Early Diversification of Seeds and Seed-Like Structures Cyrille Prestianni

Early diversification of seeds and seed-like structures Cyrille Prestianni

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Cyrille Prestianni. Early diversification of seeds and seed-like structures. Carnets de Geologie, Carnets de Geologie, 2005, CG2005 (M02/06), pp.33-38. hal-00167621

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Early diversification of seeds and seed-like structures.

[Diversification précoce des graines et structures assimilées]

Cyrille PRESTIANNI 1

Key Words: Seeds; diversity; Devonian; Lower Carboniferous; evolution

PRESTIANNI C. (2005).- Early diversification of seeds and seed-like structures. In: STEEMANS P. & JAVAUX E. (eds.), Pre-Cambrian to Palaeozoic Palaeopalynology and Palaeobotany.- Carnets de Géologie / Notebooks on Geology, Brest, Memoir 2005/02, Abstract 06 (CG2005_M02/06) Mots-Clefs : Graines ; diversité ; Dévonien ; Carbonifère inférieur ; évolution

The seed habit is one of the most important A. Moresnetia-type evolutionary acquisition in plant evolution. It The first type of preovule is the Moresnetia- allowed colonisation of new ecological niches, type. It is characterised by a four unit cupule leading to a level of diversification never formed by two successive cruciated observed before. The seed habit involves dichotomous divisions. Within this group, we occurrence of a single functional megaspore notice a progressive fusion of the within an indehiscent megasporangium integumentary lobes, ranging from completely (nucellus), development of an endosporic dissected in the Belgian taxon Moresnetia megagametophyte, enclosure of the nucellus by zalesskyi STOCKMANS (1948), emend. FAIRON- an integument, and capture of pollen before DEMARET et SCHECKLER (1987) [West European dispersal from the sporophyte. VCo biozone] to a nearly completely fused integument in Archaeosperma arnoldii PETTITT et Early ovulate structures are better regarded BECK (1968) [North American LE-LN biozone]. as preovules (sensu STEWART & ROTHWELL, 1993) Xenotheca devonica ARBER et GOODE (1915), as their nucellus is surrounded by unfused or emend. HILTON et EDWARDS (1999) [West partially fused integumentary lobes, and they European LL biozone] and Elkinsia polymorpha consequently lack a well-defined micropyle. The ROTHWELL et alii (1989), emend. SERBET et functions of the micropyle were than assumed ROTHWELL (1992) [North American VH biozone] by modifications of the nucellar apex. have an intermediate degree of fusion. The Many preovules are known from Upper degree of fusion of the integument can be Devonian deposits (see Fig. 1). They show a observed only on perfectly preserved variety of morphologies, but they all share the specimens. This led HILTON (1999) to doubt the same set of modifications of the nucellar apex: justification of a distinction between the genera the hydrasperman syndrome (ROTHWELL, 1986; Moresnetia, Elkinsia and Xenotheca. ROTHWELL & SCHECKLER, 1988). The nucellar apex We also include in the Moresnetia-type two is modified into a pollen chamber (sensu slightly different taxa: Kerrya mattenii ROTHWELL GORDON, 1941) closed by a plinth (sensu et WIGHT (1989) [West European LE/LN GORDON, 1941) and extended by a cylindrical biozone] and Lenlogia krystofovichii PETROSYAN structure (HILTON, 1996), the salpinx (sensu in LEPEKHINA et alii (1962) emend. KRASSILOV et GORDON, 1941). The pollen chamber contains a ZAKHAROVA (1995) [LL Biozone]. Kerrya mattenii central parenchymatous column. We here call possesses a six unit cupule, but its overall lagenostome (sensu SCOTT, 1917) the whole organisation conforms to the Moresnetia-type. modification of the nucellar apex, pollen Lenlogia krystofovichii is poorly understood, but chamber plus apex. may be provisionally included in this group All these Upper Devonian types show various because of its apparent structural resemblance. degrees of fusion of the integumentary lobes The Moresnetia-type comprises the most and/or characteristics of the cupule, a set of ancient type of preovules. Its first vegetative segments that usually encloses the representatives are found in the upper Frasnian pre-ovulate structure. On the basis of the of Russia (IURINA et alii, 1988). This early characteristics of these parts, the Upper occurrence may be a partial explanation for its Devonian preovules can be classified in the wide geographic distribution by late Famennian following types. times (see Fig. 2). This type ranged across the D/C boundary, for it is represented by the Carboniferous lagenostomalean seeds ovules (CLEAL, 1993; LONG, 1975).

