The evolution of dinoflagellates

The evolution of dinoflagellates1 J. P. BUJAKAND G. L. WILLIAMS

Can. J. Bot. Downloaded from www.nrcresearchpress.com by 199.201.121.12 on 06/04/13 For personal use only.

Atlantic Geoscience Centre, Geological Survey of Canada, Bedford Institute of Oceanography, Dartmouth, N.S., Canada B2Y 4A2 Received December 16, 1980

BUJAK,J. P., and G. L. WILLIAMS. 1981. The evolution of dinoflagellates. Can. J. Bot. 59: 2077-2087. Recent work on modern dinoflagellates indicates that these organisms occupy a critical position in the evolution of life, being intermediate between prokaryotes and eukaryotes. It further suggests that dinoflagellates acquired chloroplasts through symbiosis with ingested autotrophic organisms. Two models have been proposed to explain the development of the cellulosic theca in the Dinophyceae. The first, the plate increase model, is based primarily on observations of living algae, while the second, the plate reduction model, relies mainly on paleontological data. However, neither satisfactorily reconciles both lines of evidence and so the plate fragmentation model is proposed. This postulates that dinoflagellates with two anterior flagella and a wall consisting of two large valves were successful through much of the Paleozoic. A major evolutionary breakthrough occurred in the Triassic with the development of a transverse-longitudinal flagellar arrangement and change in swimming direction. Associated with these modifications was a fragmentation of the valves into numerous polygonal plates. Subsequent evolution emphasized the influence of the two flagellar furrows over the number and arrangement of thecal plates. This led to a decrease in number and stabilization of the thecal plates as seen in modem dinoflagellates.

Dinoflagellates are unicellular microorganisms with a free-swimming biflagellate stage in their life cycle, and are characterized by the presence of distinctive pigments and nuclear structure. They are one of the most important groups of phytoplankton. As such, they are a critical part of the aquatic food chain and help maintain the earth's atmospheric oxygen supply. Dinoflagellates are also the notorious cause of red tides and paralytic shellfish poisoning, resulting from toxins produced by several species. Other dinoflagellates produce luminescence in the sea and the remains of some are a major source of liquid hydrocarbons. Dinoflagellates have a variety of life styles (Fig. 1). Most are planktonic, living in the surface waters of seas and lakes, but a few are sand dwellers and some are symbionts or parasites. The majority are autotrophic. The remainder are heterotrophic and include both holozoic and saprophytic forms. The life cycle of dinoflagellates is complex and has several stages. All species have a biflagellate motile stage which is usually dominant but lasts for only a few minutes in some. It was originally thought that dinoflagellates only propagated asexually, but sexual reproduction has now been observed in several species (Pfiester 1975,1976,1977; Pfiester and Skvarla 1979; Tuttle and Loeblich 1974; von Stosch 1965,1972,1973;Zingmark 1970). Ten percent or more of living species form cysts and Dale (1976) has suggested that the majority of these are hypnozygotes. The cysts usually sink to the bottom

h his paper was presented in a symposium entitled Landmark Events in the Evolution of Plants, co-sponsored by the Canadian Botanical Association and the Canadian Association of Palynologists at Carleton University on June 21, 1979.

where they can remain dormant for several years and may be inadvertently canied to other areas, causing red tide outbreaks in previously unaffected regions (Dale 1976). The motile dinoflagellate stage is quickly destroyed after death by bacterial action, but the cyst is composed of resistant organic material. This is similar in composition to the walls of spores and pollen and is often fossilized. Fossils thus provide an incomplete record of dinoflagellate development since only cyst-producing species are represented. This record dates back to the Late Triassic about 200 million years ago when the earliest definite dinoflagellate fossils occur, although a possible older dinoflagellate, Arpylorus Calandra, has been recorded from the Silurian of North Africa (Calandra 1964; Sarjeant 1978). Recent work on living dinoflagellates has shown that they probably had a long pre-Triassic history when they did not produce fossils that are recognized as dinoflagellates. This is outlined below. Early dinoJlagellate evolution: the mesokaryotic nucleus Two basic forms of cellular organization are recognized by biologists. The prokaryotes lack membranebound DNA, Golgi apparatus, mitochondria, and plastids, and include the bacteria and blue-green algae. This condition is considered by many to be primitive and to have preceded the development of eukaryotes. The eukaryotes possess a membrane-bound nucleus and are thought to have evolved from prokaryotic ancestors. Grell and Wohlfarth-Bottermann (1957) and Grass6 and Dragesco (1957) were the first workers to recognize the unusual nature of the dinoflagellate nucleus. Dodge

