A new hypothesis about the origin of isoetalean lycopsids was proposed based on palynological data. The occurrence of three apical papillae on the proximal surfaces of miospores is a significant palynological feature that is clearly defined in both isoetalean and selaginellalean clades. Three apical papillae appeared for the first time within lower Silurian (Wenlockian ca. 430 My) and only in rhyniophytoid plants. Using this observation, we suggest that isoetalean lycopsids could have evolved directly from rhyniophytoids and not from protolepidodendralean lycopsids in the middle Devonian (Eifelian-Givetian) as previously suggested, because protolepidodendralean spores do not possess three apical papillae. Spores with three apical papillae, reported as dispersed as well as in situ, were recorded continuously from the lower Silurian (Wenlockian) through the Devonian, Carboniferous, Permian, Mesozoic to Cenozoic era and form a phylogenetically independent lineage.

Institute of Geology Academy of Sciences of the Czech Republic Rozvojová 269 16500 Prague Czech Republic

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Stewart W.N., Rothwell G.R. Paleobotany and the Evolution of Plants. 2nd ed. Cambridge University Press; Singapore: 2010. 536p

Taylor T.N., Taylor E.L., Krings M. Paleobotany: The Biology and Evolution of Fossil Plants. Academic Press; New York, NY, USA: 2009. 1230p

Thomas B.A., Cleal C.J. Arborescent lycophyte growth in the late Carboniferous coal swamps. New Phytol. 2018;218:885–890. doi: 10.1111/nph.14903. PubMed DOI

Wang Q., Li C.S., Geng B.Y., Chitaley S. A new species of Lepidostrobus from the Upper Devonian of Xinjiang, China and its bearing on the phylogenetic significance of the order Isoëtales. Bot. J. Linn. Soc. 2003;143:55–67. doi: 10.1046/j.1095-8339.2003.00200.x. DOI

Thomas B.A. Paleozoic herbaceous lycopsids and the beginning of the extant genera Lycopodium and Selaginella. Ann. Miss. Bot. Gard. 1992;79:129–153. doi: 10.2307/2399756. DOI

Simpson M.G. Plant Systematics. 3rd ed. Elsevier; Amsterdam, The Netherlands: 2019. Evolution and diversity of vascular plants.744p

Bek J. Paleozoic in situ spores and pollen. Lycopsida. Palaeontographica B. 2017;296:1–199. doi: 10.1127/palb/296/2017/1. DOI

Libertín M., Kvaček J., Bek J., Žárský V., Štorch P. Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous. Nat. Plants. 2018;4:269–271. doi: 10.1038/s41477-018-0140-y. PubMed DOI

Gonez P., Gerrienne P. A new definition and a lectotypification of the genus Cooksonia Lang 1937. Int. J. Pl. Sci. 2010;171:199–215. doi: 10.1086/648988. DOI

Fanning U., Richardson J.B., Edwards D. Cryptic evolution in an early land plant. Evol. Trends Pl. 1988;2:13–24.

Edwards D., Davies K.L., Richardson J.B., Axe L. The ultrasctucture of of spores of Cooksonia pertonii. Palaeontologia. 1995;38:153–168.

Fanning U., Richardson J.B., Edwards D. A review of in situ spores in Silurian land plants. In: Blackmore S., Barnes S.H., editors. Pollen and Spores: Patterns of Diversification, Systematics Association. Volume, 44. The Systematics Association (Clarendon Press); Oxford, UK: 1991. pp. 25–47.

