Morphogenesis of the reproductive shoots of Welwitschia mirabilis and Ephedra distachya (Gnetales), and its evolutionary implications

For decades, Gnetales appeared to be closely related to angiosperms, the two groups together forming the anthophyte clade. At present, molecular studies negate such a relationship and give strong support for a systematic position of Gnetales within or near conifers. However, previous interpretations of the male sporangiophores of Gnetales as pinnate with terminal synangia conflict with a close relationship between Gnetales and conifers. Therefore, we investigated the morphogenesis of the male reproductive structures of Welwitschia mirabilis and Ephedra distachya by SEM and light microscopy. The occurrence of reduced apices to both halves of the antherophores of W. mirabilis gives strong support for the assumption that the male ‘flowers’ of W. mirabilis represent reduced compound cones. We assume that each half of the antherophore represents a lateral male cone that has lost its subtending bract. Although both halves of the antherophores of Ephedra distachya lack apical meristems, the histological pattern of the developing antherophores supports interpreting them as reduced lateral male cones as well. Therefore, the male sporangiophores of Gnetales represent simple organs with terminal synangia. Although extant conifers do not exhibit terminal synangia, similar sporangiophores are reported for some Cordaitales, the hypothetical sister group of conifers. Moreover, several Paleozoic conifers exhibit male cones with terminal sporangia or synangia. Therefore, we propose that conifers, Cordaitales and Gnetales originated from a common ancestor that displayed simple sporangiophores with a terminal cluster of sporangia.     

Morphogenesis of leaves and cones of male short-shoots of Ginkgo biloba L.

Although the subject of several studies, the phylogeny of Ginkgo biloba is still ambiguous. Most of the morphological and some palaeontological studies assume a close relationship to conifers, but other palaeontological studies regard the origin of Ginkgo biloba in groups that exhibit a pinnate bauplan like Peltaspermales or Dicranophyllales. This divergence has led to controversial interpretations of male sporangiophores and leaves. Attempting to resolve this, here we have investigated the male cones and leaves of short-shoots by SEM and light-microscopy. Our results indicate that the male sporangiophores are simple structures, and the observed formation of thickened cell walls at the sterile adaxial side of the sporangiophores, similar to the endothecium of the sporangia, gives weak support for a precursor of Ginkgo-sporangiophores that displayed simple male sporangiophores with radial arrangement of the sporangia. Thus, our interpretations of the male sporangiophores of Ginkgo biloba allude to a relationship with Coniferales, Gnetales and Cordaitales and reject a close relationship of Ginkgo biloba with pinnate groups like Cycadaceae, as assumed by some molecular studies. In contrast to previous studies on long-shoot leaves, our results on short-shoot leaves give no indication for a compound character of Ginkgo leaves. Moreover, we infer that Ginkgo leaves could be derived from a simple bauplan, by two modifications of the basic growth pattern of conifer leaves, assuming that the dissection of Ginkgo leaves is secondary. Although more comparative investigations are necessary, our results support a coniferophyte origin of the Ginkgoales.     

CALLANDRIUM CALLISTOPHYTOIDES,GEN. ET SP. NOV., THE PROBABLE POLLEN-BEARING ORGAN OF THE SEED FERN,CALLISTOPHYTON

A new genus of pteridosperm pollen organ is described from Pennsylvanian age coal balls of Illinois. Individual sporangia are grouped into radial synangia which are borne in opposite pairs on the abaxial surface of slightly modified pinnules. Sporangia contain monosaccate pollen with a distinct sulcus, referable to the pollen genus Vesicaspora. Pinnules are borne on a regularly pinnate frond which is circinately coiled when young. At least a large portion of the frond is fertile and possesses anatomical features similar to those of Callistophyton. Phyletic relationships with other pteridosperm pollen organs are discussed.     

