Angiosperm Origins and Evolution
|
by: Sebastian Molnar Abstract The origin and evolution of angiosperms has been under considerable dispute. The present study is a review of three questions in particular: 1) from what basal lineage did the angiosperms originate?, 2) when did the angiosperms originate?, and 3) where did angiosperms originate? Fossil evidence is discussed with respect to the timing and to the possible mechanisms (or causes) of angiosperm evolution. The ‘center of origin” theory is discussed in relation to phylogenetic series of extant taxa, and to continental drift during the Jurassic through to the Cretaceous. Introduction Angiosperms are the most diverse group of the plant kingdom, comprising of about 250,000 species in 350 families (Kenrick, 1999). Not all families are equivalent in diversity -- certain families (e.g. Asteraceae, Orchidaceae, Poaceae) have much larger numbers of species than others (Stebbins, 1981). ‘Key innovations’ have been explored, however, there is no consistency between groups that may lead to a general explanation for the evolution of angiosperm diversity (Stebbins, 1981). Takhtajan (1976) suggested that neoteny -- a delay in development causing juvenile forms of the body or of particular organs to be expressed in the adult stage -- played a significant role in angiosperm evolution. Reproductive structures (Stebbins, 1981; Takhtajan, 1976) and insect pollination (Burger, 1981) are also considered to be important factors involved in angiosperm evolution. A fundamental problem that must be dealt with is whether the angiosperms are monophyletic or polyphyletic. As a group, the angiosperms have typically been viewed as being monophyletic (i.e. a group consisting of all descendents derived from a single ancestor) (e.g. Doyle and Donoghue, 1993; Takhtajan, 1969). Hughes (1994) has argued that, unless proven otherwise, the angiosperms should be assumed to be polyphyletic (i.e. a group that does not have a common ancestor). In this case, the very use of the term ‘angiosperm’ would become taxonomically meaningless, as it would be used to describe an ‘unnatural’ group. Recently, however, phlylogenetic analyses using nuclear, mitochondrial, and plastid gene sequences have aided in clarifying relationships between the various angiosperm families (Bremmer, 2000; Qiu et al., 1999; Soltis et al., 1999). The monocots and eudicots are each supported as being monophyletic (reviewed in Crane et al., 1995; Kenrick, 1999). The angiosperms as a whole were found to be monophyletic to the exclusion of the gymnosperms (Qiu et al., 1999; Soltis et al., 1999). Several characters, including the closed carpel, the eight-celled female gametophyte, and double-fertilization, are considered defining features of angiosperms (Dilcher, 2000; Stebbins, 1976) and support the monophyletic grouping (Crane et al., 1995). Although molecular data can been used to resolve familial relationships of extant taxa, fossil evidence is required to know what existed in the past (Hughes, 1994, p 22). A limitation in the fossil record is the selective preservation of plant tissues. Delicate structures, such as the flower, may not be preserved very well or at all. Also, it has been argued that early angiosperms may have evolved in montane habitats (e.g. upland theory), far away from depositional environments necessary for fossilization (Axelrod, 1952). In opposition to this view, Truswell et al. (1987) point out that pollen from upland habitats should be represented in the lowland samples. In any case, the fossil record for angiosperms is likely to be incomplete in certain areas. The evolution of the angiosperms has remained an engima since at least the time of Darwin (Axelrod, 1952). Three major issues currently surround the origin and evolution of the angiosperms: 1) the time of their origin, 2) the geographic location of their origin, and 3) the ancestral plant group from which they evolved. The present study is a brief review of the literature on these issues. The First Angiosperms The angiosperms underwent a major diversification during the Mid-Cretaceous. There is an abundance of angiosperm fossils that have been found at this stratigraphic level, which has been associated with a decrease in gymnosperm abundance (Crane and Lidgard, 1989; Lidgard and Crane, 1990; but see Wing et al., 1993). The time of angiosperm origin, however, remains unclear and the fossil evidence for the earliest angiosperms is still debated (Crane, 1993; Crane et al., 1995; Scott et al., 1960). A closed carpel