Gensel P.G. Devonian in situ spores: A survey and discussion. Rev. Palaeobot. Palynol. 1980;30:101–132. doi: 10.1016/0034-6667(80)90009-3. DOI

Allen K.C. A review of in situ late Silurian and Devonian spores. Rev. Palaeobot. Palynol. 1980;29:253–270. doi: 10.1016/0034-6667(80)90062-7. DOI

Punt W., Hoen P.P., Blackmore S., Nilsson S., LeThomas A. Glossary of pollen and spore terminology. Rev. Palaeobot. Palynol. 2007;143:1–81. doi: 10.1016/j.revpalbo.2006.06.008. DOI

Neuburg M.F. Recent data on the morphology of Pleuromeia Corda from the Lower Triassic of the Russian Platform. Dokl. Akad. Nauk S.S.S.R. 1961;136:200–203.

Magdefrau K. Zur Morfologie und phylogenetischen Bedeutung der fossilen Pflanzengattung Pleuromeia. Beih. Bot. Zbl. 1931;48:119–140.

Grauvogel-Stamm L., Lugardon B. The Triassic lycopsids Pleuromeia and Annalepis: Relationships, evolution, and origin. Amer. Fern J. 2001;91:115–149. doi: 10.1640/0002-8444(2001)091[0115:TTLPAA]2.0.CO;2. DOI

Grauvogel-Stamm L., Lugardon B. The spores of the Triassic lycopsid Pleuromeia sternbergii (Munster) Corda: Morphology, ultrastructure, phylogenetic implications and chronostratigraphic inferences. Int. J. Pl. Sci. 2004;165:631–650. doi: 10.1086/386562. DOI

Bek J., Chitaley S., Grauvogel-Stamm L. Occurrence of spores from an isoetalean lycopsid of the Polysporia-type in the Late Devonian of Ohio, USA. Rev. Palaeobot. Palynol. 2009;156:34–50. doi: 10.1016/j.revpalbo.2009.04.008. DOI

Lugardon B., Grauvogel-Stamm L., Dobrushkina I. The microspores of Pleuromeia rossica Neuburg (Lycopsida, Triassic): Comparative ultrastructure and phylogenetic implications. C. R. Acad. Sci. Paris. 1999;329:435–444. doi: 10.1016/S1251-8050(00)80068-3. DOI

Lugardon B., Grauvogel-Stamm L., Dobrushkina I. Comparative ultrastructure of the megaspores of the Triassic lycopsid Pleuromeia rossica Neuburg. C. R. Acad. Sci. 2000;330:505–508. doi: 10.1016/S1251-8050(00)00145-2. DOI

Grauvogel-Stamm L., Lugardon B., Zavialova N. Microspores of the Middle Triassic lycopsid Lepacyclotes (syn. Annalepis) zeilleri: Morphology, ultrastructure, laminated zones and comments about the lycopsid evolution. Rev. Palaeobot. Palynol. 2022;301:104642. doi: 10.1016/j.revpalbo.2022.104642. DOI

Naugolnykh S.V., Zavialova N. Densosporites polaznaensis sp. nov. with comments on its relation to Viatcheslavia vorcutensis Zalessky. Palaeobotanist. 2004;53:21–33.

Lopez G., Perreira Z., Fernandez P., Picarra M., Oliveira T.J. Silurian to Lower Devonian palynomorphs from the Barrancos region, Ossa Morena zone, Portugal; Proceedings of the CIMP Faro’09 II Joint Meeting of Spores/Pollen and Acritarch Subcommissions; Faro, Portugal. 20–24 September 2009; pp. 63–68.

Wellman C., Steemans P., Vecoli M. Paleophytogeography of Ordovician–Silurian land plants. Geol. Soc. London Mem. 2015;38:461–476. doi: 10.1144/M38.29. DOI

Mehlqvist K., Steemans P., Vajda V. First evidence of Devonian strata in Sweden—A palynological investigation of Övedskloster drillcores 1 and 2, Skåne, Sweden. Rev. Palaeobot. Palynol. 2015;221:144–159. doi: 10.1016/j.revpalbo.2015.06.007. DOI

Rubinstein C., Steemans P. New palynological data from the Devonian Villavicencio Formation, Precordillera of Mendoza, Argentina. Amegh. 2007;44:3–9.