Oscillatory Heat-Production in the Male Cones of Cycads

Microcalorimetric analysis of heat-production by single intactsporophylls from thermogenic male cones of two cycad species(Ceratozamia miqueliana H. Wendl. and Zamia furfuracea L. f.)showed an oscillatory behaviour for three consecutive days duringpollen maturation and shedding. In sporophylls from C. rumphiiMiq., a weakly thermogenic species with no maximum of heat-production,such oscillations were not detected. The presence of the alternativerespiratory pathway in the sporophylls of the male cones ofZamia pumila L. has been demonstrated. Key words: Alternative pathway, cycads, heat-production, microcalorimetry, oscillation     

DEVELOPMENT OF THE POLLEN TUBE OF ZAMIA FURFURACEA (ZAMIACEAE) AND ITS EVOLUTIONARY IMPLICATIONS

Compared with pollen tubes of conifers, gnetophytes, and angiosperms, the pollen tube of cycads is exclusively a vegetative structure, uninvolved with the siphonogamous conduction of sperm to an egg. The cycad pollen tube appears to function primarily to obtain nutrients for the extensive growth and development of the male gametophyte. Previous workers have suggested that, similar to an haustorial fungus, the cycad pollen tube penetrates the reproductive tissues of the sporophyte by enzymatically destroying nucellar cells. These earlier studies did not document the precise structural relationship between the growing male gametophyte and its “host” tissue, the nucellus. Pollen tube growth, and its relation to the nucellus, was examined in Zamia furfuracea with light and transmission electron microscopy. Following germination, the pollen tube of Zamia furfuracea grows intercellularly through the subepidermal layers of the micropylar apex of the nucellus. Electron micrographs clearly show additional localized outgrowths of the pollen tube penetrating the walls of individual nucellar cells. Intracellular haustorial growth ultimately leads to the complete destruction of each penetrated cell, and appears to induce the degeneration of proximal unpenetrated nucellar cells. This pattern of intracellular penetration of the sporophyte by the male gametophyte in Zamia furfuracea is fundamentally different from what has been described in any other major group of seed plants (where intercellular growth of the male gametophyte is the rule), and suggests that the heterotrophic and tissue-specific relationships that male gametophytes of seed plants have with their host sporophytes are substantially more diverse than had previously been known.     

Zamia grijalvensis sp. nov. (Zamiaceae,Cycadales) from Chiapas,Mexico with notes on hybridization and karyology

Zamia grijalvensis, a new cycad species from Chiapas, México, is described and illustrated. This species is similar to Z. lacandona with respect to leaves, but differs in habit, morphology and colour of the female and male cones. The female cone of Z. grijalvensis is reddish brown to orange brown, whereas that of Z. lacandona is dark brown with lighter beige tomentum. The male cone of Z. grijalvensis is erect, whereas that of Z. lacandona is decumbent. The new species may be of natural hybrid origin and is discussed in the light of other findings among cycads. Preliminary diploid chromosome counts for Z. grijalvensis 2n = 19, 20 and karyotypes appear variable, as previously found in its congeners with wide distribution, such as Z. paucijuga and Z. prasina, both of which are characterised by high diploid numbers with a high number of telocentric and few metacentric chromosomes. These changes in chromosome number are probably the result of stressful environmental factors.     

Caterpillars of Eumaeus childrenae (Lepidoptera: Lycaenidae) feeding on two species of cycads (Zamiaceae) in the Huasteca region, Mexico

There are few genera of butterflies that feed on cycads. Among them the genus Eumaeus (Lycaenidae) presents aposematic coloration in all its life stages. In this work we report for the first time the herbivory of young leaflets of Ceratozamia mexicana and Zamia fischeri (Zamiaceae) by caterpillars of E. childrenae in their natural habitat in the Huasteca region, Mexico.     

STUDIES OF PALEOZOIC MARATTIALEANS: THE MORPHOLOGY AND PROBABLE AFFINITIES OF TELANGIUM PYGMAEUM GRAHAM

Telangium pygmaeum Graham is known from Upper Pennsylvanian coal balls from the Calhoun coal mine (Illinois). The species was described as possessing radial synangia consisting of 3-5 sporangia fused laterally for about f13 their length. Synangia were believed to be sessile and borne terminally or laterally on a branching rachis without lamina. Examination of new coal ball material of the same age indicates that the synangia are borne abaxially on the pinnules of a compound frond with the anatomy of a Psaronius leaf (Marattiales). Synangia are sessile and borne in two rows, one on either side of the pinnule midrib, under the unbranched lateral veins. Synangia are radial, 0.6 mm in diam, and consist of a ring of thin-walled sporangia fused to near their apices prior to dehiscence, but separating on dehiscence to release spores along their inner midline. Spores are spherical, trilete, 30-48 μm in diam, with a granulate ornamentation. The new genus Araiangium is proposed for this material based on the organization of the sessile thin-walled synangia. Araiangium is compared with other marattialean genera with sessile synangia (Acaulangium, Acitheca), and with the pedicellate synangia of various species of Scolecopteris. Criteria used in the delimitation of genera in Paleozoic anatomically preserved marattialean fertile foliage are discussed.     

