PHYLOGENY OF COCCOLITHOPHORIDS AND THE EVOLUTION OF CALCIFICATION
Jeremy R. Young (1), Chantal Billard(2), Paul Bown(3), Lluisa Cros(4),
Sean Davis(5), Markus Geisen(1), Masanobu Kawachi(6), Steve Mann(5),
Linda Medlin(7), Ian Probert(2), Alberto Saez(7)
1 Palaeontology Department, The Natural History Museum London, SW7 5BD, UK
2 Laboratoire de Biologie et Biotechnologies Marines, Universite de Caen Basse Normandie, Caen, France
3 University College London, Gower St., London WC1E 2BT, UK
4 Institut de Ciencias del Mar, CSIC, Passeig J. de Borbo, Barcelona, Spain
5 School of Chemistry, University of Bristol, Bristol, BS8 1TS, UK
6 Environmental Biology Division, National Institute for Environmental Studies, Tsukuba, Japan
7 Dept. of Plankton Biology, Alfred Wegener Inst. f. Polar & Meeresforschung, Bremerhaven, Germany
Traditionally, knowledge of coccolithophorid phylogeny has been entirely dependant on stratophenetic data and because this is by no means complete there has been considerable uncertainty about interrelated fundamental questions, such as: the relationship of holococcolithophorids to heterococcolithophorids; the relationship of coccolithophorids to other haptophytes; whether coccolithophorids constitute a monophyletic group; and whether calcification has evolved repeatedly or only once.
Over the past decade and especially the last few years new data has become available from a range of sources enabling a new synthesis to be proposed. Key lines of information include:
Biomineralisation studies - (Young et al 1992) demonstrated that many heterococcoliths are characterised by a highly distinctive biomineralisation mode commencing with nucleation of alternating sub-vertical and sub-radial calcite crystals and hypothesised that this was a conserved mode indicating a common phylogenetic origin for all heterococcolithophorids. this hypothesis has been strongly supported by subsequent research (e.g. Young et al. 1999, Marsh et al. 199). Moreover Young et al. (1999) argued that the radically different holococcolith biomineralisation mode was equally distinctive and implied a common phylogenetic origin for all holococcolithophorids.
Molecular genetics - molecular phylogenies of haptophytes are rapidly being developed (Fujiwara et al. 1994, Inouye 1997, Medlin et al.1997, Edvardsen et al. 2000). These strongly indicate: (1) that coccolithophorids form a discrete clade within the haptophytes (including a few species who have secondarily lost the ability to calcify). (2) that the major diversification of the class Prymnesiophyceae occurred slightly before the diversification of the coccolithophorids (Medlin et al. 1997), which is known from stratophenetic data to have occurred in the Early Jurassic, ca 200 Ma, (Bown 1987). (3) That the origin of the Haptophyta and the subsequent divergence of the classes Pavolovophyceae and Prymnesiophyceae occurred much earlier, probably in the Early Palaeozoic (ca 850Ma, 420Ma, respectively Medlin et al. 1997).
Life-cycle studies - it remains true that life-cycles have only been documented in a few haptophytes and very few coccolithophores. Synthesis of the data by Billard (1994) lead to the prediction that haplo-diplontic life-cycles were common to haptophytes and that distinct periplast types were characteristic of the phases In particular it was predicted that heterococcoliths might consistently occur on diploid phases and holococcoliths on haploid phases. This has been supported by flow cytometry studies of Emiliania huxleyi (Green et al. 1996) and most recently Coccolithus pelagicus (Probert et al. unpubl.), (see also Edvardsen et al. 1996 for documentation of the haplo-diplontic life-cycles in a non-calcifying haptophyte). The data on Coccolithus pelagicus is critical because it provides the first direct confirmation that holococcoliths are indeed produced by haploid phase.
Combination coccospheres - the life cycle data has been greatly supplemented by documentation of combination coccospheres including holococcoliths and heterococcoliths (Thomsen et al. 1991, Kleijne 1992, Alcober & Jordan 1997, Young et al. 1998, Cros et al, in press, Cortes in press, Sprengel et al. in press, Cros et al. this vol., Geisen et al. this vol.). This work strongly supports the hypothesis that holococcoliths and heterococcoliths are alternate life-cycle phases and moreover indicates that in some species nannoliths substitute for holococcoliths.