0008-4026/81/112077-11$01.OO/O 01981 National Research Council of CanadaIConseil national de recherches du Canada

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CAN. J. BOT. VOL. 59, 1981


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FIG. 1. Various types of dinoflagellates. (A) Gonyaulux, a unicellular, biflagellate, thecate form. (B) Dinamoebidium, an amoeboid form. (C) Polykrikos, a colonial motile form. (D) Dinothrix, a filamentous form. A, C from Schiller (1933-1937). B fromAlgenkunde by B. Fott, 1956. Reprinted by permission of Gustav Fischer Verlag, Wollgrasweg 49, Postfach 720143, 1 Stuttgart 70, Germany. D from An evolutionary survey of theplant kingdom by R. F. Scagel, R. J . Bandoni, G. F. Rouse, W. B. Schofield, J. R. Stein, and T. M. C. Taylor. O 1965 by Wadsworth Publishing Co., Inc. Reprinted by permission of Wadsworth Publishing Co., Belmont, CA, U.S.A. 94002.

(1965, 1966) and Loeblich (1976) subsequently found that dinoflagellates are unusual in having a combination of prokaryotic and eukaryotic features. The prokaryotic dinoflagellate features determined by the above authors are listed below. (1) The fibrillar diameter of dinoflagellate chromatin is 3-6nm. (2) Basic proteins, typical of eukaryotes, have not been detected in free-living dinoflagellates, and the basic proteins present in parasitic dinoflagellates differ qualitatively and quantitatively from those of eukaryotes. (3) The chromosomes of all dinoflagellates are attached to the nuclear membrane. (4) The fibrillar arrangement of the dinoflagellate chromosome is similar to that of the bacterial nucleoid, both having archlike swirls of fibrils. This may be due to the low level of chromosomal proteins in the dinoflagellate chromatin which allows it to fold into a state similar to that assumed by the bacterial chromosome. In contrast, the dinoflagellate nucleus has several

eukaryotic features as outlined by Loeblich (1976). (1) Larger amounts of repeated DNA are present, unlike the very small amounts of repeated DNA sequence in prokaryotes. The repeated DNA sequences in eukaryotes are typically interspersed with longer sequences of unique DNA. Studies on dinoflagellates indicate that they possess up to 60% of repeated DNA interspersed with highly complex DNA. (2) As in eukaryotes, there is a discrete phase of DNA synthesis in dinoflagellates in contrast to a prokaryotic pattern of continuous DNA synthesis. (3) Although basic proteins have not been detected in free-living dinoflagellates, some parasitic forms do contain basic proteins. (4) Free-living dinoflagellates have many membrane-lined cytoplasmic tunnels piercing the dividing nucleus. These tunnels contain elongated extranuclear microtubules. The earlier belief that dinoflagellates differ from higher eukaryotes in lacking an extranuclear spindle is giving way to the interpretation of these extranuclear microtubules as an extranuclear spindle. The combination of prokaryotic and eukaryotic features led Dodge (1965) to postulate that dinoflagellates, for which he proposed the term Mesocaryota, were intermediate in nuclear organization between the prokaryotes and eukaryotes. Loeblich (1976) subsequently reviewed these features and concluded that they suggest that dinoflagellates are a geologically old group and diverged "from the higher eukaryotic lineage before evolution of eukaryotic chromatin but after the evolution of repeated DNA" (Fig. 2). Fossil remains of blue-green algae between 1600 and 2000 million years old are known with certainty from the Middle Precambrian Gunflint Chert (Barghoorn and Tyler 1965). However, Schopf and Barghoorn (1967) recorded prokaryotes from the Fig Tree Group of the Transvaal which has been estimated to be more than 3100 million years old. According to Schopf (l970), eukaryotic organization possibly appeared at the beginning of the Late Precambrian (1700 million years ago) and definitely existed 900 million years ago, as recorded in the Bitter Springs Formation of Australia. This is based on the presence in the Bitter Springs Formation of granular, subspherical organic bodies in fossilized cells of the genus Caryosphaeroides Schopf. These bodies are interpreted as remnants of degraded nuclei. The cells also appear to have been plasmolyzed during preservation, with a resulting separation of inner and outer wall layers. Within the same formation the genus Eomycetopsis Schopf is interpreted as being of fungal affinity and thus would be eukaryotic. Schopf (1968) also recorded the genus Gloeodiniopsis Schopf from the Bitter Springs Formation and considered it to be of possible dinophycean affinity. This paleontological evidence, taken with Dodge's and

BUJAK AND WILLIAMS

NON-PHOTOSYNTHETIC DINOFLAGELLATES


PHOTOSYNTHETIC DINOFLAGELLATES

PRDBABLE A C Q U I S I T I O N OF CHLOROPLASTS FROM INGESTED EUKARYOTES AND PROKARYOTES

DEVELOPMENT

(MOSTLY FREE SWIMMING)

CHLOROPLASTS

1

(MOSTLY PARASITIC)

1

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FIG. 2. Possible pattern of early dinoflagellate evolution, based partly on the work of Dodge (1965) and Loeblich (1976).

