The history of land plants involves three phases in the development of the male gametophyte•. The prothallus is the growth form of the gametophyte generation, which is linked to a wet habitat. The most famous example is bracken fern, in which nectaries are found in the axils of the stem and petiole (Potonié, 1891).
The natural result of this process is the fertilization of the eggs, which are transferred to the megagametophyte. Of the five, all conifers and ginkgo are obligately wind-pollinated, probably primarily (Proctor et al., 1996). Associated data on disseminated coprolites come from the Calhoun coal in the Illinois Basin, although other occurrences are known.
Moths and butterflies are the most phytophagous of all the four major holometabolan insects. Apis mellifera, one of the most specialized pollen consumers, may be informative about the origin of primitive palynivores during the late period. There is evidence of "osmotic shock", which is caused by the transfer of pollen from the crop rich in nectar or honey, characterized by high osmolarity, to the much lower osmolarity of the ventricular region of the foregut, resulting in some pollen wall. fragmentation (Kroon et al., 1974).
Some of the best-documented pollinators are springtails (CoUembola) based on gut-content examinations (Marshall, 1978; Waldorf, 1981), but are poor pollinators.
POLLINATION AS A MUTUALISM
After mixing with nectar and enzymes secreted by bee salivary glands, pollen protoplasts can flow from their pollen grains without disruption of the pollen wall (B arker and Lehner, 1972). Although most of the pollen grains examined in bees remain mechanically intact and even undisturbed, each grain is enzymatically degraded causing its protoplasts to emerge through germination pores or other relatively thin sites (Whitcomb, 1929; (Peng et al., 1985). The mecopteran cavity is an extension of the skull and mouthparts, and scorpions have been observed feeding on nectar deep in tubular flowers (Pigott, 1958).
All three are examples of the role of complexity in the development of mutual benefit. They are pollinated by several genera of the lepidopteran family, Prodoxidae (joicca moths), and are a textbook example of mutualism in which the adults are highly host-specific, beneficial pollinators, while their larvae are seed predators of the same Yucca species. (Figure 3). The pollination cycle of yucca involves the extraction of pollen, followed by flight from the flower, the search for another inflorescence, which follows, the insertion of an ovule into a suitably mature ovule, followed by the ascent to the stigma of the same. a flower on which previously collected pollen is deposited on the surface.
Based on the mtDNA phylogeny of Prodoxidae and Yucca, Pellmyr and Leebens-Mack (1999) were able to trace the links between these two coevolutionary taxa with Ma (Fig. 3). Earlier examples were cited from Boganiidae on Zamiaceae and Chrysomelidae on Araucariaceae (Fig. 2), although there are many taxa from other basal families Chrysomelidae (Aulacoscelinae) and Curculionoidea (Belidae-Pachyurinae, Nemonychidae, AUocoryninae) that occur on conifer and cycad taxa. (Forster et al., 1994; Morrone, 1997; Farrell, 1998). Either male or female of the species can serve as a larval and later pupal feeding site, with the subsequent emergence of the adult pupa evidenced by an exit hole, usually at the base of the sporophyll.
For male cones, it is typically a pupated female beetle that emerges from its pupal chamber in the cone tissue, moves through the basal area of the cone and collects pollen on her hairy integument as she brushes along the pollen sacs before a flight to other male cones for oviposition or feeding. This configuration of a closed space between the ovoid micropyles and the cycad megasporophyll bases is similar in position to that found in the closed bisporangiate cones of the Bennettitales, especially the family Cycadeoidaceae (Crepet, 1974; Donaldson, 1992). The phylogeny of the moth superfamily Incurvarioidea is shown, based on mitochondrial DNA sequence data, with neighbor-joining and maximum likelihood trees with identical topology (see Pellmyr and Leebens-Mack [1999] for details).
From the base of the oval receptacle emerged large footed microsporophylls, which extended outward from the median axis of the cone but turned back toward the receptacle, each constricting its base and revealing numerous pollen-filled microsporangia attached to the lateral tips . This interpretation is reinforced by evidence of insect-damaged tissue adjacent to the normal space between the micropylar tips of the eggs and adjacent microsporophyll parenchymal tissue, indicating beetle pollination (Delevoryas, 1968; Crepet, 1974). Angiosperms and Tanglevein Flies.•One of the most striking associations, with implications for the fossil record of preangiosperm pollination, is the relationship between long-tongued flies (Nemestrinidae) and their host plants in South Africa, members of the Iridaceae, Geraniaceae , and Orchidaceae.
EVOLUTIONARY ASSEMBLAGES
The proboscis of these fossil flies, when present, are typically elongated and designed for nectar-sucking; in addition, the recurved marginal veins at the tip of the wing suggest hovering flight, also evidence of nectarivory. Notably, these mid-Mesozoic forms occur in deposits that either predate the appearance of angiosperms or, if contemporaneous with angiosperms (Sun et al., 1998), were left-over holdovers from the Late Jurassic (Luo, 1999) that occurs in deposits that lack a deep neck. angiosperm flowers (Labandeira 1998c). The temporal occurrence of these brachyceran flies most likely indicates pollination of seedlings by a pollination drop mechanism (Labandeira, 1998c).
