AMER. ZOOL., 19:1195-1215 (1979).
Cladistic Approaches in the Study of Soil and Plant Parasitic Nematodes
V. R. FERRIS
Department of Entomology, Purdue University,
West Lafayette, Indiana 47907
SYNOPSIS. Cladistic analysis of free-living soil nematodes of the Leptonchoidea (Nematoda: Dorylaimida) resulted in groupings different from those obtained by traditional
methods. We can interpret distributions of species groups obtained by phyletic analysis
in relation to plate tectonic events. Similar techniques are applicable to plant parasitic
nematodes. Grouping on the basis of synapomorphies produced a cladogram of genera
of the family Heteroderidae (Nematoda: Tylenchida) in which Meloidodera and Cryphodera
appear to be the most ancestral genera and the cyst forming genera the most derived.
A cladogram of groups of species in Heterodera sensu lato showed a major division, with
the round cyst nematodes and the Cacli group in one grouping and the rest of the Heterodera
species in the second. I interpret present-day distributions by a strict vicariance view and
suggest potential falsifiers; and also discuss ancient dispersal routes as alternative ways
of thinking about nematode distribution.
INTRODUCTION
ical relationships. I hope to demonstrate
that the cladistic approach has the potential
for strengthening the systematics of freeliving and plant parasitic nematodes in a
way not possible with other techniques. An
analysis that emphasizes identification of
sister groups and reconstruction of hypothetical ancestral character combinations
can make possible a powerful explanatory
model by which to postulate directions of
change and pathways of evolution (Ball,
1978). In addition, a cladistic analysis provides the basis for a falsifiable hypothesis of
the historical biogeography of the group
being analyzed (Ball, 1975; Platnick and
Nelson, 1978).
Phylogenetic principles in systematics
were outlined by Hennig (1966) and Brundin (1966, 1968). Phylogenetic relationship
is concerned with genealogy, which may be
something different from similarity. The
recent literature abounds with excellent
discussions of cladistics which explore the
implications and applications of Hennig's
(1966) terminology and principles (Nelson,
1970, 19736; Ashlock, 1971; Griffiths,
1973; Cracraft, 1974; Platnick, 19766,
1977a, 19776; Engleman and Wiley, 1977;
Kavanaugh, 1977).
Hennig's (1966) technique is based on the
principle that monophyletic sister groups
are detected by the possession in common
FREE-LIVING SOIL NEMATODES
of advanced (or apomorphic) homologous
character states, which must have been presI became interested in cladistics in order
ent also in a shared ancestor. Shared primi- to explore new approaches to historical biotive (or plesiomorphic) homologous char- geography (Nelson, 1969, 1973a; Ball,
acter states tell us nothing about genealog1970, 1971; Valentine, 1971; Croizat etal.,
1974; Rosen, 1974; Raven and Axelrod,
1 acknowledge support by the Systematic Biology 1974; Cracraft, 1975; Edmunds, 1975; ErProgram of the National Science Foundation, Grant win, 1975). A nematode group was chosen
DEB 77-12656. Parts of earlier drafts of the manuscript were read by Mark Deyrup, Michel Luc, Gareth with care for a first application of these
Nelson, L. I. Miller, P. H. Raven, and Dieter Sturhan; I methods. The Leptonchoidea, a group of
am grateful for all their comments, criticisms, and free-living soil nematodes, was an excellent
suggestions. I thank D. E. Rosen and the Society of group for phylogenetic and biogeographic
Systematic Zoology for permission to reproduce Figure 3, and C. G. Goseco for help with Figures 1,2, and analysis for the following reasons: 1) lep5. Journal paper No. 7467, Purdue University Agricul- tonchoids possess many apomorphic chartural Experiment Station, West Lafayette, IN.
acter states; 2) They are found primarily in
1195
1196
V. R. FERRIS
secluded natural areas (where they probably all feed on fungi) rather than in cultivated fields; 3) As a part of a diverse nematode fauna in their natural uncultivated
habitats, they are rare in relative numbers;
and 4) They possess no special drought
resistant long-lived stages as do many of the
successful plant parasitic groups.
To accumulate the necessary data, we
collected or borrowed specimens from all
over the world; and eventually revised
nearly every genus in the superfamily
(Goseco et al., 1975a, 19756, 1976, 1977).