Loeblich's hypotheses, suggests that dinoflagellate precursors with a mesokaryotic organization may have diverged more than 900 million years ago, and perhaps more than 1700 million years ago when the earliest possible eukaryotes are known to have occurred. Dinophycean-syndiniophycean separation Five classes have been erected in the Pyrrhophyta, two of which, the Ebriophyceae and the Ellobiophyceae, are small and poorly known. Two of the other classes, the Dinophyceae and the Desmophyceae, were combined by Dodge (1975) and Loeblich (1976) into a single class, the Dinophyceae. The Class Syndiniophyceae was established by Loeblich (1976) for intracellular parasitic dinoflagellates with anomalous nuclear features, based upon the work of Ris and Kubai (1974). The following characteristics of each class are taken from Bold and Wynne (1978). Class Ebriophyceae: cells colourless, biflagellate, lacking resistant outer covering; an internal siliceous skeleton is present. Class Ellobiophyceae: cells parasitic, attached, lacking a theca but with a complex pellicle; motile stages of the gymnodinioid type. Class Syndiniophyceae: cells parasitic, without a cellular covering of plates; nuclei with low chromosome

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numbers; chromosomes V-shaped and with detectable amounts of basic protein; mitosis associated with centrioles. Class Dinophyceae: motile cells biflagellate, one flagellum located in a transversely aligned groove and with a vibrating beat, the other flagellum beating in a longitudinally aligned groove and extending in a posterior direction from the cell. Class Desmophyceae: motile cells with two apically or subapically inserted flagella, one directed longitudinally forward and the other beating in a plane perpendicular to the first and encircling the first. The Desmophyceae, which previously incorporated three orders, are included in the Dinophyceae in Table 1 and in subsequent discussions. The Ebriophyceae and Ellobiophyceae thus differ from the Dinophyceae only in their life-style and wall structure, being identical to the Dinophyceae in their nuclear structure. The Syndiniophyceae Loeblich differ fundamentally in nuclear structure because of their chromosome number, chromosome structure, and the nature of mitotic division. As noted by Loeblich (1976), the nuclear structure of the Syndiniophyceae differs from the Dinophyceae in several respects. (1) They have a low chromosome number (4 to 10) compared with the Dinophyceae (12 to 400). (2) They have V-shaped chromosomes with the apex attached to the nuclear membrane. The Dinophyceae have rod-shaped chromosomes. (3) The chromosomes contain histochemically detectable basic proteins unlike the Dinophyceae. (4) The Syndiniophyceae have centrioles, and only one microtubule-containing membrane-lined tunnel piercing the dividing nucleus. The Dinophyceae have many membrane-lined cytoplasmic tunnels piercing the dividing nucleus. These differences indicate that the Syndiniophyceae and the Dinophyceae (taken in this context to include the Ebriophyceae and Ellobiophyceae) separated at an early stage in dinoflagellate evolution. However, as Loeblich (1976) observed, it is difficult to say whether the Dinophyceae or Syndiniophyceae are the more primitive, since fossilized remains of the Syndiniophyceae have not been recognized. Figure 2 shows both classes evolving at about the same time from an early mesokaryotic dinoflagellate ancestor. The acquisition of chloroplasts The presence of endosymbionts in some species of dinoflagellates, and comparisons of the type of pigments and the structure of pyrenoids in modem species, indicate that chloroplasts were acquired by dinoflagellates through symbiosis with ingested organisms (Figs. 2, 3). Dodge (1971) and Tomas and Cox (1973) observed two nuclei in the dinoflagellates Glenodiniumfoliaceum

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CAN. 1. BOT. VOL. 59. 1981

TABLE1. Classification of the division Pyrrhophyta following Loeblich (1976), with the class Desmophyceae included within the Dinophyceae Class

No. of orders


Dinophyceae (F)

