essays in Evolutionary Plant Biology. Palaeobotanist 41: 67-74. Acknowledgements-Sincere appreciation is expressed to the Dimichele WA. DavisJI & Olmstead RG 1989. Origins ofheterospory Director. Birbal Sahni Institute of Palaeobotany, Lucknowfor inviting and the seed habit: The role 'Ofheterochrony. Taxon 38: I-II. Professor DL Dilcher to the BSIP at which time the work on this Dineley DL 1979. Tectonic setting of Devonian sedimentation. In: manuscript was formulated and a first draft was made. Thanks are House MR et al. (Editors)- The Devonian System. Special Paper. also extended to Dr Terry A. Lollfor assistance with illustrations and Palaeontology 23: 49-63. preparation of this manuscript. We would like to thank Professor Dodd 18 & Stanton JRS 1990. Paleoecology concepts and appl icalion Richard M. Bateman. Professor William A. DiMichele, and Biological John Wiley and Sons. New York. Reviewfor the use of Fig. I, and Professor Henry N. Andrews and the Fitting H 1900. Bau und Entwickelungsgeschichte der Makrosporen Palaeontological Associationfor the use offigures A, B, and C in Pl. von Isoetes und Selaginella und ihre Bedeutung fur die Kenntniss I. This paper is dedicated to Professor Leon Stuchlik in appreciation des Wachsthums pflanzlicher Zellmebranen. Botanische Zeitung for his professional service and recognition of the value of his many 58: 107-156. research contributions. Fowler K & Stennett-Wilson J 1978. Sporoderm architecture in modern Azalia. British Fern. Gazette II: 412-428. Fuglewiez R & Prejbisz A 1981. Devonian megaspores from NW REFERENCES Poland. 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