Our analyses in the Leptonchoidea are not
yet complete, but we have established a
number of important facts (Ferris, 1977ft;
Ferris et al., 1976, 1978; and unpublished
data). By studying the entire superfamily,
together with comparisons with other nematode groups, we can distinguish homologous character state polarity with some degree of confidence. We have found a trend
from a plesiomorphic long cylindrical basal
esophageal bulb to a short pyriform bulb
with internal thickenings (Fig. 1). The
plesiomorphic state lacks the constriction
anterior to the bulb. The number and spacing of the auxiliary male sexual organs, the
supplements, is also an important charac-
ter, with a trend from numerous and closely
spaced supplements to those few in number and widely spaced (Fig. 2). Likewise,
the arrangement of the female gonads is
important, with a trend from the plesiomorphic paired symmetrical state to a
monodelphic state, which in some cases is
prodelphic and in others opisthodelphic.
Characters of the head and oral armature
are more difficult to interpret, probably
because they seem to change in response to
ecological factors related to food ingestion.
Our cladistic approach resulted in an entirely new division of the family Leptonchidae into two groups of genera, one without the constriction of the esophagus, and
one with the constriction. Within each
group, the trends in other characters noted
above are clearly evident. The present-day
distributions of the species on a worldwide
basis yield patterns that can be interpreted
in relation to plate tectonic events now
known to have occurred at various times
during the past 200 million years, and responsible for subdivisions of ancestral biota
in many diverse groups (see Raven and
Axelrod, 1974). A cladistic representation
of the history of these geological events is
shown in Figure 3 (Rosen, 1978).
FIG. 1. Esophagi in Leptonchoidea showing trend from long cylindrical basal bulb to short pyriform bulb
with internal thickening. B, C, and F show a constriction anterior to the bulb. A, E, and G do not have the
constriction. (D shows a unique three-part esophagus.)
CLADISTIC APPROACHES IN STUDY OF NEMATODES
1197
FIG. 2. Posterior portions of males in Leptonchoidea showing trend (A to C) from numerous closely spaced
supplements (A) to fewer, widely spaced supplements (B and C).
We postulate that the ancestor of the
Leptonchidae (and of the Leptonchoidea)
was in Pangaea prior to 180 m.y.b.p. (millions of years before present). The most
primitive genus, Funaria van der Linde,
was also in Pangaea, but radiated primarily
in Laurasia after the split of Pangaea into
Laurasia and Gondwanaland (Fig. 3). The
rest of the genera of the Leptonchidae
were Gondwanian. Our knowledge of the
evolutionary pathways, derived from the
cladistic analysis, together with known facts
regarding the time of geological events
(Fig. 3) enables us to interpret present-day
distributions to understand the history of
the group in both space and time (Croizat,
1962; Ball, 1975). Our hypotheses on Leptonchoidea led us to the conclusion that
some species evolved prior to the break up
of Gondwanaland (Fig. 3) and have persisted in some areas (as relict species) until
the present (Ferris et al., 1976). This is a
claim for species longevity not made for
other biota, but we believe it is plausible.
Annelid worms are known (from fossil evidence) to have been well established by the
early Paleozoic. It is reasonable to assume
that nematodes also invaded land during
the Paleozoic and diversified. Stanley
(1975) has suggested that rotifers and certain gastrotrichs may have low rates of extinction because of their small size, abundance, physiological traits and characteristically broad niches; and that because of
their low extinction rates such groups do
not need high diversification rates to ensure survival. This may also be the case with
soil nematodes. Their organizational plan
is effective but simple; and their very simplicity is probably evolutionarily limiting,
with invasion of new habitats dependent on
only minor modifications of the basic plan.
An important feature of our hypothesis is
our evidence that many Leptonchoidea did
not become extinct on the Indian plate as
it rafted northward from Gondwanaland
to collide with the Asian part of Laurasia
(Fig. 3). The evidence is based on present-day distributions of nematode species
with synapomorphies in India, Australia,
Africa and South America, but not in
Eurasia.
1198
V. R. FERRIS
.0
10
20
30
40
50
60
70
80
90
100
110
120
130
140
150
160
170
180
PANGAEA
FIG. 3. Cladistic representation of the history of the breakup of Pangaea greatly simplified, with approximate time scale of the fragmentation events and the conjunction of India and Laurasia. Numbers = millions of years before present (m.y.b.p.). (After Rosen, 1978.)
CLADISTIC APPROACHES IN STUDY OF NEMATODES
Following our discovery of patterns of
distribution in the Leptonchoidea (order
Dorylaimida), which could be explained by
vicariance biogeography, we looked briefly
also (unpublished data) at the species of the
genus Peltamigratus Sher. This genus is a
member of the order Tylenchida, which
contains most of the nematode parasites of
higher plants, but Peltamigratus is found
primarily in natural areas, rather than cultivated fields. Moreover, it is a genus with
some unusual synapomorphies which enabled us to order the species easily into consistent groups on the basis of data from the
literature. The known distribution of the
species provides evidence of a Gondwanian
distribution much as in the genera of the
Leptonchidae.