15 including: Gymnodiniales Dinophy siales Peridiniales Prorocentrales 1

Syndiniophyceae (L)

Life style Predominantly free swimming

Intracellular parasites

Ebriophyceae (L)

1

Siliceous plus heterotrophic or phagotrophic

Ellobiophyceae (L)

1

Parasites with a filamentous vegetative stage

NOTE:F, Fritsch; L, Loeblich

teristic of dinoflagellates), and the presence of an internal pyrenoid within the chloroplasts, in contrast to the stalked pyrenoids typically found in dinoflagellates. Dodge (1975) subsequently found fucoxanthin to be the predominant carotenoid in other dinoflagellate species with internal pyrenoids but only one, mesokaryotic nucleus. These observations led him to suggest that primitive dinoflagellates lacked chloroplasts and later acquired them through endosymbiosis with autotrophic PIRIDlnlH ACPUIRfD PLASM chrysophycean algae. This condition would be similar to that seen today in G . foliaceum and P. balticum. Subsequently, the eukaryotic nucleus of the endosymbiont was lost (as seen in Gymnodinium micrum (Leadbetter and Dodge) Loeblich and Gymnodinium venejcum Ballantine), while the internal pyrenoids and fucoxanthin were retained. The most advanced condition achieved in dinoflagellates would be the development of peridinin in place of fucoxanthin, the presence of stalked pyrenoids, and a single, mesokaryotic nucleus. Loeblich (1976) suggested a variation of Dodge's hypothesis, with fucoxanthin being acquired from a eukaryotic endosymbiont and peridinin being obtained from a captured prokaryotic organism. Nonphotosynthetic dinoflagellates, such as the Syndiniophyceae, FIG. 3. Simplified model of the possible way in which may never have acquired the ability to photosynthesize dinoflagellates acquired various types of pigments, pyrenoids, or may have lost this ability through the degeneration of their plastids. and nuclei. Stein and Peridinium balticum (Levander) Lemmer- Evolution of the wall in the Dinophyceae mann. In both species one of the nuclei was eukaryotic The class Dinophyceae includes 15 of the 18 Pyrand the other was mesokaryotic. Detailed study of the rhophyta orders. They are mostly free swimming and structure of P. balticum showed that the eukaryotic photosynthetic, and are subdivided primarily on wall nucleus belonged to a chrysophycean endosymbiont structure, swimming direction, and flagellar position. The Dinophyceae are either "naked (unarmoured), lying within the colourless cytoplasm of the dinoflagellate host and separated from it by a plasma membrane lacking a cellulosic covering, or possess a cellulosic (Tomas and Cox 1973). Other features indicating a wall (theca) divided into several "plates" (armoured) nondinophycean affinity for the endosymbiont were the whose number and arrangement is characteristic of the presence of the carotenoid fucoxanthin (characteristic of four main orders shown in Table 2. It was previously most Chrysophyta), the absence of peridinin (charac- thought that there was a clear distinction between the i

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BUJAK AND WILLIAMS

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TABLE2. Diagnostic features and fossil record of the four main orders of the class Dinophyceae. The remaining 11 orders are not shown


Fossil record Order

Features

Definite

Probable

Prorocentrales

Armoured with two anterior flagella

None

Also may include Precambrian to modem acritarchs

Dinophysiales

Armoured with two subsymmetrical valves separated sagitally, both flagella arise ventrally

Possible ancestral forms, all cysts, Jurassic.


Gymnodiniales

Unarmoured, both flagella arise ventrally

One ?cyst genus, Late Cretaceous


Peridiniales

Armoured with numerous plates arranged in latitudinal series, both flagella arise ventrally