Many of the populations of these scattered coprolites consist of nearly monotaxic contents, with occasional "foreign" grains of other palynomorphs and incorporation of leaves or other reproductive organ tissues such as sporangial rings, microsporophyll fragments, and trichomes. Insectivores responsible for the consumption of Middle and Late Pennsylvanian palynomorphs are poorly known due to the dispersed nature of the coprolites. The presence of probable aromatic glands near the reproductive organs of certain Permian cycads and seed hairs (Halle, 1929; Mamay, 1976) and the presence of a specialized tissue that probably decomposed and produced fluids that collected in the pollen chamber under the micropyle of the conifer Fergliocladus, also provides support for presence.
In contrast, almost all of the higher-level insect lineages and many of the lower-level insect lineages that have survived to the present indicate a change of host between palynivores, nectarivores, or pollinators, rather than a parallel demise with ancient host plants. These surviving insect taxa include nemestrinid, tabanid and apiocerid flies, chrysomeloid and curculionoid beetles and xyelid sawflies (Krassilov and Rasnitsyn, 1983; Ren, 1998; FarreU, 1998), although an exception is a proflangiopsid grasshopper with cheirolepidaceous Classopollis pollen in his intestines. (Krassilov et al., 1997a, 1997b). Although there are only four extant lineages of non-angiosperm seed plants today, the diversity of pollination strategies based on fossil evidence alone was undoubtedly much greater than extant descendants would suggest (Harris, 1973; Pederson et al., 1993).
The importance of these major plant and insect interactions has been profound over the past 130 million years, if at all. This expansion was initiated during the radiation of the earliest angiosperm clades, including Amborellaceae, Winteraceae, and Chloranthaceae•. All early known Assemblage 4 associations documented from the mid-Cretaceous to the K/T boundary are still extant at.
This review is not exhaustive for reasons of space, but includes most of the prominent studies. Crepet and Nixon, 1998; see also OUerton, 1996), showing persistence in the face of large angiosperm host turnover (Johnson et al., 1989) and the extinction of insect herbivores (Labandeira et al., 1999). Many of today's highly specialized, largely fiduciary mutualists, including yuccas and yucca moths, complex orchid pollination variations, and others probably originated during the Early Cenozoic (Fig. 3; Taylor and Crepet, 1987; Pellmyr and Leebens -Mack, 1999), although they are in the minority (Waser et al., 1996).
CONCLUSIONS
ACKNOWLEDGEMENTS
Morphology and reproductive biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the Late Triassic. A new gnetophyte from the Late Camian (Late Triassic) of Texas and its bearing on the origin of the angiosperm carpel and stamen, p.32-67. Time in the evolution of derived floral characters•Upper Cretaceous (Turonian) taxa with tricolpate and tricolpate pollen.
Fossil Clusiaceae from the Late Cretaceous (Turonian) of New Jersey and implications regarding bee pollination. New genus of Boganiidae (Coleopteran) from Australia, with observations on gland apertures, breadfruit associations and geographical distribution in the family. Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species.
Some species of the genera Melanostoma, Platycheirus and Pyrophaena (Diptera, Syrphidae) and their relationship to flowers. The feeding of grasshoppers (Orthoptera, Tettigonoidea) on the pollen of flowers and their possible significance for the origin of entomophilia in plants. Scanning electron microscope observations of pollen food bolus in the digestive tract of honey bees {Apis mellifera L.) Canadian Journal of Zoology.
Pollen in the gut of Permian insects: first evidence of pollinivory and its evolutionary significance. The phylogenetic system of tracheats (mandibulata): on the interrelationships of "Myriapoda" and Insecta, phylogenetic ages and primary ecological niches. Osmotic shock as a prerequisite for pollen digestion in the digestive tract of the worker bee.
New Carboniferous Diplura, Monura, Thysanura, the six-legged ground plan, and the role of thoracic side lobes in the origin of wings (Insecta).
PALEONTOLOGICAL SOCIETY PAPERS, V 6, 2000
A revision of the nemestrinid flies (Diptera, Nemestrinidae) described by Rohdendorf, and a description of new taxa of the Nemestrinidae from the Upper Jurassic of Kazakhstan. Morphological specializations in Central European bees for the ingestion of pollen from flowers with anthers hidden in narrow corolla tubes (Hymenoptera: Apoidea). Systematic position of the genus Rocalia (Hymenoptera Tenthredinidae) that feeds on fern spores, with description of a new species from Japan.
Forty million years of mutualism: Evidence for the Eocene origin of the yucca-yucca moth association. Mechanics of pollen digestion by the adult bee and the relation of undigested portions to bee dysentery. Initial observations of reproductive behavior and an insect polluting agent of Bowenia serrulata (W. Bull) Chamberlain.