is considered to be the major distinguishing character for angiosperms, although showy flowers, fruits, nuts, and seeds may also be used in identification (Dilcher, 2000). A number of fossils that were thought to have been angiosperms of pre-Cretaceous origin, were later rejected as such on the basis of ambiguous classification (Scott et al., 1960). Recently, however, a fossil from the Yixian Formation in China (Archaefructus liaoningensis) exhibiting the presence of closed carpels was found, revealing that angiosperms were present in the Late Jurassic (Sun et al., 1998). Pollen and pollen-bearing organs were not found in the specimen. Whether Archaefructus flowers were unisexual or bisexual, remains unknown. The majority of angiosperms are hermaphrodites (Dellaporta and Calderon-Urrea, 1993), and this has implications in identifying ancestral forms of the angiosperms. Takhtajan (1969) has argued for the existence of an ancient gymnosperm with bisexual strobili as the ancestral angiosperm, however, the angiosperm ancestor potentially could have been either unisexual or bisexual. Thus, it is still uncertain what basal lineage gave rise to the angiosperms. The Coevolution of Plants and Insects The coevolution between insects and plants (i.e. insect pollination) was probably an influential process in the angiosperm origin and divergence (Dilcher, 2000; Labandeira, 1998; Labandeira et al., 1994; Takhtajan, 1969, pp. 132-133). Thus, a complete understanding of angiosperm evolution must include fossil evidence from both plants and insects. Stebbins (1981) argued that insect pollinators probably did not play a significant role early on in angiosperm evolution, although they were likely to have had a selective role for bisexual flowers later on. This was based on the absence of efficient or reliable pollinators in the fossil record of the Early Cretaceous. Instead, he argues that flexibility in seed production, dispersal, and seedling establishment was of primary importance in angiosperm diversification. Stebbins’ argument may still be tenable, however, fossils of insect pollinators (Brachycera flies) have been recently found in Late Jurassic rocks (Ren, 1998). Extant Brachycera are known to consist of a wide variety of pollinators (Ren, 1998). The initial pollinators were likely to have been generalists derived from a group with a pollinivorous habit (Labandeira, 1998). Insect pollinators of the Cretaceous and Tertiary were more diverse and specialized, and included the Coleoptera, Lepidoptera, and Hymenoptera (Ren, 1998). Labandeira (1998) indicated that insect pollination likely began with gymnospermous taxa in the Jurassic, while ‘fine-tuning’ of the mechanism by angiosperms occurred later. The presence of Brachycera flies in the Jurassic, coupled with Archaefructus, suggests that insect pollination may have occurred early in angiosperm evolution. The Angiosperm Center of Origin The geographic origin of the angiosperms has been under considerable debate. In the late nineteenth and early twentieth centuries, the dominant view had been that the angiosperms originated high in the northern latitudes and even in the polar-regions (reviewed in Takhtajan, 1969, p. 137). This view has been disputed for a more tropical “center of origin” (between 45 N to 45 S) from which they migrated towards the polar regions (Axelrod, 1959). The fossil evidence suggests that angiosperms did not establish in the Arctic until the Late Cretaceous, since angiosperm fossils from the Early Cretaceous are found only at low latitudes (Takhtajan, 1969, p. 139). On the other hand, the Arctic may have been an important site for some level of floral evolution in the Late Cretaceous (Hickey et al., 1983). In general, angiosperms began to migrate toward the poles late in the Early Cretaceous, eventually replacing the relict Jurassic-flora at higher latitudes towards the end of the Mesozoic (Axelrod, 1959). Although the precise location of the angiosperm center of origin is uncertain, it is predicted to be in south-eastern Asia (Takhtajan, 1969; 1987). Takhtajan (1969) has suggested that the ‘cradle of the angiosperms’ occurs somewhere between Assam and Fiji due to the high abundance of ‘primitive’ angiosperm families (e.g. Magnoliaceae and Winteraceae) found in that region of the Pacific basin. A serious flaw in the south-east Asian center of origin theory, acknowledged by Takhtajan himself (1969, p. 156), is the lack of fossil evidence. Hughes (1994, p. 22) has argued directly for the primacy of the fossil record to