NEMATODE PARASITES OF ECONOMIC CROP
PLANTS
Most nematodes are free-living, but some
soil forms are parasitic on crop plants.
Losses in the U.S. A to such plant parasitic
forms are placed currently at four billion
dollars yearly, a figure considered by most
researchers to be low (Ferris, 1977a). Among
the most important plant parasitic nematodes worldwide are the cyst nematodes,
which belong to the family Heteroderidae.
The economic significance of members of
the Heteroderidae has produced a vast literature, and a high percentage of the
world's nematologists are working on this
group.
1199
Most nematologists consider the cyst nematodes, which attack various vegetables,
legumes, grains and other crops, to be the
major nematode pests of temperate agriculture (Stone, 1977). Cyst nematodes are
by far the most important pests of potatoes
and sugar beets, and are a serious pest of
wheat, oats, barley and rye (Jones, 1972;
Weischer and Steudel, 1972; Winslow and
Willis, 1972; Mai, 1977; Meagher, 1977).
The soybean cyst nematode is a serious pest
of soybeans. Other cyst nematodes are
known from cultivated and wild hosts in
many parts of the world.
Until the 1970s, the group of nematodes
now known as the Heteroderidae (Table 1)
comprised only three morphologically very
distinct genera. Wouts and Sher (1971) described two additional genera, and suggested an evolutionary scheme. Since 1971
several genera have been added, and additional evolutionary schemes proposed
(Wouts 1973aAc; Stone, 1975; Husain,
1976; Mulvey and Stone, 1976; Luc et al.,
1978). During this period various groupings of the genera into subfamilies were
proposed (Table 1) with the subfamily combinations essentially grade groups in the
terminology of Brundin (1968). Membership in the groups, as well as suggested phylogenies, were based on the possession of
certain characters believed to be plesiomorphic. In a recent paper Luc et al. (1978)
abolished the subfamilies altogether on the
grounds that the subdivisions were neither
accurate nor useful. Their argument is
understandable, but the resulting listing of
TABLE 1. Groupings of the genera of the Heteroderidae into subfamilies as proposed by several recent authors.
Wouts, 1973<z,A,cand
Husain, 1976
Heteroderinae
Heterodera Schmidt
(Globodera) Skarbilovich
Sarisoderinae
Sarisodera Wouts & Sher
Ataloderinae
Atalodera Wouts
Sherodera Wouts
Meloidoderinae
Meloidodera Chitwood
Hannon & Esser
Cryphodera Colbran
Zelandodera Wouts
Stone, 1977
Lucetal., 1978
Heteroderinae
Heterodera
Globodera (Skarbilovich)
Punctodera Mulvey and Stone
Sarisodera
Ataloderinae
Atalodera
Sherodera
Meloidoderinae
Meloidodera
Cryphodera
Zelandodera
Heterodera
Globodera
Punctodera
Sarisodera
Meloidodera
Cryphodera
Atalodera
Hylonema Luc, Taylor & Cadet
1200
V. R. FERRIS
MEI.OIDODERA
THECAVERCKYPHODERA ATAI.ODERA MICULATUS
HYLONEMA
SARISODERA
HETERODERA
GI.OBODERA
PUNCTODERA
8
6,7
FIG. 4. Cladogram of the genera of Heteroderidae. Large circles (with outline sketches of mature females)
across top represent genera; small circles represent hypothetical ancestors with apomorphic character states
indicated by numerals (which correspond to characters listed in Table 2).
genera is hardly satisfying in terms of further analysis and synthesis.
Cladistic analysis of Heteroderidae
I believe the family Heteroderidae can be
analyzed cladistically, and that such analysis
will lay the basis for much fruitful research
and understanding. I have constructed the
cladogram of Figure 4 on the basis of seven
characters which I consider to be homologous throughout the genera and for which
I have designated character state polarity
(Table 2). The general technique of Hennig (1966) and Brundin (1968), was used to
join species groups (in this case genera) on
the basis of synapomorphies working backward in time. The data of Table 2 can be
easily adapted for use in any of several numerical analyses for producing the most
parsimonious branching patterns of a
cladogram (e.g., see Camin and Sokal, 1965;
Farris, 1970; TzrrhetaL, 1970).