1 Doctorant F.R.I.A., Département de Géologie, Laboratoire de Paléobotanique, Paléopalynologie et Micropaléontologie, Université de Liège, Allée du 6 août, B18, Sart-Tilman, 4000 Liège (Belgium) [email protected] 33 Carnets de Géologie / Notebooks on Geology - Memoir 2005/02, Abstract 06 (CG2005_M02/06)

Figure 1: Stratigraphic distribution of Devonian and Lower Carboniferous ovules and ovule-like structures. Dotted line separates preovules (left) from ovule-like structures (right). See text for references. Stratigraphic scale modified from DREESEN et alii (1993) and STREEL et alii (1987). AD. Acinosporites acanthomammilathus - Densosporites evonicus; BJ. Verrucosisporites bulliferus - Cirratriradites jekhowskyi; BM. Verrucosisporites bulliferus - Lophozonotriletes media; P. Spelaeotrilete balteatus - Rugospora polyptycha; CM. Schopfites claviger - Auroraspora macra; GF. Grandispora gracilis - G. famenensis; GH. Grandispora gracilis - A. hirtus; HD. Kraeuzelisporites hibernicus - Umbonatisporites distinctus; LE. Retispora lepidophyta - Indotriradites explanatus; LL. Retispora lepidophyta - Knoxisporites literatus; TA. Samarisporites triangulatus - Acyspora var. ancyrea; TCo. Samarisporites triangulatus - Chelinospora concinna; L; M; PC. Spelaeotriletes pretiosus - Raistrickia clavata; VCo. Diducites versabilis - Grandispora cornuta; VI. Vallatisporites allatus - Retusotriletes incohatus; LN. Retispora lepidophyta - Verucosiporites nitidus; VH. Apiculiretusispora verrucosa - Vallatisporites hystricosus.

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D. Condrusia-type B. Aglosperma-type The fifth type is the Condrusia-type The second type of preovule is the acupulate represented by three described species, C. Aglosperma-type. It includes: Aglosperma rumex STOCKMANS (1948), C. minor STOCKMANS quadrapartita HILTON et EDWARDS (1996) [West (1948) and C. brevis PETROSYAN in LEPEKHINA et European LL-LE biozone] and Aglosperma alii (1962). They differ from all the others in the avonensis HILTON (1998) [West European VI characteristics of their cupule which is Biozone]. Their integument is formed by three composed of two flat bilaterally symmetrical to four flat lobes fused up to their lower third. wings adpressed against each other. In the two species currently under investigation, C. rumex C. Warsteinia and Dorinnotheca-types and C. minor, the integument is not dissected An adaptation to anemochory may be into lobes and shows a complex organisation observed in the third and fourth types: the with three layers, the middle one consisting of Warsteinia-type and the Dorinnotheca-type. large sclerified cells. The nucellus appears to be Warsteinia paprothii ROWE (1997) [West fused with the integument. Its apex is modified European LE biozone] is acupulate. Its into a very long salpinx protruding above both integument is made of four winged lobes the integument and the cupule wings. adnate or fused to the nucellus. The Dorinnotheca-type, represented by E. Other preovules and seed-like Dorinnotheca streelii, FAIRON-DEMARET (1996) structures [West European VCo], is putatively In addition, two new types of preovules anemochoreous too. Its cupule is composed of occur in the Irish Hook Head locality (KLAVINS & eight parts fused proximally so that they form a MATTEN, 1999; KLAVINS, 2000). They are both cup, the segments of which divide to form at radially symmetrical and present the least 40 free endings. Each cupule contains only hydrasperman-type of reproduction. Their one central ovule. The integument is composed integument is made of four lobes fused basally of four free terete lobes (FAIRON-DEMARET, and curving inward over the ovule apex. One of 1996).

Figure 2 (modified from SCOTESE, 2002): In red the geographic area covered by the Moresnetia-type during the late Famennian. Data from PETTITT & BECK (1968), FAIRON-DEMARET & SCHECKLER (1987), IURINA (1988), ROTHWELL et alii (1989), ROTHWELL & WIGHT (1989), KRASSILOV & ZAKHAROVA (1995) and HILTON & EDWARDS (1999).