reveal events of the past. In contrast, determination of the center of origin, Takhtajan (1987) argues, must come primarily from distributions of extant taxa in a phylogenetic series, whereas the paleobotanical evidence can only reveal migration patterns (e.g. the equator-to-poles direction), but not the center from which the angiosperms initially spread. He considers south-east Asia (including Burma, Thailand, Indo-China, and Malaysia) to be the most likely region where angiosperms originated, since that is where the highest abundance of primitive angiosperms occur at present. Current distributions may not necessarily be similar to those of the past -- they may simply reflect ‘centers of survival’ rather than ‘centers of origin’ (Takhtajan, 1969, p. 158). Descendants of the first angiosperms may have dispersed far from their point of origin (Takhtajan, 1987). In a phylogenetic series, “the most advanced members...are further from the centre of origin” (Takhtajan, 1987, p 28). South America has few species from the Magnoliales (and they appear to be more advanced than those in southeast Asia), while Africa has none (Takhtajan, 1969). As such, these regions, along with western Gondwanaland, were excluded as possible sites harboring the “cradle of the angiosperms”. As described in extensive detail by Vakhrameev (1991), the gymnosperms (e.g. conifers, ginkgos, cycads) dominated in the Siberian-Canadian region during the Early Cretaceous. In Canada, angiosperms do not appear until the Mid-Cretaceous (Axelrod, 1952). Angiosperms also appeared to have invaded Northeast Asia gradually from the south during the Early Cretaceous (Axelrod, 1959). Audley-Charles (1987) has discussed the movement of Gondwanan continental fragments or “Noah’s arks” (e.g. Burma, Thailand, Malaya, Sumatra), which could have enabled the dispersal of angiosperms northward to mainland Asia. Eastern Gondwanaland, as it may have appeared in the Late Carboniferous, is shown in figure-1. Areas that are currently part of south-eastern Asia were connected to each other and to Australia-New Guinea. In the Late Jurassic, south-east Asian continental fragments have separated from Gondwanaland (figure-2). By this time, Indo-China, North Tibet, and Iran had long since separated and moved towards mainland Asia. Dispersal between mainland Asia and Australia-New Guinea is unlikely, as the distance is considered to be too far apart (Audley-Charles, 1987). In the Early Cretaceous, dispersal between mainland Asia and Australia-New Guinea is still unlikely (figure-3) due to flooding (Audley-Charles, 1987). There was a rise in sea level during the Cretaceous, and this would have directly influenced the amount of land available for colonization. However, land on south-east Asian continental fragments (e.g. Burma, Thailand, Sumatra, Malaya) was largely exposed above sea level throughout the Jurassic and the Cretaceous (Audley-Charles, 1987). Dispersal to mainland Asia became increasingly likely as the continental fragments moved closer. By the Late Cretaceous (figure-4), dispersal between mainland Asia and Australia-New Guinea is possible.
Truswell et al. (1987) considered the potential routes of angiosperm invasion into Australia. The earliest angiosperms appeared in Australia about 10 Ma after their appearance in other parts of the world (Truswell et al., 1987). Thus, the continental fragments which separated from Australia in the late Jurassic did not initially carry angiosperms, as the concept of “Noah’s arks” would suggest (Truswell et al., 1987). This does not exclude the possibility that angiosperms arose on such continental fragments after rafting from Gondwanaland. The continental fragments could have acted as ‘stepping stones’ allowing the exchange of angiosperms between Australia and south-east Asia (Truswell et al., 1987). Taking into consideration the timing of continental fragments rafted from Gondwanaland, and assuming that the center of origin occurred in south-east Asia, angiosperms must have originated no earlier than the Late Jurassic. The finding of Archaefructus in the Yixian formation suggests that angiosperms had to have colonized mainland Asia by the Late Jurassic, and that they had probably evolved for some time before this period. Takhtajan (1987) propounds an idea put forth by Carlquist -- that the angiosperms originated on an archipelago. An archipelago may offer wider niche opportunities than a single island, allowing for rapid diversification (Takhtajan, 1987, p. 30). A combination of insect pollination and flexibility in dispersal capabilities probably facilitated the spread and diversification of angiosperms on the major landmasses before and during the Mid-Cretaceous. References: 1. Audley-Charles, M.G. (1987) Dispersal of Gondwanaland: relevance to evolution of the angiosperms. pp. 5-25 in Whitmore, T.C. Biogeographical Evolution of the Malay Archipelago. Clarendon Press, Oxford. 