If we make the reasonable assumption
TABLE 2. Characters ofgenera of Heteroderidae and character state polarities used to prepare cladogram of Figure 4.
Character
number
Name of character
Plesioriiorphic character state
Apomorphic character state
1.
2.
position of vulva
female cuticle
subequatorial
annulated
3.
4.
length of spicules
relative position of anus
and vulva
body wail of mature female
phasmids, second stage
juvenile
cuticle around vulva
shape of female body
short (<30/xm)
widely separated
subterminal
not annulated (except
anterior end)
long(>30/xm)
close together (4); may be
located on prominence (4 + )
rugose (5) or cyst (5 +)
without lenslike structure
5.
6.
7.
8.
no cyst
with lenslike structure in
muscle layer
not fenestrated
irregularly swollen or
lemon shaped
fenestrated
round or pear shaped
CLADISTIC APPROACHES IN STUDY OF NEMATODES
that the genera of the Heteroderidae are
derived from a vermiform tylenchid ancestor with annulated cuticle (Wouts and Sher,
1971), then the round and pear-shaped cyst
forms Globodera and Punctodera stand out as
apomorphic sister genera sharing a common (hypothetical) ancestor indicated by
circle 8 on Figure 4. These two genera and
Heterodera are fenestrated (Fig. 5), and
share a common ancestor (designated by
circle 6,7) with Heterodera. (In addition, the
phas.nids of the second stage juvenile lack
the lenslike structure in the nearby muscle
layer.) Thus Heterodera becomes the sister
group of Globodera + Punctodera. Sarisodera
also forms a cyst and is designated a sister
group of Heterodera + (Globodera + Puncto-
1201
Thecavermiculatus do not have annulations
in the female cuticle (except at the anterior
end), the spicules in Atalodera are long (no
males have been found for Thecavermiculatus), and the anus and vulva are close
together (Robbins, 1978). These two genera are joined to the cladogram at hypothetical ancestor 2,3,4. (The two genera are
coordinated by the synapomorphy of having the anus and vulva located on a prominence.) Cryphodera, although retaining the
plesiomorphic cuticular annulations, does
possess a synapomorphic subterminal vulva
(as do all genera discussed thus far) and is
therefore joined at hypothetical ancestor 1.
Meloidodera retains all the postulated
plesiomorphic character states on Table 2,
although the body is swollen (as are the
rest). If a form more nearly vermiform is
discovered, it will probably fit to the left of
dera) joined at hypothetical ancestor 5 + .
Hylonema females have a rugose cuticle surface described by Luc et al. (1978) as,
"somewhat resembling a young Heterodera Meloidodera.
cyst." Hylonema is joined to the cladogram The resulting cladogram (Fig. 4) is
by hypothetical ancestor 5. Atalodera and amenable to testing and falsification, as it
FIG. 5. A, longitudinal section through swollen female nematode which has become a lemon-shaped cyst
with eggs; B, longitudinal section through vulval region of cyst; C, posterior end of male; D, E, F, ventral
view of cyst showing bifenestrae, ambifenestrae and circumfenestra respectively, (a = vulva; b = vagina;
c = underbridge; d = bulla; e = fenestra; f = phasmid; g = spicules).
1202
V. R. FERRIS
should be if it is to have scientific value
(Popper, 1968; Cracraft, 1974; Wiley,
1975; Engleman and Wiley, 1977; Platnick,
19776). Brundin (1968) and Hennig (1966)
emphasized that if we have worked properly in preparing such a phylogenetic scheme,
all new knowledge about the group will fit
into the scheme to extend our understanding of the course of evolution of the group.
When information becomes available which
proves to falsify the cladistic hypothesis (or
part of the hypothesis), a new hypothesis is
developed and the process begins again.
Each cycle brings us nearer to an understanding of the true evolutionary events.
I developed the cladogram of Figure 4
prior to the discovery of Thecavermiculatus
and Hylonema. Both these genera fitted into
the scheme and strengthened it. I have not
included the genera Sherodera (synonymized by Luc et al., 1978, with Atalodera) or
Zelandodera (synonymized by Luc et al.,
1978, with Cryphodera) on the cladogram for
the sake of simplicity. These missing genera
can easily be added to the cladogram if the
synonymies prove to be incorrect. During
the development of cladograms, specializations may be discovered that do not occur in
all members of at least one of the two sister
groups. For instance, one species of Sarisodera (Luc et al., 1973) has lost the lenslike
structure near the phasmid (character 6)
although other species have not (Wouts and
Sher, 1971). (Sarisodera is a sister group of
Heterodera + (Globodera + Punctodera), which
have lost the structure.) Hennig (1966) and
Brundin (1968) suggest that such unique
parallelisms are confirmations of the relationship and an indication of relative plesiomorphy between sister groups.