Abundant but selective, all cysts, Late Triassic to present


wall structure of naked and armoured dinoflagellates, by the Late Cretaceous genus Dinogymnium Evitt, but Dodge and Crawford (1970) have demonstrated a Clarke, and Verdier (Fig. 4C). complete morphological gradation. The order Peridiniales (Figs. 4D-4F) is armoured In the following sections, the number of plates with numerous plates arranged in several latitudinal defined is exclusive of those in the flagellar furrows. series relative to a polar swimming direction. Some The order Prorocentrales, as typified by the genus genera such as Woloszynskia Thompson possess over 40 Prorocentrum Ehrenberg (Fig. 4A), possesses two large plates which are typically thin and polygonal, but the plates of approximately equal size and two flagella majority of Peridiniales, as typified by the genus which are anteriorly located relative to the swimming Peridinium Ehrenberg (Fig. 4D) possess about 20 plates direction. Loeblich (1976) figured specimens with six to (excluding smaller plates associated with the flagellar seven additional plates which are very small and are furrows) which can be arranged in several ways. grouped around the flagella. No fossil representatives The Peridiniales have a flagellar arrangement similar belonging to this order are known. to that in the Gymnodiniales and Dinophysiales. The The order Dinophysiales, as typified by the genus majority of recognizable fossil dinoflagellates are inDinophysis Ehrenberg (Fig. 4B), is armoured with two cluded in the Peridiniales and have a known stratisubsymmetrical valves separated sagitally and two fla- graphic range from Triassic to Recent. gella which arise ventrally. Nine plates are present, excluding those in the flagellar furrows. A transverse The Arpylorus question Dinoflagellates have an abundant fossil record from flagellum encircles the cell in a furrow while the other, longitudinal flagellum, trails behind during swimming. the Late Triassic to the present, with over 2000 species Possible ancestral forms of the Dinophysiales are known being described. The possible occurrence of a Late from the Jurassic and are included in the genus Nanno- Silurian dinoflagellate species, which would predate the next oldest recognizable fossil dinoflagellate by some ceratopsis Deflandre. The order Gymnodiniales, as typified by the unar- 200 million years, is therefore both exciting and moured genus Gymnodinium Stein, does not possess daunting since it hints at a fossil record that may be cellulosic plates. Dodge and Crawford (1970), howev- incomplete in the extreme. er, showed that there is a morphological continuum The genus Arpylorus was described by Calandra ranging from unarmoured forms of the Gymnodinium (1964) from the Late Silurian of Tunisia. Sarjeant type to forms possessing strongly developed cellulosic (1978) in a detailed re-examination of Calandra's plates typical of the Peridiniales. As in the Dinophys- material concluded that Arpylorus is a dinoflagellate iales, the flagella of the Gymnodiniales arise ventrally cyst. As evidence he cited (1) the presence of an and show differentiation into transverse and longitudinal excystment opening (archeopyle); (2) the presence of a flagella. Fossil Gymnodiniales are probably represented paracingulum (a structure reflecting the position of the L2

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FIG. 4. Representatives of the class Dinophyceae. ( A ) Prorocentrum Ehrenberg, typical of the order Prorocentrales. (B) Dinophysis Ehrenberg, typical of the order Dinophysiales. (C) Dinogymnium Evitt, Clarke, and Verdier, a fossil representative of the order Gyrnnodiniales. (D-F) Three genera of the order Peridiniales. D, Peridirzium Ehrenberg; E, Gonyaulax Diesing; F, Ceratium Schrank. Scale bar = 10 prn.

transverse flagellar furrow); (3) vestiges of tabulation; and (4) the tendency of the cyst to split into pieces resembling in size, shape, and relative position the plates of a thecate dinoflagellate. The question of whether Arpylorus is a dinoflagellate is critical to any model which attempts to explain

dinophycean evolution. If it is a dinoflagellate as stated by Sarjeant, it would indicate that by the Silurian the Dinophyceae already possessed a transverse-longitudinal flagellar arrangement, and a covering of peridinialean-like plates. It would also indicate that the fossil dinophycean record is extremely incomplete with


BUJAK AND WILLIAMS

a major gap in at least the Upper Paleozoic. With our present state of knowledge, therefore, the fossil record could not be used as evidence to support or refute any of the evolutionary models discussed below. Alternatively, Arpylorus may not represent a Silurian dinoflagellate. Openings are present in the walls of a variety of fossil microorganisms, many of which are not cysts. Thus, the presence of an opening in Arpylorus can not alone be taken as proof of dinophycean affinity. Also, the presence of polygonal fields is a common feature in nondinoflagellates such as the Prasinophyceae which occur frequently in Lower Paleozoic rocks. As noted by Sarjeant, the tendency of Arpylorus to break into pieces is not typical of dinoflagellate cysts. Undoubted dinoflagellate affinity would be indicated by the presence of the two flagellar furrows (cingulum and sulcus). Indications of a cingulum are not clearly shown in any of Sarjeant's photographs but are shown in the camera-lucida drawings. Sarjeant was only able to discern with difficulty a sulcus in a few of the 22 examined specimens. In our present state of knowledge it seems preferable to keep an open mind on the question of whether or not Arpylorus is a dinoflagellate. Plate increase model The plate increase model was proposed by Loeblich (1976) who suggested that the Prorocentrales were ancestral to the Dinophyceae. His line of reasoning was as follows. The anterior arrangement of the two flagella in Prorocentrum is similar to that found in other algal cells such as the Desmocapsales and Protaspidales, whereas the transverse-longitudinal arrangement seen in the other dinophycean orders is unique to dinoflagellates (Fig. 5). He surmised that the transverse-longitudinal arrangement evolved from a less complicated, apical arrangement. He also noted that the acritarchs, a palynological group of uncertain affinity which are abundant in the Paleozoic, do not possess obvious dinoflagellate characters such as the longitudinaltransverse grooves and evidence of polygonal plates or openings, as shown by typical peridinialean cysts. According to Loeblich (1976, p. 23): The existence of Prorocentrum, a dinoflagellate with an apical flagellar orientation but lacking polygonal thecal plates, provides a rationale for reinterpreting as dinoflagellates some of the remains of organisms referred to as Acritarcha.