Kermandji A.M.H. Silurian-Devonian miospores from the western and central Algeria. Rev. Micropaléontol. 2007;50:109–128. doi: 10.1016/j.revmic.2007.01.003. DOI

Rubinstein C., Steemans P. Spore assemblages from the Silurian–Devonian boundary, in A1-61 borehole, Ghadames Basin, Libya. Rev. Palaeobot. Palynol. 2002;118:397–421. doi: 10.1016/S0034-6667(01)00124-5. DOI

Steemans P., Rubinstein C., Mélo J.H. Siluro–Devonian spore biostratigraphy of the Urubu River area, western Amazon Basin, northern Brazil. Geobios. 2008;41:263–282. doi: 10.1016/j.geobios.2007.06.003. DOI

Cramer F.H., Diez J.B. Earliest Devonian spores from the Province of Leon, Spain. Pollen Spores. 1975;17:331–344.

Rodriguez R.M. Miosporas de la Formacion San Pedro/Furada, (Silurico superior–Devonico Inferior), Cordillera Cantabrica, NO de Espana. Palinology. 1978;1:407–433.

Richardson J.B., Rodriguez R.M., Sutherland S.J. Palynological zonation of Mid-Palaeozoic sequences from the Cantabrian Mountains, NW Spain: Implications for inter-regional and interfacies correlation of the Ludford/Prıdolı and Silurian/Devonian boundaries, and plant dispersal patterns. Bull. Nat. Hist. Mus. Geol. 2001;57:115–162.

Le Herissé A. Les spores du Dévonien inférieur du Synclinorium de Laval (Massif Armoricain) Palaeontographica B. 1983;188:1–81.

Breuer P., Steemans P. Devonian Spore Assemblages from Northwestern Gondwana: Taxonomy and Biostratigraphy. Spec. Pap. Palaeontol. 2013;89:5–163.

Muro G.V.J., Rubinstein C.V., Steemans P. Silurian miospores from the Precordillera Basin, Argentina: Biostratigraphic, palaeonvironmental and palaeogeographic implications. Geol. Mag. 2014;151:472–490. doi: 10.1017/S0016756813000393. DOI

Holland C.B., Richardson J.B. The British Isles. In: Martinsson A., editor. The Silurian–Devonian Boundary. Schweitzerbarthische Verlagsbuchhandlung; Stuttgart, Germany: 1977. pp. 35–44. (International Union of Geophysical Sciences Series A No. 5. E).

Steemans P. Palynostratigraphie de l’Dévonien dans l’ouest de l’Europe. Service Géologique de Belgique. Mém. Eplicat. Cart. Géol. Min. Belg. 1989;27:453.

Rubinstein C., Melo J.H., Steemans P. Lochkovian (earliest Devonian) spores from the Solimoes Basin, northwestern Brazil. Rev. Palaeobot. Palynol. 2005;133:91–113. doi: 10.1016/j.revpalbo.2004.09.003. DOI

Mendlowicz P., Machado-Cardoso K.B., Pereira T.R., Steemans P. Resultados Palinoestratigráficos do Devoniano da Sub-Bacia de Alto Garcías (Bacia do Paranza–Brasil) In: Carvalho I.S., Cassa B.R.C.T., Schwanke C., Carvalho M.A., Fernandes A.C., editors. Paleontologia: Cenários de Vida. Interciência; Rio de Janeiro, Brazil: 2007. pp. 607–619.

McGregor C.D., Owens B. Devonian spores of eastern and northern Canada. Geol. Surv. Can. Pap. 1996;66:1–66.

McGregor C.D. Lower and Middle Devonian spores of Eastern Gaspé, Canada. I. Systematics. Palaeontographica B. 1973;142:1–77.

McGregor C.D., Camfield M.M. Upper Silurian to Middle Devonian spores of the Moose River Basin, Ontario. Geol. Surv. Can. Bull. 1976;263:1–63.