Cyanobiont diversity within and among cycads of one field site.

Limited diversity was found among cyanobionts from a cultivated population of cycads at a field site in Florida. All isolates were classified as Nostoc but were different from the one Nostoc species found in the soil. These cyanobacteria were root endophytes of several plants of Zamia integrifolia and one of Dioon. The isolates were similar morphologically and in their reactions to four fluorescein isothiocyanate conjugated lectins. Electrophoretic protein profiles and zymograms distinguished one cyanobiont and the soil Nostoc. A tenacious Anabaena epiphyte was also discovered inhabiting the surfaces of root nodules.     

Paleozoic seed fern pollen organs

Paleozoic pollen organs exhibit numerous morphological forms that have been arranged in categories based on their probable organization. Progymnosperm ancestors are characterized by three dimensional branching systems bearing pairs of terminal sporangia. Early Mississippian examples of seed fern fertile branches appear little modified from the progymnosperms. These pteridosperm microsporangia are nonsynangiate and thin walled with longitudinal dehiscence. By Upper Mississippian time all forms show sporangial clustering into large or small groups, with several taxa exhibiting radially symmetrical synangia. In the Lower Pennsylvanian all pollen organs are synangiate and appear to consist of a uniseriate ring of sporangia that either surround a central hollow, or are bilaterally flattened. Sporangial dehiscence in all forms is longitudinal and toward the center of the synangium. In bilateral synangia with no central hollow, the sporangia either separate laterally or effective dehiscence areas are restricted to the free apical portions of the sporangia. Callistophytacean synangia resemble the lyginopterid type, but are abaxial on laminar foliage. This family is thought to have evolved from the lyginopterids during the Early Pennsylvanian. Middle Pennsylvanian medullosan pollen organs are all radial and may be solitary, aggregated into groups, or fused into a large compound synangium. Several pollen organ types are reinterpreted, and the possible evolutionary relationships among the various Paleozoic pollen organ forms are discussed based on synangial organization, patterns of frond branching, and pollen or prepollen morphology.     

Lunzia austriaca – a bennettitalean microsporangiate structure with Cycadopites-like in situ pollen from the Carnian (Upper Triassic) of Lunz,Austria

Based on new evidence obtained from freshly collected fossils, we here provide an emendation of Lunzia and Lunzia austriaca with an updated interpretation of the organ architecture, function and affiliation. The specimens reveal that Lunzia austriaca is a pollen organ resembling structures assigned to Weltrichia. Lunzia austriaca comprises cup-shaped pollen organs that develop up to about ten, basally fused lobes carrying appendices. The appendices are arranged pairwise and inserted laterally to a rachis-like structure, in a pinnate architecture on their adaxial side and are interpreted as prominent segments or fertile pinnae that bear numerous synangia identifying them as microsporophylls. The nature of the rachis-like structure is not straightforward. The rachis-like structure could either be fused with a bract – this fused structure then constituting the lobes – or itself been modified depicting a foliate appearance. The microsporophylls are narrow at the base and involute apically or with a sterile apical cowl. Numerous synangia with contracted bases are arranged on the inner (adaxial) side of the microsporophylls in long rows. The synangia consist of presumably four pollen sacs (microsporangia), are oblong and dehisce longitudinally. The pollen is monosulcate, elliptical and with a smooth exine (psilate). It is identified as Monocolpopollenites (=Cycadopites); from the size range, it fits best into Cycadopites accerimus. The architecture and the epidermal anatomy of Lunzia austriaca is discussed and its structure is compared with several contemporary bennettitaleans; sterile foliage and ovulate structures most likely associated with Lunzia austriaca are Pterophyllum filicoides and Westersheimia pramelreuthensis, respectively.     

Morphology and anatomy of male cones of Pseudotaxus chienii (W.C. Cheng) W.C. Cheng (Taxaceae)

Results of the present study indicate that male cones of Pseudotaxus chienii are representing inflorescences with strongly reduced flowers. The results fit quite well with investigations showing that sporangiophores of Taxus and also of Pseudotaxus comply with reduced flowers. The only difference between male cones in Taxus and Pseudotaxus is the absence of pherophylls in Taxus. Furthermore our results complete a transition series beginning with Cephalotaxus going on to Pseudotaxus and ending with Taxus and Torreya. In this progression Pseudotaxus can be regarded as an intermediate link between the inflorescences of Cephalotaxus and the simple, unbranched cones of Taxus. The entire transition series shows that sporophyll-like sporangiophores can be derived by reduction of lateral cones. There is however no sign that a similar process has occurred in other conifer groups.     

