Origin of angiosperm characters Valentin A. Krassilov Krassilov VA 1996. Origin of angiosperm characters. Palaeobotanist45: 400-406. Models of origin for the typical angiosperm leaf, flower, stamen, pistil and double fertilization are based on evolutionary trends in proangiosperms. It is suggested that angiosperm organs are of chimeric origin, acquired by aggregation and fusion of progenitorial structures. J'hese morphological processes might involve different proangiosperm lineages in unstable (ecotonal, tectonically active) environments. An advantage of early angiosperms in such environments might be due to extended evolutionary potentials of their chimeric organs capable of acquiring new functions related to entomophily and zoochory. Key-words----Angiosperm origin, Morphology, Evolution, Proangiosperms. Valentin A. Krassilov, Palaeontological Institute, 123 Proftojusnaya, Moscow 117647, Russia. ~a:i1~aan-il~. ~. ~. '1fTlffrrv:ctft~tri~am:r-a:i1~aan-iltilmcfilFC1Cfi1mii ~ tR" ~ ~I ~ stfdlfqd ~ TfllT l ~ a:tl~do:ft\Jll WT ~ ~· tf; l"lfat"1Uf OITR CfiT ~ ~I ~ a:tiCfilR<fllll ~· ~~~it~ am:r-a:i1~ao:ft\Jll ~· CfiT ~ fcl'Cfim prrl I~ ~lt~::>il~daft;ffi4iit~Cfif4~~~-~<?f~~~cfil"~a:tT Tfl~I ANGIOSPERMS are plants of considerable structural ideal, or archetypal, rather than typical, for actually complexity including a number of characters, i.e., there could be none of the kind growing around. structural features essential for their description as a Even the expectations of finding archetypal an­ category of plant kingdom. There are characters they giosperm as a fossil are rapidly expiring with the share as well as those they do not share (or if share progress of palaeobotanical research. then reluctantly) with other plant categories. Among It is, thus, clear that the notion of angiosperm the non-shared characters, some are present in all or characters is meaningful only in comparison with majority of the hitherto studied angiosperms, the another plant category showing a number of similar It is character states alongside some dissimilar char­ the virtue which this latter category Our current no·- KRASSILOV-ORIGIN OF ANGIOSPERM CHARACTERS 401 PIATE 1 402 TIIE PALAEOBOTANIST angiosperms were taxonomically separated from giosperms, thus providing an angiosperm character gymnosperms. The mid-XIX century system-makers pool (Krassilov, 1975). Whether they all or any of have treated the both as divisions of Anthophyta, them actually gave rise to plants currently classified flowering plants, thus using the naked vs protected as angiosperms is another matter. More angiosperm ovules, and not the flower, as a principal distinction. characters are related to evolutionary trends in proan­ As far as the extant plants are concerned (and giosperms the more likely the angiosperm ancestry there was nothing else to be concerned at the time) of the latter would seem. Here I briefly summarize the the distinction is clear cut. With addition of fossil character origin models described in more details plants, such as cupuliferous pteridosperms or elsewhere (Krassilov, 1977, 1989, 1991): caytonias, it is not. On the other hand, the much 1. Proangiosperms including dirhopalostachians, debated problem whether the conifer seed-scale leptostrobaleans (czekanowskialeans), cayto­ complexes are flowers (of the same kind as the seed­ nias, and extinct gnetaleans were represented by scale complexes of grasses) or not seemed to have leptocaul trees with deciduous leafy spur shoots, been resolved by Florins (1938-1945) work on fossil shrubs and waterside - aquatic or semiaquatic - conifers showing that their seed-scales are herbs (Baisia: Krassilov & Bugdaeva, 1981). All ovuliferous shoots rather than ovuliferous leaves as these life forms might occur in early angiosperms. angiosperm carpels were then supposed to be. In Incidentally, Caspiocarpus, an early Albian an­ effect flowers were rendered typical of angiosperms giosperm from Kazakhstan with pistillate making synonymous to flowering plants. panicles attached to leafy shoots (Vachrameev & Flower itself was, with admirable circularity, defined Krassilov, 1979; Krassilov, 1991) was recons­ as a reproductive organ of flowering plants, although tructed as a herbaceous plant, and a quite similar bennettitalean flowers still posed some problems. form was then described from Koonwarra bed in when fossil data infringe a taxonomic Australia (Drinnan & Chambers, 1986). distinction the latter can nevertheless be sustained 2. The monocot-type parallel-veined leaves might either by ignoring the fossil data or by claiming the have phyllode origin (Arber, 1918) as evidenced fossil structures non-homologous - and therefore ir­ by histological studies (Kaplan, 1970) and similar relevant - to morphologically similar