Loeblich (1976) also suggested that the armoured (thecate) condition, in which the dinoflagellate cell is surrounded by a cellulosic wall, is primitive since it is shared by most plants. Unarmoured dinoflagellates such as the Gymnodiniales would thus represent advanced forms. Finally, Loeblich demonstrated the homologous rela-

FIG. 5. Flagellar number and arrangement in motile cells of the various algal divisions. (A-E) Chlorophyta (green algae). (F, G) Euglenophyta (euglenoids). (H, I) Phaeophyta (brown algae). (J-L) Chrysophyta (golden and yellow-green algae). (M, N) Pyrrhophyta (dinoflagellates; M, Prorocentrum; N, Gymnodinium). (0, P) Cryptophyta (cryptomonads). All figures from Bold and Wynne's Introduction to the algae. 1978. Reprinted by permission of Prentice-Hall Inc., New Jersey.

tionship between the two large valves of Prorocentrum and the two halves (epitheca and hypotheca) of the other orders of Dinophyceae (Fig. 6). He observed that the two flagella in the Prorocentrales are identical to those of other dinoflagellates, one bearing hairs and an associated striated band (equivalent in structure to the transverse flagellum) and the other lacking both (equivalent to the longitudinal flagellum). The two flagellar pores in Prorocentrum are surrounded by several small plates which are located in a notch in one of the major plates, termed the left valve by Biecheler (1952). As shown in Fig. 6, the relative positions of the flagellar pores in Prorocentrum indicate that the left valve is equivalent to the epitheca, and the right valve is equivalent to the hypotheca. The notched area with small plates would be equivalent to the sulcus of other dinoflagellates. Using Loeblich's hypothesis, the diagram shown in Fig. 7 has been constructed, and shows the Peridiniales evolving by differentiation of the thecate wall into several series of polygonal plates. This must have been accompanied by a change in swimming direction. Further increase in the number of plates and thinning of the thecate wall would lead to dinoflagellates such as Woloszynskia. Ultimate thinning of the cellulosic plates

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CAN. J. BOT. VOL. 59, 1981

SWIMMING DIRECTION L E F T VALVE,


\RIGHT

I

VALVE

FIG. 6. Diagram showing the homologous relationship between various features of Prorocentrum-like dinoflagellates (A, B) and dinophycean forms having a transverse and a longitudinal flagellum (C, D). Left valve, epitheca; right valve, hypotheca; flagellum marked T, transverse flagellum; flagellum marked L, longitudinal flagellum. Note also the difference in swimming direction.

I VENTRAL

FUGELU

I

FIG.7. The plate increase model of dinophycean evolution.

would result in their loss and the development of unamoured dinoflagellates such as Gymnodinium. Dinophysialean dinoflagellates with their unusual plate arrangement would have evolved after the change in swimming direction since their flagella are arranged ventrally as in the Peridiniales. Plate reduction model The plate reduction model is based on the observation that most Late Triassic to modem dinoflagellates show a general reduction in plate number (~orhoferand Davies 1980; Eaton 1980). According to the plate reduction