Cladistic analysis of Heterodera sensu lato
The economically important members of
the Heteroderidae are species which form
cysts (excluding the two known species of
Sarisodera, which have been found only on
willow and guinea grass). All cyst forming
plant parasitic species of economic importance were considered to belong to Heterodera until 1976, when Globodera and Punctod-
era were given generic status (Behrens,
1975; Mulvey and Stone, 1976). (Globodera
had been named a subgenus of Heterodera
TABLE 3. Species of Heterodera and of Globodera and
Punctodera grouped on the basis of characters listed in
Table 5.
Globodera group
Globodera virginiae (Miller & Gray)
Globodera solanacearum (Miller & Gray)
Globodera tabacum (Lownsbery & Lownsbery)
Globodera rostochiensis (Wollenweber)
Globodera pallida (Stone)
Globodera achilleae (Golden & Klindic)
Globodera millefolii Kifjanova & Krall)
Globodera artemisiae (Eroshenko & Kasachenko)
Globodera mali (Kifjanova & Borisenko)
Punctodera group
Punctodera punctata (Thorne)
Punctodera matadorensis Mulvey & Stone
Punctodera chalcoensis Stone, Moss & Mulvey
Cacti group
Heterodera cacti Filipjev & Schuurmans Stekhoven
Heterodera betulae Hirschmann & Riggs
Heterodera weissi Steiner
Heterodera estonica Kifjanova & Krall
Heterodera thornei Golden & Raski
Heterodera amaranthi Stoyanov
Avenae group
Heterodera avenae Wollenweber
Heterodera mani Matthews
Heterodera latipons Franklin
Heterodera bifenestra Cooper
Heterodera iri Matthews
Heterodera turcomanica Kifjanova
Heterodera ustinovi Kifjanova
Heterodera hordecalis Andersson
Fici-humuli group
Heteroderafici Kifjanova
Heterodera leuceilyma DiEdwardo & Perry
Heterodera sacchari Luc & Merny
Heterodera cajani Koshy
Heterodera oryzae Luc & Brizuela
Heterodera zeae Koshy, Swarup & Sethi
Heterodera humuli Filipjev
Heterodera cyperi Golden, Ray & G. S. Cobb
Heterodera mothi Khan & Husain
Heterodera graminophila Golden & Birchfield
Heterodera graminis Stynes
Goettingiana group
Heterodera goettingiana Liebscher
Heterodera carotae Jones
Heterodera cruciferae Franklin
Heterodera urticae Cooper
Schachtii group
Heterodera schachtii Schmidt
Heterodera galeopsidis GofFart
Heterodera glycines Ichinohe
Heterodera lespedezae Golden & G. S. Cobb
Heterodera trifolii GofFart
Heterodera limonii Cooper
Heterodera rosii Duggan & Brennan
Heterodera daverti Wouts & Sturhan
CLADISTIC APPROACHES IN STUDY OF NEMATODES
by Skarbilovich, 1959). For this reason a
more satisfactory understanding of the
evolution of this important group of plant
parasites may be gained by looking at
Globodera and Punctodera together with
groupings of Heterodera species (Table 3).
Species of Heterodera sensu lato have been
previously grouped in a variety of ways by
numerous authors, with varying results.
Among recent authors, Franklin (1971) divided the species into groups on the basis of
shape of cyst (round or lemon shaped),
presence or absence of projections near the
vulva called bullae (Fig. 5B), and by nature
of the thin-walled region in the vulval area
(the vulval cone in lemon-shaped species)
called the fenestration (Figs. 5D-F). Matthews (1971) and Mulvey (1972, 1974) used
similar terminal and cone top structures,
but produced somewhat different groupings. Green (1975) grouped the species on
the basis of vulval and vaginal characters.
Stone (1975) arranged the species on the
basis of scanning electron microscope
(SEM) observations of lip regions of second
stage juveniles. More recently Stone (personal communication) has grouped the
species on the basis of several characters
FICI-HUMULI
COETTINGIANA
1203
including type of host group. All of these
researchers have found some of their
groups to be similar to, and some quite different from, the groups of other researchers. An abbreviated list of species and the
groups to which they were assigned by several recent authors is given in Table 4. The
horizontal lines on Table 4 divide the species into groups as they appear on my listing
of Table 3, which is a longer list of species
(although still incomplete). The species in
Table 3 are divided into groups on the
basis of the characters of Table 5.
