Gingko biloba - its ancestors and allies
Ginkgo biloba is a long-lived, dioecious and deciduous tree up to more than 30 meters high and 10 meters in girth (Figure 1). It bears flabellate leaves with a long petiole and dichotomously branching veins, which grow either in tuft at the terminal end of dwarf shoots or are attached sparsely to the newly-sprung long shoot (Figures 2-3). It has a long fossil record and is well known as having the preeminent claim to be described as a living fossil (Seward, 1911, 1919). Living Ginkgo is called "Baiguo" (white nut), "Yajiao" (duck foot), "Gongsunshu" (grandfather/grandson tree), "Yinxing" or "Icho" (silver apricot) and "maidenhair tree" in China, Japan and other countries. However, the name Ginkgo originates from 1712 when the traveller Kaempfer proposed for this plant. Linnaeus, the founder of the binomial system of nomenclature, adopted this designation adding the species name 'biloba' to denote the bisection of the wedge-shaped lamina of the leaf into two divergent segments (Seward, 1911). According to Tori and Tori (1997), the name Ginkgo was derived from "Ginkyo" which is a Japanese pronounciation of the Chinese characters "Yinxing".
In the modern day flora Ginkgo biloba is the sole representative of a once greatly flourished plant group in geological history – Ginkgoales. For a long time, our knowledge of the evolutionary history of Ginkgo and its allies was based mainly on leaf fossils (Seward, 1911; Florin, 1936; Tralau, 1967, 1968; Harris et al., 1974). Recent studies on fossil reproductive organs revealed that vegetative leaves previously referred to Ginkgo, or ginkgophytes are rather heterogeneous (Zhou, 1991, 1997). Quite a number of so-called ginkgophyte fossils belong to other extinct plant groups than Ginkgoales, such as Czekanowskiales which bear characteristic bivalve capsules containing rows of seeds are markedly distinguished from Ginkgo (Harris, 1951; Krassilov, 1970).
Different hypotheses have been proposed for the origin and relationships of Ginkgoales by palaeobotanists and botanists based on molecular biological as well as comparative morphological approaches (Zimmermann, 1959; Crane, 1985; Doyle and Donoughue, 1986; Meyen, 1987; Archangelsky and Cueneo, 1990; Zhou, 1991; Stewart and Rothwell, 1993; Chase et al., 1993; Rothwell and Serbet, 1994; Haseba, 1997; Burleigh and Mathews, 2004). There is yet no direct fossil evidence and unanimously accepted theory about the origin of ginkgoales, although most believe that they were originated from progymnosperms, related either to pteridosperms and cycads, or to cordaites and conifers (Kenrick and Crane, 1997). Their precise ancestry is therefore uncertain.
The earliest representative of Ginkgoales that exhibits the essential characters of Ginkgo can be traced back to the early Permian. Trichopitys Saporta (Florin, 1949) from the Autunian (Permian) in Lodéve, southern France bears vegetative shoots with spirally arranged, not flattened dichotomously branching leaves and axillary fertile shoots with up to 20 pedicellate ovules on the distal end of lateral branches (Figure 4). Some authors, however, consider Trichopitys to be related to peltaspermalean pteridosperms Dichophyllum and Bairmopteris (Meyen, 1987), or the enigmateic seed plants Polyspermophyllum and Dicranophyllum (Archangelsky and Cueneo, 1990). In the late Permian, flattened and laminated leaves of the Sphenobaiera type occurred, but no petiolate ginkgoalean leaves existed yet.
Ginkgoaleans drastically diverge and radiate in the early Mesozoic. In the late Triassic, almost all known evolutionary lineages (families) were simultaneously present (Figures 5-6). The diversity of both vegetative and reproductive organs reached the highest peak in the geological history respectively (Figure 7). The emergence of a large number of new taxa, the rapid increase in geographical distribution, and the simultaneous accomplishment of major morphological innovations also supports an early Mesozoic, notably late Triassic radiation of ginkgoaleans (Zhou and Wu, 2006).
The representative members of the five lineages so far known in the Mesozoic ginkgoaleans are as follows: Ginkgo (Ginkgoaceae including Grenana Samylina 1991 and possibly Nehvizdyella Kvacek et al. 2005), Karkenia (Karkeniaceae) (Archangelsky, 1965), Toretzia and Umaltolepis (Umaltolepidiaceae) (Stanislavsky, 1973; Krassilov, 1970, 1972), Yimaia (Yimaiaceae) (Zhou and Zhang, 1992) (Figure 8) and Schmeissneria (Schmeissneriaceae) (Kirchner and Van Konijnenburg-van Cittert, 1994). Authentic pollen organs are hitherto only scarcely known (Van Konijnenburg-van Cittert, 1971). Ginkgoalean vegetative organs, especially leaves are abundant in the Mesozoic strata. The leaves are of considerably varied shape and extent of division even within a single species. On the other hand, similar-looking vegetative organs may belong to different mother plants. For instance, Ginkgoites type leaves are known in different genera belonging respectively to three families (Zhou, 1997).
As compared with the late Palaeozoic Trichopitys, all the Mesozoic members have reduced (shortened) shoots (dwarf shoots). Their leaves tend to be laminated, and petiolate (becoming complete), and the deeply divided laminae tend to be fused and webbed. The ovulate organs are generally markedly reduced. Except for those in Karkeniaceae, ovules decrease in number and increase in size, and pedicels become shortened and eventually lost. The general evolutionary trend of ginkgoaleans is reduction of both reproductive and vegetative organs (Zhou, 1991, 1997).
The oldest Ginkgo ovulate organs may be dated back to about 170 Myr in the middle Jurassic of China (Zhou and Zhang, 1989). G. yimaensis (Figures 9-10) is quite different from G. biloba. It has more than one (two to four) mature pedicellate ovules and is associated with deeply dissected leaves. Ovulate organs that bear only one mature sessile ovule directly on the peduncle as normally in the living species are known in the Palaeocene G. adiantoides (Crane et al., 1990) (Figure 12). Recently, new ovulate organs called G. apodes (Figure 11) were found in the lower Cretaceous (about 121 Myr) Jehol biota, northeastern China (Zhou and Zheng, 2003; Zheng and Zhou, 2004) which are essentially of the modern type bearing sessile ovules as in G. biloba, but has more ovules. The finding testifies a roughly 120 Myr morphological stasis of Gingko ovulate organs and provides further evidence for the reduction hypothesis of Ginkgo evolution through heterochrony (peramorphosis) (Figure 12).
Ginkgoaleans were greatly flourished and had a world-wide distribution during the great part of Mesozoic. From the late Cretaceous onward, ginkgoaleans rapidly decreased. In the late Cretaceous and early Tertiary, Ginkgo had a circum-polar distribution, but retreated from North America in the late Miocene (about 10 Myr ago) and became extinct in Europe in Pliocene (about 17 Myr ago) (Wolf, 1987; Kovar-Eder et al., 1994; Samylina, 1967). In East Asia, the latest Ginkgo fossils have been recoded from the late Pliocene and Pleistocene in Japan (Uemura, 1997). In China, there is no record of Ginkgo in sediments younger than Eocene. Whether Ginkgo is a refugee that has existed during the whole Cenozoic there or just an immigrant from Japan to the Yangtze valley quite recently remains unknown.
Contribution by Professor Zhiyan Zhou
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