AN E V A L U A T I O N OF A P O S S I B L E P H Y L O G E N E T I C

R E L A T I O N S H I P B E T W E E N THE E U G L E N O P H Y T A A N D
KINETOPLASTIDA

P E T E R A. K I V I C and P A T R I C I A L. W A L N E
Department of Botany, University of Tennessee, Knoxville, TN 37996-1100, U.S.A.

(Received 5 October, 1983)

Abstract. Without close phylogenetic ties to any of the other algae, the Euglenophyta are a taxonomic
enigma. The argument is made here that the euglenopbytes have extensive morphological homology with the
zooflagellate trypanosomatids, bodonids, and Isonema. A phylogenetic sequence is postulated linking these
groups; the available data suggest that the euglenophytes had their origin in these zooflagellates and that the
introduction of the chloroplast and a phototrophic mode of nutrition was a relatively late step in this
evolutionary process.

1. Introduction

The euglenoid flagellates are a traditional taxonomic puzzle: a diverse collection of

phototrophs, phagotrophs and osmotrophs which are all closely related to one another
but not, according to all available evidence, to any other algal group (Dodge, 1975;
Leedale, 1967). Their closest affinities are perhaps with some fairly obscure zoo-
flagellates. The present work is an exploration of these possible euglenoid-zooflagellate
connections.
Three zooflagellate taxa were examined for possible phylogenetically relevant
similarities with the euglenoids: the trypanosomatids, uniflagellate and exclusively
parasitic; the bodonids, tiny, biflagellate and mostly free living; and the biflagellate
marine flagellate, lsonema. The bodonids and trypanosomatids are closely related and
have been combined as the Kinetoplastida (Brooker, 1971a; Honigberg, 1963);
together or separately, they have been suggested a number of times as possible
eugtenoid relatives (e.g., Bovee, 1972; Brooker, 1971a; Burzell, 1973; Dodge, 1973;
Hutner et ai., 1968; Leedale, 1970; Mignot, 1964, 1966; Porter, 1973; Round, 1980;
Schuster et al., 1968; Swale, 1973; Taylor, 1976, 1980; Vickerman and Preston, 1976).
isonema has no known affinities, but has been described as having certain euglenoid
properties and possible euglenoid affiliations (Porter, 1973; Schuster et at., 1968; and a
presumptive isonema: Bodammer and Sawyer, 1981).
Information obtained from an extensive literature search has afforded a criticaI
comparison of several organellar systems in these organisms.

2. Morphological Comparisons
The above groups are by no means identical, and within each there are, of course,

Origins oJLiJe 13 (1984) 269-288. 0302-1688/84/0133-0269503.00.

9 1984 by D. Reidel Publishing Company.
270 P.A. KIVIC AND P. L. WALNE

instances of broad morphological variation among taxa; but we do find a relatively

large number of characters which are similar or essentially the same in most of the
organisms considered:
a. General morphology. The kinetoplastids, euglenoids and lsonema all manifest a
similar external morphology: an ovoid-toqanceolate body shape, usually with a helical
symmetry; the flagella (usually two) insert within an anterior subapical pocket. In the
phagotrophs, a tubular ingestion apparatus usually opens near the right-ventral edge
of the flagellar pocket.
b. Pattern of movement. A peculiar crawling movement termed 'metaboly' or
'euglenoid motion' is found in all euglenoids not totally restricted by a rigid pellicle,
and has traditionally been considered a basic euglenoid characteristic (Leedale, t967;
Mikolajczyk and Kuznicki, 1981; Pringsheim, 1956). Euglenoid motion, or behavior
very similar to it, however, has also been described in Isonema (Porter, 1973; Schuster
etal., 1968), and in the bodonids Cryptobia vaginalis (Vickerman, 1977) and
Rynchomonas metabolita (Burzell, 1973).
c. Flagellar placement. Of the two flagella, usually only the anterior is employed in
propelling the cell. The posterior flagellum is very reduced in some phototrophic and
osmotrophic euglenoids (Leedale, 1967; Leedale and Hibberd, 19~74), but in the
phagotrophs it is characteristically long and trails passively as a ventral 'skid' in
contact with the substratum (Burzell, 1973; Leedale, 1967; Mignot, 1966, 1975; Swale,
1973; Vickerman, 1977; Vickerman and Preston, 1976), possibly serving to keep the
cell close to its food source (Burzell, 1973). The single motile flagellum of the parasitic
trypanosomatids is probably the posterior one (Kivic and Walne, unpublished).
d. Paraflagellar rod. In addition to the usual 9 + 2 microtubular axoneme the
euglenoid flagellum contains a paraflagellar rod (PFR, paraxial rod, intraflagellar
structure) in contact with the axoneme and with a distinctive latticework substructure
(Hyams, 1982; Kivic and Vesk, 1972; Leedale, 1967; Mignot, 1966; Moestrup, 1982).
A similar PFR structure is found in most trypanosomatids (Fuge, 1969; McGhee and
Cosgrove, 1980) and in all of the bodonidsthus far examined ultrastructurally. The
PFR is absent from Isonema (Porter, 1973; Schuster et al., 1968), a few of the
trypanosomatid species (Freymuller and Camargo 1981; McGhee and Cosgrove,
1980), and the reduced posterior flagella of numerous euglenoids (Leedale, 1967).
e. Nucleus and nuclear division. Nuclear architecture and division in euglenoids
(Leedale, 1970) are essentially the same as in bodonids, trypanosomatids and Isonema
(Raikov, 1978), which also have a totally closed mitosis, an intranuclear spindle, and
no metaphase plate formation. In all these taxa, cytokinesis begins at the flagellar
pocket and proceeds posteriorly, following the helical organization of the cell cortex
(Grasse, 1952; Hollande, 1952a, b; Leedale, 1967; Porter, 1973; Schuster et al., 1968).
f. Mitochondria. The euglenoid chondriome (at least as represented by that of
Euglena gracilis) also appears to be a single large reticulum (Pellegrini, 1980). In both
the bodonids and the trypanosomatids, the chondriome similarly consists of a single
large mitochondrion (Paulin, 1975, 1977), which varies in shape from a simple loop
(Rynchomonas, Bodo) or tube (Trypanosoma) to more complex ramifying designs