Synthesis - From this evidence it appears likely that that the major diversification of haptophytes occurred in the Early Mesozoic and that a key event within this was the acquisition of calcification. We hypothesise this was a unique event and that calcification was subsequently passed from the haploid to the diploid phase (or vice versa). This implies that acquisition of calcification is a more significant evolutionary step than has previously been assumed. In addition the differential expression of calcification in two phases of the life cycle of a single organism provides an unique opportunity for studying the functional genomics and biochemistry of biomineralisation.
REFERENCES
Alcober, J., Jordan, R.W., 1997. An interesting association between Neosphaera coccolithomorpha and Ceratolithus cristatus (Haptophyta). European Journal of Phycology, 32, 91-93.
Billard, C., 1994. Life cycles. In: Green, J.C., Leadbeater , B.S.C., (Eds.), The Haptophyte Algae. Systematics Association Special Volume 51, 167-186.
Bown P. R. 1987. Early Mesozoic calcareous nannofossils. Special Papers in Palaeontology, 38, 1-118.
Cortes, M.Y., (in press) Further evidence for the heterococcolith-holococcolith combination Calcidiscus leptoporus - Crystallolithus rigidus. Marine Micropaleontology, 39.
Cros L., Kleijne A., Zeltner A., Billard C., Young J. R.. (in press). New examples of holococcolith-heterococcolith combination coccospheres and their implications for coccolithophorid biology. Marine Micropaleontology, (INA7 Proceedings Special Issue), 39.
Cros L., Kleijne A. & Young J.R. (this vol.) Coccolithophorid diversity in the genus Polycrater and possible relations with other genera. Abstracts INA8, Bremen 2000
Edvardsen B, Eikrem W., Vaulot D. & Paasche E. 1996. Comparison between the authentic and alternate Chrysochromulina polylepis: morphology, growth, taxonomy and ploidy level. In: Harmful and toxic algal blooms (Eds. Yasumoto T., Oshima Y & Fukuyo Y.), IOC UNESCO, 231-234.
Edvardsen B, Eikrem W., Green J.C., Andersen R.A., Moon-van fer Staay S., & Medlin L. K., (2000) Phylogenetic reconstructions of the Haptophyta inferred from 18S ribosomal DNA sequences and available morphological data. Phycologia, 39, 19-35.
Fujiwara S., Sawada M., Someya J., Minaka N., Kawachi M. & Inouye I. 1994. Molecular phylogenetic analysis of rbcL in the Prymnesiophyta. Journal of Phycology, 30, 863-871.
Geisen, M., Cros, L., Probert, I., &. Young J.R. (this vol.): Life-cycle associations involving pairs of holococcolithophorid species - complex life cycles or cryptic speciation? Abstracts INA8, Bremen 2000.
Green, J.C., Course, P.A., Tarran, G.A., 1996. The life-cycle of Emiliania huxleyi: A brief review and a study of relative ploidy levels analysed by flow cytometry. Journal of Marine Systems, 9, 33-44.
Inouye I. 1997. Systematics of Haptophyte algae in Asia-Pacific waters. Algae (The Korean Journal of Phycology), 12, 247-261.
Kleijne, A., 1991. Holococcolithophorids from the Indian Ocean, Red Sea, Mediterranean Sea and North Atlantic Ocean. Marine Micropaleontology 17, 1-76.
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Sprengel C. & Young J. R. (in press) First direct documentation of associations of Ceratolithus cristatus ceratoliths, hoop-coccoliths and "Neosphaera coccolithomorpha" planoliths. Marine Micropalaeontology, (INA7 Proceedings Special Issue), 39.
Thomsen, H. A., ¯stergaard, J. B., Hansen, L. E., 1991. Heteromorphic life histories in arctic coccolithophorids (Prymnesiophyceae). Journal of Phycology 27, 634-642.
Young J.R., Didymus J.M., Bown P.R., Prins B., Mann S., 1992: Crystal assembly and phylogenetic evolution in heterococcoliths. Nature, 356, 516-518.
Young, J.R., Jordan, R.W., Cros, L., 1998. Notes on nannoplankton systematics and life-cycles . Ceratolithus cristatus, Neosphaera coccolithomorpha and Umbilicosphaera sibogae. Journal of Nannoplankton Research, 20 (2), 89-99.
Young J. R., Davis, S. A., Bown P. R. & Mann S. (1999) Coccolith ultrastructure and biomineralisation. Journal of Structural Biology., 126, 195-215.
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