model (Fig. 8), the ancestral dinoflagellate was an unamoured gymnodinialean type and may have formed acritarch-like cysts. Development of a thin cellulosic wall with many polygonal plates led to forms such as the Late Triassic dinoflagellate Suessia Morbey which possessed more plates and latitudinal plate series than the later peridinialean dinoflagellates. A modem representative of these early forms may be the genus Woloszynskia which has more than 40 polygonal plates. Subsequent reduction in the number of plates with accompanying increase in their thickness and standardization into distinct latitudinal series led to the typical peridinialean dinoflagellates. These first occur with certainty in the Jurassic and include most of the known fossil taxa of proven dinoflagellate affinity. Exceptions are the Silurian genus Arpylorus Calandra discussed above, the possible dinophysialean precursor Nannoceratopsis Deflandre from the Jurassic, and the probable gymnodinialean genus Dinogymnium from the Late Cretaceous. Dinophysialean dinoflagellates evolved as an offshoot of the Peridiniales by rearrangement of the plates. The Prorocentrales, which would be the most advanced forms according to this model, evolved by a change in swimming direction towards the area of flagellar insertion, and by either fusion or assimilation of the "epithecal and hypothecal" plates into two large valves, the left and right of Biecheler (1952). Two mechanisms have been proposed for decreasing the number of plates in the Peridiniales. One, termed unidirectional plate growth by ~orlioferand Davies (1980), suggests that loss of some plates occurred through their gradual decrease in size accompanied by a corresponding increase in size and importance of other plates. This would lead eventually to a few large plates directly descended from and homologous to single plates of the ancestral dinoflagellates. ,The second, termed multidirectional plate fusion by Dorliofer and Davies (1980), suggests that plate loss occurred through GIHHOOlHlALES (01

e . g Yolaszynrkla

A

S W E PERlOlHlALES (,401

mST

A

MOOlFlEO PLATE ARQAHGEMEHT

REOUCTIOH I H PLATE HWBER

OcYELoPMini OF A CELLULOSIC WALL VENTRAL F L A G E L U OIHOFUGELUTE

FIG. 8. The plate reduction model of dinophycean evolution.

BUJAK AND WILLIAMS

2085


fusion of plates, so that a single large plate would be homologous to several smaller plates of the ancestral dinoflagellates. The plate fragmentation model The two models of dinophycean evolution outlined above do not satisfactorily combine the paleontological and neontological evidence. The supposition that anterior insertion of the flagella is a primitive feature (Loeblich 1976) is taken into account in the plate increase model but cannot be accommodated in the plate reduction model. Conversely, the fossil record, with the exception of Arpylorus, while supporting the plate reduction model, is not consistent with the plate increase model. A model is therefore proposed below in which both neontological and paleontological factors are amalgamated. The plate fragmentation model (Fig. 9) suggests that ancestral dinophycean dinoflagellates had an undifferentiated cellulosic wall consisting of two valves and two anterior flagella (Fig. 10A). The Prorocentrales are living representatives of this early order. Some palynomorphs of uncertain origin (acritarchs) may be the cysts of these primitive forms, as suggested by Loeblich ( 1976). Change in swimming direction led to one flagellum becoming transverse and encircling the cell, and the other becoming longitudinal and trailing behind. Associated with this development was fragmentation of the valves into numerous undifferentiated polygonal plates (Fig. lOB), as seen in Late Triassic peridinialeans such as the genus Suessia. In these forms latitudinal series of plates can be discerned, an arrangement presumably developed in response to the positioning of the transverse flagellum. The fossil record indicates that the dinoflagellates underwent a major development in the Late Triassic and that this was accompanied by a decline in the acritarch populations in associated assemblages,

FIG. 9. The plate fragmentation model of dinophycean evolution.

FIG. 10. Evolution of tabulation according to the plate fragmentation model. (A) Prorocentrum-like ancestor with two valves. (B) Suessia-Woloszynskia-like form with numerous plates arranged geometrically. (C) Hypothetical form intermediate between B and D showing the reduction in plate number. (D) Modem Gonyaulax showing stabilization of individual plate size and shape in contrast to the geometric pattern seen in B.

suggesting that the two events were related. If some dinoflagellates evolved a new swimming mode in the Middle-Late Triassic, it may have been related to the initial separation of the super-continent Pangaea which was accompanied by changing oceanic circulation patterns and an increase in continental shelf area. Subsequent evolution of the Peridiniales emphasized the importance of the transverse flagellar furrow (cingulum) and the longitudinal flagellar furrow (sulcus). This placed increasing emphasis on the latitudinal rows of plates in several ways: the number of latitudinal rows decreased, the number of plates within each row decreased, and the shape, position, and relationship of each plate stabilized (Fig. 10C). Such forms are first seen as fossils in the Early Jurassic, indicating that evolution from Suessia-like ancestors to these more advanced forms was relatively rapid. Subsequent evolution of the peridinialeans involved changes in detail leading to separation of several groups including the Pareodinia group, the Gonyaulax group (Fig. lOD), and the Peridinium group. The relationship between the Dinophysiales and other m o u r e d dinophycean dinoflagellates was until recently uncertain because of the apparently unrelated arrangement of the plates. Work by Pie1 and Evitt (1978), however, has shown that the Jurassic genus Nannoceratopsis has a plate arrangement which may be interme-