Richardson J.B., Lister R.T. Upper Silurian and Lower Devonian spore assemblages from the Welsh Borderland and South Wales. Palaeontol. 1969;12:201–252.

Al-Ghazí A. New evidence for the Early Devonian age of the Jauf Formation in northern Saudi Arabia. Rev. Micropaléontol. 2007;50:59–72. doi: 10.1016/j.revmic.2007.01.005. DOI

Moreau-Benoit A. Les spores du Dévonien de Libye. Premiére partie. Cah. Micropaléontol. 1979;4:1–58.

Turnau E., Milaczewski L.I., Wood G.D. Spore stratigraphy of Lower Devonian and Eifelian, alluvial and marginal marine deposits of the Radom-Lublin area (central Poland) Ann. Soc. Geol. Pol. 2005;75:121–137.

McGregor C.D. Late Silurian and Devonian spores from Bolivia. Acad. Nac. Cien. 1984;69:1–75.

Perez-Leyton M.A. Spores du Dévonien Moyen et Supérieur de la coupe de Bermejo-La Angostura (Sud-Est de la Bolivie) Ann. Soc. Géol. Belg. 1990;113:373–389.

Mortimer M.G. Some lower Devonian microfloras from southern Britain. Rev. Palaeobot. Palynol. 1967;1:95–109. doi: 10.1016/0034-6667(67)90113-3. DOI

LeHerisse A. Lower Devonian spores of the Laval Synclinorium (Massif Armoricain) Palaeontographica A. 1983;188:1–81.

Delsate D., Blieck A., Steemans P. Preliminary report of Lower to Middle Emsian (Lower Devonian) flora and fauna from Consthum and Merkholtz (Grand Duchy of Luxembourg) with Porolepid (Sarcopterygii) and Heterostracan Fish remains. Geol. Belg. 2003;7:21–26.

McGregor D.C., Playford G. Canadian and Australian Devonian Spores: Zonation and Correlation. Volume 125 Geological Survey of Canada; St. Ottawa, ON, Canada: 1992.

Loboziak S., Streel M. Late Lower and Middle Devonian miospores from Saudi Arabia. Rev. Palaeobot. Palynol. 1992;89:105–113. doi: 10.1016/0034-6667(95)00044-X. DOI

Moreau-Benoit A. Palynological datation the beds enclosing the plomb-zinc mineralization in the Weiss and Luderich Mines, (Lower Devonian, Bergishes Land, Rhine Schist Massif) C. R. Acad. Sci. 1985;300:295–300.

Arkhangelskaya A.D. Spores from Lower and Middle Devonian deposits of the Russian Plate. In: Menner V.V., Byvsheva T.V., editors. Atlas of Spores and Pollen of Phanerozoic Oil- and Gas-Bearing Strata of the Russian and Turanian. Volume 253. VTrudy Vsesoiuznogo Nauchno-Issledovatel’skogo Geologorazvedochnogo Neftianogo Instituta (VNIGNI); Moscow, Russia: 1985. pp. 32–80. (In Russian)

Richardson J.B., McGregor D.C. Silurian and Devonian spore zones of the Old Red Sandstone Continent and adjacent regions. Geol. Surv. Can. Bull. 1986;364:1–79.

Ravn R.L., Benson D.G. Devonian miospores and reworked acritarchs from southeastern Georgia, USA. Palynology. 1988;12:179–200. doi: 10.1080/01916122.1988.9989343. DOI

Loboziak S., Streel M., Caputo M.V., Melo J.H.G. Middle Devonian to Lower Carboniferous miospore stratigraphy in the Central Parnaiba Basin (Brazil) Ann. Soc. Géol. Belg. 1988;115:215–226.

McGregor D.C. Devonian spores from the Barrandian Region of Czechoslovakia and their significance for Interfacies correlation. Geol. Surv. Can. Pap. 1979;79:189–197.