I constructed the cladogram of Figure 6
on the basis of five homologous characters
(Table 5) for which a reasonable hypothesis
regarding polarity could be established. In
contrast with several earlier authors, I did
not use presence or absence of bullae or the
characteristics of the structure extending
across the vulval cone known as the underbridge (Fig. 5B). Both kinds of structures
seem to be of uncertain origin and of varying interpretation (Cook, 1975; Green,
1975; Golden and Raski, 1977; McLeod
and Khair, 1977). Recent information such
as that of Stone (1975) on lip patterns as
observed by SEM and of Green (1975) on
SCHACHTII
GLOBODERA
PUNCTODERA
FIG. 6. Cladogram of species groups of Heterodera and of Globodera and Punctodera. Large circles across toprepresent species groups; small circles represent hypothetical ancestors with apomorphic character states
indicated by numerals (which correspond to characters listed in Table 5). Lip patterns (after Stone, 1975)
are sketched.
1204
V. R. FERRIS
TABLE 4 . Groupings ofspecies o/Heterodera sensu lato by several recent authors*
Mulvey, 1972
Matthews, 1971
Basis:
lip pattern (SEM)
Basis:
cone top structures
Basis:
structures in vulval cone
cruciferae
carotae
goettingiana
3
3
3
5
5
5
Cruciferae
Cruciferae
Cruciferae
urticae
schachtii
limonii
trifolii
galeopsidis
3
5
5
5
5
5
4
4
4
4
Cruciferae
Schachtii
Schachtii
Schachtii
Schachtii
fid
4
4
4
4
5
Humuli
Humuli
Humuli
Humuli
Basis: vulvaland
vaginal characters
humuli
tatipons
bifenestra
CO CO
Stone, 1975
Green, 1975
avenae
mani
4
4
CO CO
Avenae
Avenae
cacti
weissi
rostochiensis
2
2
1
2
2
1
Cacti
Cacti
Rostochiensis
punctata
6
1
Rostochiensis
'Green (1975) did not label his groups; Stone (1975) and Mulvey (1972) numbered them; and Matthews
(1971) gave them names. Horizontal lines divide species according to my groupings on Figure 3.
the nature of vulval and vaginal characters,
has been of crucial significance in making
possible the kind of analysis which I attempt
here. Likewise, the careful and complete
observations of other authors (Miller and
Gray, 1968, 1972; Franklin, 1971; Matthews,
1971; Mulvey, 1972, 1973, 1974; Shepherd et al., 1972, 1974; Clark et ai, 1973;
Wouts, 1973a; Mulvey and Stone, 1976;
Wouts and Weischer, 1978) are such that
this is probably the only large group of
nematodes for which sufficient information
could be assembled from the literature for
cladistic analysis.
The cladogram of Figure 6 was developed by starting with the round and pearshaped species (Globodera and Punctodera)
and grouping on the basis of synapomorphies as before. The hypothetical ancestral
member of this group is presumed to have
possessed plesiomorphic states of each of
the five characters. Evolution progressed in
two directions from this ancestor. In one
group (on the left in the cladogram, Figure
6) the basic hexaradiate lip pattern evolved
to a pattern with an elongate disc (pattern
4 of Stone, 1975). The Avenae group (see
Table 3) is the plesiomorphic member of
TABLE 5. Characters of species groups of Heterodera and of Globodera and Punctodera and character state
polarities used to prepare cladogram of Figure 6.
Character
number
1.
Name of character
Plesiomorphic character state
2.
3.
cuticle around vulva
vulval cone
lip pattern
bi- or ambi- fenestrate
present
basic hexaradiate
4.
5.
tips of spicules
vulval slit
tips bifid
short (6-19 fim)
Apomorphic character state
circumfenestrate
absent
with elongate disc (3) or
further development (3+)
tips not bifid
long (>30 iim)
CLADISTIC APPROACHES IN STUDY OF NEMATODES
1205
TABLE 6. Genera of Heteroderidae and distribution.*
Genus
Meloidodera Chitwood, Hannon & Esser
Cryphodera Colbran
Atalodera Wouts and Sher
Thecavermiculatus Robbins
Hylonema Luc, Taylor, & Cadet
Sarisodera Wouts & Sher
Heterodera Schmidt
Globodera (Skarbilovich)
Punctodera Mulvey & Stone
Distribution
U.S.A. (S.W., Central, and S.E.); U.S.S.R.; India
U.S.A. (N.W.); Japan; U.S.S.R.; Australia; New
Zealand
U.S.A. (S.W.)
U.S.A(S.W.)