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the two new preovules presents an integument iterative (sensu BATEMAN & DIMICHELE, 1994) composed of three distinct layers. However, aspect of heterospory. without published description or illustration, further discussion is impossible. G. The Early Carboniferous representatives After Devonian times, a gap is observed in Some Upper Devonian seed-like structures the seed record. This remains enigmatic (it was are not understood well enough to be placed in probably related to lack of adequate deposits) one or another group. They are provisionally for a lot of vegetative parts assignable to seed- included in an heterogeneous type containing plants are found, but reproductive organs are the Frasnian seed-like structure Sphinxia recorded either not at all or very rarely wuhania LI et alii (1997), the enigmatic (GALTIER, pers. com.). It is only at the PC Spermolithus devonicus JOHNSON (1917) and the biozone that an increase in the seed record is two poorly described Belgian seeds "Xenotheca" observed. A very peculiar type of seed, bertrandii STOCKMANS (1948) and Coumiasperma remyi (GALTIER et ROWE, 1991) Pseudosporogonites hallei STOCKMANS (1948). has been reported once. It is atypical because the usual hydrasperman nucellar apical F. The earliest representatives modification is absent. This ovule is interpreted Contrary to earlier opinion, the preovules of as showing adaptation to aquatic dispersal the Upper Devonian are very diverse. This (GALTIER & ROWE, 1991). More classical diversity, as well as the sophistication of the hydrasperman types are also described as hydrasperman reproduction, strongly suggests Gnetopsis hispida GENSEL et SKOG (1977) and an origin for early seeds older than the Lagenospermum imparirameum ARNOLD (1939) Frasnian. The Givetian taxon Runcaria emend. GENSEL et SKOG (1977). Some other heinzelinii STOCKMANS 1948, emend. GERRIENNE taxa of the Lydienne Formation are also et alii 2004, probably represents one of the mentioned (ROWE & GALTIER, 1990; UNGER, early stages in this evolution (GERRIENNE et alii, 1856; MEYER-BERTHAUD & ROWE, 1997), but their 2004). This taxon already possesses most of affinities remain uncertain. However, some the characteristics of the Upper Devonian have been compared to the Moresnetia preovules (see above). It consists of a short morphological group (ROWE & GALTIER, 1990) or basal cuplike cupule made of four segments. to some Carboniferous genera. This cupule contains a radially symmetrical megasporangium surrounded by an integument After the CM biozone [Lower Carboniferous], comprising at least 16 free lobes. The we observe a rapid and important expansion of megasporangium bears a long distal extension the seed plants. The number of genera for emerging above the integument and enlarged isolated seeds increases (LONG, 1975); a lot of at the top. The apical extension of the types are known. This is the beginning of the megasporangium probably played a role in the worldwide dominance of seed plants. capture of microspores. Consequently, the reproductive biology of Runcaria putatively Bibliographic references included anemophilous pollination and dissolution of sporangial cells to allow ARBER E.A.N. & GOODE R.H. (1915).- On some fossil plants from the Devonian rocks of fertilization (GERRIENNE et alii, 2004). The morphology of its megasporangium and its North Devon.- Proceedings of the Cambridge presumable particular type of reproduction Philosophical Society, vol. 18, p. 89–104. distinguishes Runcaria from all the Famennian ARNOLD C.A. (1939).- Lagenospermum early seeds. imparirameum sp. nov., a seedbearing fructification from the Missipian of MARSHALL and HEMSLEY (2003) described Pennsylvania and Virginia.- Bulletin of the Spermasporites allenii, a Givetian seed- Torrey Botanical Club, Lawrence, vol. 6, p. megaspore. The "seed-megaspores" are 297-303. obligatory tetrads, with a unique functional and BATEMAN R.M. & DIMICHELE W.A. (1994).- three aborted megaspores. Spermasporites Heterospory: the most iterative key allenii seems to be enclosed in a sporangium. innovation in the evolutionary history of the Whether or not this sporangium is indehiscent plant kingdom.- Biological Reviews, remains unknown. The relative ultrastructural Cambridge, vol. 69, p. 345-417. simplicity of the outer megaspore layer and the CLEAL C.J. (1993).- Gymnospermophyta. In: presence of monomegaspory (sensu BATEMAN & BENTON M.J. (ed.), The Fossil Record 2.- DIMICHELE, 1994) led MARSHALL and HEMSLEY London, Chapman & Hall. (2003) to suggest gymnospermous affinities for DREESEN R., POTY E., STREEL M. & THOREZ J. Spermasporites. As the sporangium contains (1993).- Late Famennian to Namurian in the both micro- and megaspores, the structural Eastern Ardenne, Belgium.- Subcommission differences and the uncertainties about on Carboniferous Stratigraphy, Guidebook, dehiscence seem to us rather suggestive of a Services associés de paléontologie de lineage discrete from that of the seed plants. l'Université de Liège, 60 p. This taxon might be another example of the FAIRON-DEMARET M. (1996).- Dorinnotheca