Ouyang S. Microfossils from the Devonian Heitai Formation of Mishan County, Heilungjiang Province. Acta Palaeontol. Sin. 1984;23:69–84. (In Chinese with English 1324 summary)

Marshall J.E.A., Fletcher T.P. Middle Devonian (Eifelian) spores from a fluvial dominated lake margin in the Orcadian Basin, Scotland. Rev. Palaeobot. Palynol. 2002;118:195–209. doi: 10.1016/S0034-6667(01)00114-2. DOI

Loboziak S., Caputo M.V., Melo J.H.G. Middle Devonian—Tournaisian miospores biostratigrahy in the southwestern outcrop belt of the Parnaiba Basin, north-central Brazil. Rev. Micropaléontol. 2000;43:301–318. doi: 10.1016/S0035-1598(00)90154-5. DOI

Blieck A., Gagnier P.I., Bigey F.P., Edgecombe G.D., Janvier P., Loboziak S., Rachebeuf P.R., Sempere T., Steemans P. New Devonian fossil localities in Bolivia. J. South Amer. Earth Sci. 1996;9:295–308. doi: 10.1016/S0895-9811(96)00015-6. DOI

Turnau E. Miospore stratigraphy of Middle Devonian deposits from Western Pomerania. Rev. Palaeobot. Palynol. 1996;93:107–125. doi: 10.1016/0034-6667(95)00122-0. DOI

Uyeno T.T. Biostratigraphy and Conodont Faunas of Upper Ordovician through Middle Devonian Rocks, Eastern Arctic Archipelagon. Volume 210 Geological Survey of Canada; St. Ottawa, ON, Canada: 1990.

Loboziak S., Streel M. Some new data on the Devonian miospores of the Parana Basin (Brazil) Sci. Géol. Bull. 1987;44:381–391.

Burjack M.I.A., Loboziak S., Streel M. Quelques donne´es nouvelles sur les miospores de´voniennes du basin Paraná (Brasil) Sci. Geol. 1987;40:381–391.

McGregor D.C., Uyeno T.T. Devonian spores and conodonts of Melville and Bathurst Island, District of Franklin. Geol. Surv. Can. Pap. 1972;71:1–37.

McGregor D.C. Devonian miospores of North America. Palynology. 1979;3:31–52. doi: 10.1080/01916122.1979.9989183. DOI

Marshall J.E.A., Allen K.C. Devonian miospore assemblages from Fair Isle, Shetland. Palaeontology. 1992;25:277–312.

Su Y. A second time study of the Devonian “Heitai Formation” in the type locality of eastern Heilongjiang Province. Bull. Shen. Inst. Geol. Miner. Res. 1983;6:1–10.

Grey K.A. A mid-Givetian miospore age for the onset of reef development on the Lennard Shelf, Canning Basin, Western Australia. Rev. Palaeobot. Palynol. 1991;68:37–48. doi: 10.1016/0034-6667(91)90056-9. DOI

Bek J., Drábková J., Dašková J., Libertín M. The sub-arborescent lycopsid genus Polysporia Newberry and its spores from the Pennsylvanian (Bolsovian–Stephanian B) continental basins of the Czech Republic. Rev. Palaeobot. Palynol. 2008;152:176–199. doi: 10.1016/j.revpalbo.2008.05.002. DOI

Somers Y., Alpern B., Doubinger J., Grebe H. Revision du genre Lycospora Schopf, Wilson & Bentall. In: Alpern B., Streel M., editors. Les Spores. Volume 5. Microfossiles organiques du Paléozoïque; Centre National de la Recherche Scientifique (CNRS); Paris, France: 1972. pp. 9–110.

Ravn R.L. An Introduction to the Stratigraphic Palynology of the Cherokee Group (Pennsylvanian) Coals of Iowa. Volume 6. Iowa Geological Survey; Iowa City, IA, USA: 1986. pp. 1–117. Iowa Geological Survey Technical Paper.