Africa (Ivory Coast)
U.S.A. (West and S.W.); Africa (Ivory Coast)
Worldwide
Worldwide
North America and Europe
* Based on literature.
the sister group resulting from the splitting al. (1973) found a difference in spicule
of this hypothetical ancestor into daughter cusps between those members of the Schachspecies. The second daughter species gave tii group which they examined and memrise to an hypothetical ancestor with a long- bers of the Goettingiana group.
er vulval slit (ancestor 5 on the cladogram).
Additional information will be forthMy Fici-humuli group is heterogeneous coming from laboratories around the world
and future discoveries will undoubtedly on morphological and physiological charproduce refinements in its definition and in acters such as sex attractants (Green and
the cladistic relationships. Hypothetical an- Plumb, 1970), karyotype and genotype
cestor 3+ possessed further modification of (Triantaphyllou, 1970, 1971, 1975aA" Berge
the lip region (lip pattern 3 of Stone, 1975) et al., 1973; Jones, 1975; Dalmasso, 1978),
and gave rise to the Goettingiana and and serology (Webster and Hooper, 1968).
Schachtii groups.
Research into biochemical characteristics
On the right side of the cladogram, of nematodes has progressed to the point
hypothetical ancestor 1 (which was circum- where one female can be analyzed in the
fenestrate) split to form the Cacti group genus Meloidogyne (Berge and Dalmasso,
with a small modification of the basic 1975; Berge et al., 1976; Dalmasso, 1978)
hexaradiate lip pattern; and hypothetical and such techniques can be used for Hetancestor 2,4 in which the vulval cone disap- eroderidae. Serological evidence already
peared, the cysts became spherical or pear obtained (Webster and Hooper, 1968) can
shaped, and the spicules lost their bifidity. be interpreted as evidence for separation of
Globodera retains the plesiomorphic basic the Goettingiana group, the Schachtii
hexaradiate lip pattern, but the pattern is group and Globodera (Green and Plumb,
1970). The specificity of male attractants
altered slightly in Punctodera.
emitted
by females also suggests division
Additional data tend to support the general features of the cladogram. Stone (1972) into the same three groups. An interesting
suggested that the Cacti subgroup (which he problem developed during the research on
felt possessed characters intermediate be- male attractants (Green and Plumb, 1970)
tween Globodera and Heterodera) was so dis- in that H. avenae (lemon-shaped cysts)
tinct that it might need a formal name. Green seemed to be associated with Globodera
(1975) felt that the vulval and vaginal charac- (round cysts) by virtue of the fact that both
ters of the Cacti group were so similar to secreted attractants comprised pf only a
Globodera that despite their lemon shape {ver-few (similar) substances. The authors possus the round or pear shape of Globodera) thetulated that the ancestral heteroderid
species of the Cacti group should be placed in groups secreted attractants comprised of
Globodera] Green (1975) also felt that the many components and suggested that the
species H.fici and H. humuli shared a thick Goettingiana group was closest to the ancuticle of the vulval lips, and that H. avenae cestral Heteroderidae. However, the proband H. mani comprised a distinct group on lem described above is solved if one asthe basis of their vaginal structure. Clark et sumes instead that simple attractants are
1206
V. R. FERRIS
plesiomorphic, and that the Avenae group
and Globodera simply retain the plesiomorphic condition (Fig. 6).
Table 3 lists only species for which I was
able to find the necessary data in the literature, but if my hypothesis has validity, all
other species known or yet to be discovered
can be incorporated. As falsifiers are found,
the hypothesis can be altered and improved. Information on cuticle structure is
a potential falsifier. Shepherd et al. (1972)
found that H. carotae (Goettingiana group,
Table 3) has cuticle similar to H. trifolii
(Schachtii group, Table 3) and my cladogram shows these groups joined by common
ancestor 3 +. However, H. cruciferae and H.
goettingiana (both Geottingiana group, Table 3) are said to be readily distinguishable from each other as well as from H. avenae. Moreover, the three latter species are
said to be readily distinguished from "the
Schachtii group" by characteristic cuticular
folds. These data may constitute falsifying
information for the Goettingiana-Schachtii
part of my hypothesis and the implications
need to be examined.
Another interesting problem is raised by
the research of Green (1975, 1976) who has
studied the mechanical factors affecting the
shape of cyst nematode females. Green
(1975) feels that primitive Heterodera sensu
lato probably had a long vulva. Although I
postulate a short vulva for my hypothetical
ancestor (Fig. 6), Sarisodera (to the left of
Heterodera on Fig. 4) does have a long vulva
as do other genera to the left of Sarisodera.