Testing co-evolutionary hypotheses over geological timescales: interactions between Mesozoic non-avian dinosaurs and cycads

The significance of co‐evolution over ecological timescales is well established, yet it remains unclear to what extent co‐evolutionary processes contribute to driving large‐scale evolutionary and ecological changes over geological timescales. Some of the most intriguing and pervasive long‐term co‐evolutionary hypotheses relate to proposed interactions between herbivorous non‐avian dinosaurs and Mesozoic plants, including cycads. Dinosaurs have been proposed as key dispersers of cycad seeds during the Mesozoic, and temporal variation in cycad diversity and abundance has been linked to dinosaur faunal changes. Here we assess the evidence for proposed hypotheses of trophic and evolutionary interactions between these two groups using diversity analyses, a new database of Cretaceous dinosaur and plant co‐occurrence data, and a geographical information system (GIS) as a visualisation tool. Phylogenetic evidence suggests that the origins of several key biological properties of cycads (e.g. toxins, bright‐coloured seeds) likely predated the origin of dinosaurs. Direct evidence of dinosaur–cycad interactions is lacking, but evidence from extant ecosystems suggests that dinosaurs may plausibly have acted as seed dispersers for cycads, although it is likely that other vertebrate groups (e.g. birds, early mammals) also played a role. Although the Late Triassic radiations of dinosaurs and cycads appear to have been approximately contemporaneous, few significant changes in dinosaur faunas coincide with the late Early Cretaceous cycad decline. No significant spatiotemporal associations between particular dinosaur groups and cycads can be identified – GIS visualisation reveals disparities between the spatiotemporal distributions of some dinosaur groups (e.g. sauropodomorphs) and cycads that are inconsistent with co‐evolutionary hypotheses. The available data provide no unequivocal support for any of the proposed co‐evolutionary interactions between cycads and herbivorous dinosaurs – diffuse co‐evolutionary scenarios that are proposed to operate over geological timescales are plausible, but such hypotheses need to be firmly grounded on direct evidence of interaction and may be difficult to support given the patchiness of the fossil record.     

A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region

Phylogenetic relationships among the three families and 12 living genera of cycads were reconstructed by distance and parsimony criteria using three markers: the chloroplast matK gene, the chloroplast trnK intron and the nuclear ITS/5.8S rDNA sequence. All datasets indicate that Cycadaceae (including only the genus Cycas) is remotely related to other cycads, in which Dioon was resolved as the basal-most clade, followed by Bowenia and a clade containing the remaining nine genera. Encephalartos and Lepidozamia are closer to each other than to Macrozamia. The African genus Stangeria is embedded within the New World subfamily Zamiodeae. Therefore, Bowenia is an unlikely sister to Stangeria, contrary to the view that they form the Stangeriaceae. The generic status of Dyerocycas and Chigua is unsupportable as they are paraphyletic with Cycas and the Zamia, respectively. Nonsense mutations in the matK gene and indels in the other two datasets lend evidence to reinforce the above conclusions. According to the phylogenies, the past geography of the genera of cycads and the evolution of character states are hypothesized and discussed. Within the suborder Zamiieae, Stangeria, and the tribe Zamieae evolved significantly faster than other genera. The matK gene and ITS/5.8S region contain more useful information than the trnK intron in addressing phylogeny. Redelimitations of Zamiaceae, Stangeriaceae, subfamily Encephalartoideae and subtribe Macrozamiineae are necessary.     