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streelii FAIRON-DEMARET, gen. et sp. nov., a Abstract 17. new early seed plant from the upper KLAVINS S. & MATTEN L. (1999).- A new seed Famennian of Belgium.- Review of from the Upper Devonian of Southern Palaeobotany and Palynology, Amsterdam, Ireland.- XVI International Botanical vol. 93, n° 1-4, p. 217-233. Congress (Saint-Louis, August 1-7, 1999), FAIRON-DEMARET M. & SCHECKLER S.E. (1987).- Abstract. Typification and redescription of Moresnetia KRASSILOV V.A. & ZAKHAVOVA T.V. (1995).- zalesskyi STOCKMANS, 1948, an early seed Moresnetia-like plants from the Upper plant from the Upper Famennian of Devonian of Minusink basin, Siberia.- Belgium.- Bulletin de l'Institut Royal des Paleontological Journal, Moscow, vol. 29, n° Sciences naturelles de Belgique, Bruxelles, 1A, p. 35-43. (Sciences de la Terre), vol. 57, p. 183-199. LEPEKHINA V.G., PETROSYAN N.M. & RADCHENKO GALTIER J. & ROWE N.P. (1991).- A new G.P. (1962).- Main Devonian plants of the permineralized seed-like structure from the Altay-Sayan mountain region.- basalmost Carboniferous of France.- Neues Vsesoyuznogo Nauchno-Issledovatel'skogo, Jahrbuch für Geologie und Paläontologie - Geologicheskogo Instituta (VSEGEI), Trudy, Abhandlungen, Stuttgart, vol. 183, n° 1-3, (Novaya Seriya), Leningrad, n° 70, 189 p. p. 103-120. LI C.-S., HILTON J. & HEMSLEY A.R. (1997).- GENSEL P.G. & SKOG J.E. (1977).- Two Early Frasnian (Upper Devonian) evidence for Missipian seeds from the Price Formation of multiple origins of seed-like structures.- southwestern Virginia.- Brittonia, New York, Botanical Journal of the Linnean Society, vol. 29, n° 3, p. 332-351. London, vol. 123, p. 133-146. GERRIENNE P., MEYER-BERTHAUD B., FAIRON- LONG A.G. (1975).- Further observation on DEMARET M., STREEL M. & STEEMANS P. (2004).- some Lower Carboniferous Seeds and Runcaria, a Middle Devonian Seed Plant Cupules.- Transactions of the Royal Society Precursor.- Science, Washington, vol. 306, of Edinburgh, Edinburgh, vol. 69, n° 12, p. p. 856-858. 267-293. GORDON W.T. (1941).- On Salpingostoma dasu: MARSHALL J.E. & HEMSLEY A.R. (2003).- A Mid a new Carboniferous seed from East Devonian seed-megaspore from East Lothian.- Transactions of the Royal Society Greenland an the origin of the seed plants.- of Edinburgh, Edinburgh, vol. 60, n° 12, p. Palaeontology, London, vol. 46, part 4, p. 427-464. 647-670. HILTON J. (1996).- Famennian-Tournaisian plant MEYER-BERTHAUD B. & ROWE N.P. (1997).- A assemblages from South-West Britain.- Lower Carboniferous plant assemblage from Ph.D. thesis (unpublished), University of Thuringia (Germany): compressions.- Wales, Cardiff. Review of Palaeobotany and Palynology, HILTON J. (1998).- Spermatophyte preovules Amsterdam, vol. 97, n° 3-4, p. 361-379. from the basal Carboniferous of the Avon PETTITT J.M. & BECK C.B. (1968).- Gorge, Bristol.- Palaeontology, London, vol. Archaeosperma arnoldii - a cupulate seed 41, part 5, p. 1077-1091. from the Upper Devonian of North America.- HILTON J. & EDWARDS D. (1995).- A new Late Contributions from the University of Devonian acupulate preovule from the Taff Michigan Museum of Paleontology, vol. 22, Gorge, South Wales.- Review of n° 10, p. 139-154. Palaeobotany and Palynology, Amsterdam, ROTHWELL G.W. (1986).- Classifying the earliest vol. 93, n° 1-4, p. 235-252. Gymnosperms. In: SPICER R.A. & THOMAS B.A. HILTON J. & EDWARDS D. (1999).- New data on (eds.), Systematic and Taxonomic Xenotheca devonica ARBER & GOODE, an Approaches in Palaeobotany.- Oxford enigmatic early seed plant cupule with University Press, Oxford, p. 137-161. preovules. In: KURMANN M.H. & HEMSLEY A.R. ROTHWELL G.W. & SCHECKLER S.E. (1988).- (eds.), The Evolution of Plant Architecture.- Biology of ancestral gymnosperms. In: BECK Royal Botanical Gardens, Kew, p. 75-90. C.B. (ed.), Origin and Evolution of IURINA A.L. (1988).- The Middle and Late Gymnosperms.- Columbia University Press, Devonian floras of northern Eurasia.- New York, p. 85-134. Transactions of the Palaeontological ROTHWELL G.W., SCHECKLER S.E. & GILLESPIE W.H. Institute, Moskva, vol. 227, 176 p. (in (1989).- Elkinsia gen. nov., a Late Devonian Russian). Gymnosperm with cupulate ovules.- JOHNSON T. (1917).- Spermolithus devonicus Botanical Gazette, Chicago, vol. 150, n° 2, gen. sp. nov., and other pteridosperms from p. 170-189. the Upper Devonian beds of Kiltorkan.- ROTHWELL G.W. & WIGHT D.C. (1989).- Proceedings of the Royal Dublin Society, vol. Pullaritheca longii gen. nov. and Kerryia 15, p. 245-254. mattenii gen. et sp. nov., Lower KLAVINS S.D. (2000).- Anatomically preserved Carboniferous cupules with ovules of the gymnosperms from the Late Devonian of Hydrasperma tenuis-type.- Review of Ireland.- Botany 2000 "New Frontiers in Palaeobotany and Palynology, Amsterdam, Botany" (Portland, August 6-10, 2000), vol. 60, n° 3-4, p. 295-309.