2. Axelrod, A.J. (1952) A theory of angiosperm evolution. Evolution. 6: 29-60 3. Axelrod, D.J. (1959) Poleward migration of early angiosperm flora. Science. 130: 203-207 4. Burger, W.C. (1981) Why are there so many kinds of flowering plants? Bioscience. 31: 572, 577-581 5. Bremmer, K. (2000) Early Cretaceous lineages of monocot flowering plants. Proceedings of the National Academy of Science USA. 97: 4707-4711 6. Crane, P.R. (1993) Time for the angiosperms. Nature. 336: 631-632 7. Crane, P.R. and Lidgard, S. (1989) Angiosperm diversification and paleolatitudinal gradients in Cretaceous floristic diversity. Science. 246: 675-678 8. Crane, P.R., Friis, E.M., and Pederson, K.R. (1995) The origin and early diversification of angiosperms. Nature. 374: 27-33. 9. Dellaporta, S.L. and Calderon-Urrea, A. (1993) Sex determination in flowering plants. The Plant Cell. 5: 1241-1251 10. Dilcher, D. (2000) Toward a new synthesis: major evolutionary trends in the angiosperm fossil record. Proceedings of the National Academy of Science USA. 97: 7030-7036 12. Doyle, J.A. and Donoghue, M.J. (1993) Phylogenies and angiosperm diversification. Paleobiology. 19: 141-167 13. Hickey, L.J., West, R.M., Dawson, M.R., and Choi, D.K. (1983) Arctic terrestrial biota: paleomagnetic evidence of age disparity with mid-northern latitudes during the Late Cretaceous and Early Tertiary. Science: 1153-1156 14. Hughes, N.F. (1976) Cretaceous paleobotanical problems. pp. 11-22 in Beck, C.B. Origin and Early Evolution of Angiosperms. Columbia University Press, New York. 15. Hughes, N.F. (1994) The Enigma of Angiosperm Origins. Cambridge University Press, Cambridge. 16. Kenrick, P. (1999) The family tree flowers. Nature. 402: 358-359 17. Labandeira, C.C. (1998) How old is the flower and the fly? Science. 280: 57-59 18. Labandeira, C.C., Dilcher, D.L., Davis, D.R., and Wagner, D.L. (1994) Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Science USA. 91: 12278-12282. 19. Lidgard, S. and Crane, P.R. (1990) Angiosperm diversification and Cretaceous floristic trends: a comparison of palynofloras and leaf macrofloras. Paleobiology. 16: 77-93 20. Qiu, Y.-L., Lee, J., Bernasconi-Quadroni, F., Soltis, D.E., Soltis, P.S., Zanis, M., Zimmer, E.A., Chen, Z., Savolainen, V., and Chase, M.W. (1999) The earliest angiosperms: evidence from mitochondrial, plastid, and nuclear genomes. Nature. 402: 404-407 21. Ren, D. (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science. 280: 85-88 22. Scott, R.A., Barghoorn, E.S., and Leopold, E.B. (1960) How old are the angiosperms? American Journal of Science. 258: 284-299 23. Soltis, P.S., Soltis, D.E., and Chase, M.W. (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature. 402: 402-404 24. Stebbins, G.L. (1976) Seeds, seedlings, and origin of angiosperms. pp. 300-311 in Beck, C.B. Origin and Early Evolution of Angiosperms. Columbia University Press, New York. 25. Stebbins, G.L. (1981) Why are there so many species of flowering plants? Bioscience. 31: 573-577 26. Sun, G., Dilcher, D.L., Zheng, S., and Zhou, Z. (1998) In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science. 282: 1692-1695 27. Takhtajan, A. (1969) Flowering Plants: Origin and Dispersal. Oliver and Boyd, Edinburgh. 28. Takhtajan, A. (1976) Neoteny and the origin of flowering plants. pp. 207-219 in Beck, C.B. Origin and Early Evolution of Angiosperms. Columbia University Press, New York. 29. Takhtajan, A. (1987) Flowering plant origin and dispersal: the cradle of the angiosperms revisited. pp. 26-31 in Whitmore, T.C. Biogeographical Evolution of the Malay Archipelago. Clarendon Press, Oxford. 30. Truswell, E.M., Kershaw, A.P., and Sluiter, I.R. (1987) The Australian-south-east Asian connection: evidence from the paleobotanical record. pp 32-49 in Whitmore, T.C. Biogeographical Evolution of the Malay Archipelago. Clarendon Press, Oxford. 31. Wing, S.L., Hickey, L.J., and Swisher, C.C. (1993) Implications of an exceptional fossil flora for Late Cretaceous vegetation. Nature. 363: 342-344 32. Vakhrameev, V.A. (1991) Jurassic and Cretaceous floras and climates of the Earth. Cambridge University Press, Cambridge.
|
Get your own Free Home Page