Pollination of the cycad <Emphasis Type="Italic">Zamia incognita</Emphasis> A. Lindstr. &amp; Idárraga by <Emphasis Type="Italic">Pharaxonotha</Emphasis> beetles in the Magdalena Medio Valley,Colombia: a mutualism dependent on a specific pollinator and its significance for conservation

The genus Zamia (Zamiaceae: Cycadales) exhibits its greatest diversity in Colombia and is highly threatened by habitat loss, extraction for ornamental plant trade, and mining, among other factors. One of the most important considerations for the effective conservation of Zamia is its highly specialized reproductive biology. Despite the importance of pollination for the populations’ viability, no studies have examined the pollination process of cycads in Colombia. Herein, we describe the pollination process of Zamia incognita A. Lindstr. & Idárraga, in a natural population. Exclusion experiments were performed by selectively excluding wind, beetles, both, or neither, which demonstrated that Pharaxonotha beetles are effective pollinators of Zamia incognita and that wind does not play any role as pollen vector. By following beetles marked with fluorescent dyes and directly observing beetle movements on and into female cones and micropyles, we confirmed that Pharaxonotha sp. is the effective pollinator of Z. incognita. The beetles traveled a maximum dispersal distance from a male to female cone of nearly 22 m and a minimum distance of 5 m. We found Pharaxonotha beetles in male cones, where they complete their life cycle. Cones produce heat in a circadian pattern associated with the elongation of the cones and pollen shedding. The increase in cones’ temperature appears to play an important role in beetle attraction. We suggest that pollination droplets on the micropyles would be a reward to pollinators. We also discuss the relationship of this Zamia species with other insects, which have important consequences for the conservation of web interactions.     

苏铁类植物传粉生物学研究进展(综述)

苏铁类植物是现存最古老的种子植物,研究其传粉特点,对于研究种子植物的起源与演化、植物与动物的协同进化以及苏铁类植物的繁殖机制、濒危机制有重要意义。本文从苏铁雌雄株开花物候学、传粉媒介及传粉机制等方面,对苏铁类植物传粉生物学相关研究进行综述,并提出今后该类植物传粉生物学研究的建议：对更多苏铁属种类未知的传粉机制进行研究;更广泛地应用排除法研究苏铁类特别是苏铁属植物的传粉媒介,进一步探讨传粉昆虫与苏铁类的共生关系问题。     

Two new species of the pinnate microsporophyll Pramelreuthia from the upper Triassic of the southwestern United States

Two new species of the enigmatic gymnosperm microsporophyll Pramelreuthia, found in the Upper Triassic Chinle Formation at five localities in the southwestern United States, provide significant new evidence on key morphological characters of the genus and extend its known geographical range. These new fossils also demonstrate that the genus was polytypic and reveal the plant megafossil sources for several common and geographically widespread dispersed Upper Triassic microfossil taxa. The genus Pramelreuthia, which until this study was known only from a single specimen from the Upper Triassic of Austria, is a planar pinnate structure consisting of a slender naked axis bearing stalked synangia in opposite to subopposite pairs. Synangia of all three species of Pramelreuthia are oval to subrectangular in lateral view and are composed of two adpressed flattened valves each of which contains up to 20 or more elongate, subcylindrical, tapered sporangia that bear nonstriate bisaccate pollen. Pramelreuthia yazzi sp. nov. is slightly smaller than the type species P. haberfelneri, and its synangia contain pollen generally similar in morphology and size to several species of the dispersed pollen taxon Pityosporites, including P. chinleana, P. oldhamensis, and P. devolvens. Pramelreuthia dubielii sp. nov. is much larger than the other two species; its synangia contain pollen similar to the dispersed pollen species Protodiploxypinus americus.     

Nonlinear and correlational sexual selection on 'honest' female ornamentation

Female ornamentation has long been overlooked because of the greater prevalence of elaborate displays in males. However, the circumstances under which females would benefit from honestly signalling their quality are limited. Females are not expected to invest in ornamentation unless the fitness benefits of the ornament exceed those derived from investing the resources directly into offspring. It has been proposed that when females gain direct benefits from mating, females may instead be selected for ornamentation that deceives males about their reproductive state. In the empidid dance flies, males frequently provide nuptial gifts and it is usually only the female that is ornamented. Female traits in empidids, such as abdominal sacs and enlarged pinnate leg scales, have been proposed to 'deceive' males into matings by disguising egg maturity. We quantified sexual selection in the dance fly Rhamphomyia tarsata and found escalating, quadratic selection on pinnate scales and that pinnate scales honestly reflect female fecundity. Mated females had a larger total number and more mature eggs than unmated females, highlighting a potential benefit rather than a cost of male mate choice. We also show correlational selection on female pinnate scales and fecundity. Correlational selection, equivalent investment patterns or increased nutrition from nuptial gifts may all maintain honesty in female ornamentation.