Bek J. PhD Thesis. Geological Institute of the Academy of Sciences of the Czech Republic; Prague, Czech Republic: 1998. Spore Populations of Some Plants of Groups Lycophyta, Sphenophyta, Pteridophyta and Progymnospermophyta from Carboniferous Limnic Basins of the Czech Republic; pp. 1–505. (In Czech with English summary)

Molyneux S.G., Manger W.L., Owens B. Preliminary account of Late Devonian palynomorph assemblages from the Bedford Shale and Berea Sandstone Formations of central Ohio, USA. J. Micropalaeontol. 1994;3:41–51. doi: 10.1144/jm.3.2.41. DOI

Amenabar C.M., di Pasquo M., Carrizo H.A., Azcuy C.S. Palynology of the Chigua (Devonian) and Malimán (Carboniferous) formations in the Volcán Range, San Juan Province, Argentina. Part II. Cavate, pseudosaccate and cingulizonate spores. Ameghiniana. 2007;44:547–564.

Smith A.H.V., Butterworth M.A. Miospores in the coal seams of the Carboniferous of Great Britain. Spec. Pap. Palaeontol. 1967;1:1–324.

Bharadwaj D.C. On Porostrobus zeilleri Nathorst and its spores with remarks on the systematic position of P. benholdii Bode and the phylogeny of Densosporites Berry. Palaeobotanist. 1957;7:67–75.

Potonié R., Kremp W. Die Sporae dispersae des Ruhrkarbons ihre Morphographie and Stratigraphie mit Ausblicken auf Arten anderer Gebiete und Zeitabschnitte. Teil I. Palaeontographica B. 1955;98:65–121.

Peppers R.A. Spores in Strata of Late Pennsylvanian cyclothems in the Illinois Basin. Ill. St. Geol. Surv. Bull. 1964;90:1–89.

Bek J., Pšenička J., Drábková J., Zhou W.M., Wang J. Thomasites gen. nov. a new herbaceous lycophyte and its spores from late Duckmantian of the Radnice Basin, Czech Republic and palynological grouping of Palaeozoic herbaceous lycophytes. Rev. Palaeobot. Palynol. 2023;310:104842. doi: 10.1016/j.revpalbo.2023.104842. DOI

Chitaley S., McGregor C.D. Bisporangiostrobus harrissii gen. et sp. nov., an eligulate lycopsid cone with Duosporites megaspores and Geminospora microspores from the Upper Devonian of Pennsylvanian, USA. Palaeontographica B. 1989;210:127–149.

Grauvogel-Stamm L., Langiaux J. Polysporia doubingeri n. sp., un nouvel organe reproducteur de Lycophyte du Stéphanien (Carbonifère supérieur) de Blanzy Montceau (Massif Central, France) Sci. Géol. Bull. 1995;48:63–81.

Courvoisier J.M., Phillips T.L. Correlation of spores from Pennsylvanian coal-ball fructifications with dispersed spores. Micropaleontology. 1975;21:45–49. doi: 10.2307/1485154. DOI

Bharadwaj D.C. The palynological investigations of the Saar coals. Part I. Monography of sporae dispersae. Palaeontographica B. 1957;101:73–125.

Balme B.A. Fossil in situ spores and pollen grains: An annotated catalogue. Rev. Palaeobot. Palynol. 1995;87:81–323. doi: 10.1016/0034-6667(95)93235-X. DOI

Naugolnykh S.V. The heterosporous lycopodiophyte Pleuromeia rossica Neuburg, 1960 from the Lower Triassic of the Volga River basin (Russia): Organography and recontruction according to the “Whole-plant” concept. Wulfenia. 2013;29:1–16.

Pigg K.B. Evolution of isoetalean lycopsids. Ann. Miss. Bot. Gard. 1992;79:589–612. doi: 10.2307/2399754. DOI