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ROWE N.P. (1997).- Late Devonian winged Cambridge University Press, Cambridge, 535 preovules and their implication for the p. adaptative radiation of early seed plants.- STOCKMANS F. (1948).- Végétaux du Dévonien Palaeontology, London, vol. 40, part 2, p. supérieur de la Belgique.- Mémoires du 575-595. Musée Royal d'Histoire Naturelle de ROWE N.P. & GALTIER J. (1990).- A Lower Belgique, Bruxelles, vol. 110, 84 p. Carboniferous plant assemblage from La STOCKMANS F. (1968).- Végétaux mésodévoniens Serre (Montagne Noire, France). Part II. récoltés aux confins du Massif du Brabant Gymnosperms.- Review of Palaeobotany and (Belgique).- Institut Royal des Sciences Palynology, Amsterdam, vol. 63, n° 1-2, p. Naturelles de Belgique, Mémoires, Bruxelles, 91-115. vol. 159, p. 1-49. SCOTESE C.R. (2002).- Paleomap website.- STREEL M., HIGGS K., LOBOZIAK S., RIEGEL W. & http://www.scotese.com STEEMANS P. (1987).- Spore stratigraphy and SCOTT D.H. (1917).- The heterangiums of the correlation with faunas and floras in the type British Coal Measures.- Botanical Journal of marine Devonian of the Ardenne-Rhenish the Linnean Society, London, vol. 44, p. 59- regions.- Review of Palaeobotany and 105. Palynology, Amsterdam, vol. 50, n° 3, p. SERBET R. & ROTHWELL G.W. (1992).- 211-229. Characterizing the most primitive seed ferns. UNGER F. (1856).- Beitrag zur Palaeontologie I. A reconstruction of Elkinsia polymorpha.- des Thüringer Waldes. II.- Schiefer und International Journal of Plant Sciences, Sandstein Flora.- Denkschriften der Chicago, vol. 153, n° 4, p. 602-621. Akademie der Wissenschaften in Wien, vol. STEWART W.N. & ROTHWELL G.W. (1993).- 11, p. 139–186. Paleobotany and the evolution of plants.-