extant struc­ tendency in czekanowskians, gnetaleans ( tures, and both the methods have been vigorously witschia) and bennettites. Some of the by plant morphologists. Even aberrant phyllodial bracts still bearing miniature leaf living plants, such as gnetaleans, were treated in the blades (Harris, 1969; Krassilov, 1982a). same way. The morphological proximity of Cretaceous angiosperm leaves ly branching segments (Debeya, Proteophyllum, etc.), as well as Scoresbya-Sagenopteris leaf show inter- mediate shoot/leaf (caulome/ phyllome) ters (Krassilov, 1989). The typical dicot-type blade origin is modelled on the basis of segment fusion in compound leaves of peltasperms in­ cluding such supposedly proangiospermous plants as Furcula. Segment fusion by marginal meristems initially has not affected the originally open venation pattern. However, the PI.ATE 2 l. Pistillate head from the Palaeocene: of Kamchatka, x 20 (Maslova 4. Lemnoid fruit from the Maastrichtian of Mongolia. SEM, x 70 & Krassilov. in press). (Krassilov & Makulbekov, in press). 2. Individual flower of the same, SEM, x 30. 5. Ovule of the same showing funicle and embryo cap, SEM, x 10. 3. Flower showing distinct staminodes (s) and interfloral phyllomes (i), SEM, x 30. 6. Funicle of the same, SEM, 660. KRASSILOV-ORIGIN OF ANGIOSPERM CHARACTERS 403 PIATE 2 404 THE PALAEOBOTANIST hopalostachians. Some early angiospem flowers still retained a little modified anthocorm mor­ phology (Dilcher, 1979). Moreover, distinct inter­ floral phyllomes were recently found in florets of Palaeocene hamamelid heads (Maslova & Kras­ A silov, in press; Pl. 2, figs 1-3) indicating their primary rather than derived character in an­ giosperms. 5. Stamen origin is modelled on Meeusella, a staminate shoot with lateral branches bearing a pair of stalked sporangial heads (Krassilov & Bugdaeva, 1988; Pl. 1, fig. 3). Some lateral branches are sterile. The sporangial stalks­ second order branches, are of variable length along the axis. In the case of their extreme reduc­ tion the paired sporangial heads are sessile, with the primary branch apex protruding between them as a connective of bithecate anther. The latter thus might derive from a pair of second E order sporangiate branches while reduction of Text-figure I-Reconstruction of proangiospenn cupules: A- Lep­ the main axis would give a fascicle of stamens. tostrobus, B-Dtnopbyton, C-Eoantha, D-Batsia,. E-Caytonta and This model implies primary nature of fasciculate putative prototype with distinct subtending bract (after Krassilov, stamens (cf. Pauze & Sattler, 1978) as well as 1969). paired stamens, as in Saururaceae (Tucker, 1985) meristem occurring within the aggregate leaf and possibly also stamens with sterile ap­ blade might give rise to plate meristem which pendages (derived from sterile lateral branches mediated looping of the former midveins and, of Meeusella prototype), as in Monimiaceae and within the primary loops, oflateral veins and their Lauraceae. branches, thus forming areolate venation of 6. The tricolpate and triporate pollen grains appear­ several orders (Krassilov, 1991, 1995; Plate 1). ing rather early in the fossil record have no ob­ 3. The long debated homology of vessels in vious precursors among proangiosperms. How­ gnetaleans and angiosperms has been convinc­ ever, the monosulcate fossil pollen grains of ingly demons-trated by Muhammed and Sattler Eucommiiditestype have a zonal equatorial fur­ (1982). In addition, tracheid-like vessels with row (Hughes, 1994) or two additional furrows simple porous and scalariform perforation plates parallel to the sulcus. These furrows are scars of were found in bennettitalean leaf veins (Kras­ reduced sacci of monosaccate or bisaccate pollen silov, 1982a) evidencing the occurrence of this grains occurring in .caytonialeans and other character in more than one proangiosperm proangiosperms. A polarity change along is re­ groups. quired to transform Eucommiidites into tricolpate 4. Anthocorm model of angiosperm flower pollen grain of primitive angiosperms. Porate or (Meeuse, 1975) is supported by the occurrence of pseudoporate appertures first appeared in Clas­ anthocorms--essentially short shoots with apical sopollis, fossil pollen traditionally assigned to dusters of pistillate or staminate organs or both conifers but referred to extinct gnetaleans by mixed with interfloral phyllomes ( sterile leaves Krassilov Cl982b). Recently clumps of Classopol­ or cataphylls">--:-in several proangiosperm lis have been found in the guts ofJurassic insects groups, such as Irania, bennettites, czekano­ (Pl. 1, figs 4-6) evidencing pollinivory and possib­ wskias and possibly also caytonialeans and dir- ly entomophily. In these pollen grains the pore KRASSILOV-ORIGIN OF ANGIOSPERM CHARACTERS