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diate between the Peridiniales and Dinophysiales. This would indicate that Nannoceratopsis evolved from early peridinialean ancestors and was ancestral to the Dinophysiales. In the plate fragmentation model, the Gymnodiniales, Peridiniales, and Dinophysiales had a common ancestor with many polygonal plates. Thinning of the plates, as seen in the modem genus Woloszynskia, would ultimately lead to the naked Gymnodiniales which lack cellulosic plates. As noted by Loeblich (1976), there is some evidence for this, since the unarmoured cell covering of Gymnodinium consists of vesicles and membranes arranged identically to those in the amphiesma (cell covering) of an armoured cell. The only difference is that the Gymnodiniales lack cellulosic plates in the vesicles. It seems unlikely that such an elaborate membrane layer of vesicles would have evolved unless at one time it contained polygonal thecal plates. The naked Gymnodiniales may thus have developed from a multiplated ancestor soon after the latter had itself evolved. The Late Cretaceous occurrence of the gymnodinialean-like genus Dinogymnium probably represents only a small part of the total stratigraphic range of the order Gymnodiniales. This does not imply that the Gymnodiniales are more or less advanced than the Peridiniales, but only that the two orders evolved from a common ancestor in different ways. Evolution of the Peridiniales The vast majority of fossil dinoflagellates belong to the Peridiniales. Even though the record is incomplete, only cyst-producing species being present, it provides the only direct evidence for the pathways along which the peridinialean taxa evolved. Apart from a possible Late Silurian genus, Arpylorus, the oldest dinoflagellates that can be attributed with certainty to the Peridiniales are Triassic, and are typified by Suessia-like forms with numerous, polygonal plates which appear to be arranged in latitudinal series (Fig. 11). Although these Late Triassic forms show delineation of the transverse and longitudinal furrows as in later peridinialeans, the number of latitudinal rows and number of plates in each is greater in the older forms. By the Middle Jurassic, the number of latitudinal series and plates had been considerably reduced and had stabilized in several ways, reflecting at least three main groups of peridinialeans. The first, the Pareodinia group, is known only from the Jurassic and Early Cretaceous. The other two, the Gonyaulax and Peridinium groups, are today extremely successful and very abundant. The Gonyaulax group appears to have had several offshoots, including the Ceratium group which evolved later in the Jurassic. No recognizable fossils of the genus Ceratium Schrank occur in the Tertiary, but it is an important constituent of living phytoplankton in lakes and tropical seas. Another offshoot from the main Gonyaulax stock

FIG. 11. Schematic diagram showing the evolution of peridinialean tabulation in part. This is based on paleontological data only.

is represented by the modem genus Heteraulacus Diesing. This group is characterized by a distinctive arrangement of plates, especially at the antapical pole, and is first seen in the fossil record as the Cretaceous genus Dinopterygium Deflandre. However, the group may have diverged from the Gonyaulax stock much earlier in the Mesozoic. The third main group, typified by the modem genus Peridinium, is first known with certainty from the Early Cretaceous, but presently undescribed forms from the Jurassic indicate its divergence at an earlier date. Evolution of this group involved several subtle changes in plate shape and relationship, perhaps the most significant leading to the now extinct Wetzeliella group which was highly successful in the Early Tertiary. Another development led to the single-walled species which dominate modem marine Peridinium assemblages.

Conclusions The dinophycean fossil record can be explained by the plate reduction model while the neontological data tend to support the plate increase model. Neither theory satisfactorily combines the two lines of evidence. The plate fragmentation model is therefore proposed herein in an attempt to reconcile the neontological and paleontological data. The plate fragmentation model suggests that prorocentralean dinoflagellates were successful through much of the Paleozoic and may be represented as fossils by some of the acritarchs. During the Carboniferous and Permian their evolution remained relatively static, probably reflecting the global continental configuration and water circulation of that time. A major development in the evolution of the dinoflagellate wall occurred in the Triassic and resulted from a change in swimming direction. This may have been

BUJAK AND WILLIAMS


related to the initial separation of the supercontinent Pangaea which was accompanied by changing oceanic circulation patterns and an increase in continental shelf areas. T h e dinoflagellates thus enjoyed a resurgence and success which has continued to the present, since they were able to utilize the newly available environments because of the unique development of a transverselongitudinal flagellar arrangement, and the modification of their plates which accompanied this change.

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