I suggest that with the development of
fenestration (thin areas in the vulval region believed to be necessary for extrusion of eggs from the tough cyst), the vulval
slit became short. In the Cacti + (Globodera + Punctodera) group, the fenestration is most fully developed (circumfenestration, see Fig. 5F) and the vulval slit remains short. The longer vulval slit in ancestor 5 of the more apomorphic groups on
the left of the cladogram of Figure 6 represents a secondary lengthening of a hinged
vulval slit (situated on a vulval cone) in the
absence of circumfenestration.
In summary, the cladograms of Figures 4
and 6 incorporate most of the available data
on cyst nematodes and reflect the observation of Brundin (1968) that every sister
group pair is a more or less complex manifestation of relative stasigenesis and relative anagenesis. I believe we now have a
basis for further meaningful analysis regarding the development of this important
group of nematodes in time and space.
Use of the cladistic analyses to understand the
historical biogeography of Heteroderidae
Phylogenetic evolution forms a sequence
of processes performed on species, and
thus there is an intimate connection between phylogenetic relationship and geographic distribution (Brundin, 1968). Sister groups often display allopatry or vicariism, and biogeographical analysis logically
follows a phyletic analysis (Nelson, 1969).
The traditional classic point of departure
for biogeography was to look for a center of
origin and to postulate how the organisms
might have dispersed from that center to
distant land masses, believed to be stable in
their positions relative to one another.
Coinciding with the discovery of plate tectonics by geologists, modern biogeographers (Croizat et al., 1974; Raven and
Axelrod, 1974; Ball, 1975; Cracraft, 1975;
Rosen, 1975, 1978; Platnick, 1976a,c; Platnick and Nelson, 1978) have developed an
alternative way of thinking about biogeography that has been one of the most exciting
recent developments in systematics, and
was the basis of our biogeographic study of
leptonchoids discussed above. Basically, the
method assumes an allopatric model of
speciation and considers sister groups to be
isolated descendants of an ancestral biota
which became subdivided in response to
some change in geography, which may have
been induced by climate, physiography or
tectonics. Changes in range of an organism
resulting from dispersal are believed to occur, but to be secondary in importance to
the vicariances which determine the initial
range. Sympatry of related forms is evidence of dispersal. Data indicate that vagile
and sedentary organisms have vicariated
similarly and the patterns of distribution of
both coincide with known paleogeographic
patterns (Croizat, 1962; Platnick, 1976a;
Rosen, 1978).
Worldwide patterns of distribution for
certain of the free-living soil nematodes are
"
CLADISTIC APPROACHES IN STUDY OF NEMATODES
probably the result of plate tectonic movements of continents, rather than chance
dispersal (Ferris, 19776; Ferris et al., 1976,
1978; and unpublished data). Many nematologists, however, seem reluctant even
to consider the possibility that similar patterns might be discovered for plant parasitic forms. The belief that movement of
nematodes by man and modern commerce
is entirely responsible for present widespread distributions of the economically
important cyst nematodes is widely held. A
center of origin is postulated, which is
either the crop area in which the species was
first discovered, or the area of origin of the
important crop plant species parasitized by
the nematode species. Some interesting and
speculative sequencies have been developed, buttressed by the finding of cysts in
the hold of a ship or on a burlap bag. The
possibility that the species might already be
present in the "new" area on weed species is
rarely considered. Indeed, prevention of
such introductions and enforcement of
quarantines has been an important and
costly enterprise. I do not deny the likelihood that man has moved cysts around to
cause new infestations, particularly locally,
but I would like to open the possibility of
considering alternatives to the accepted
model to explain distribution patterns.
The most speculation has revolved
around three important pest species or
groups of species. The first of these, the
potato cyst nematodes, were formerly thought
to be one species, but are now known
to comprise at least two (Globodera rostochien-
1207
other parts of the world (Winslow and Willis, 1972; Stoned al., 1977).
The cereal cyst nematode {Heterodera avenae) is still widely thought to be indigenous
to Northern Europe (where it was originally
detected in cereals in 1874) and disseminated by man as new lands were cultivated
(Meagher, 1977). It has been in Australia at
least since 1904 and is believed to have been
introduced there from Europe in the 19th
century.
Soybean cyst nematode was first reported
from soybeans in Japan in 1915, although
the symptoms of the disease had been
noticed since 1881 (and attributed to H.
schachtii, the sugar beet nematode which
had been discovered earlier in Germany
where sugar beet production was first developed). Soybean cyst nematodes were not
detected in North America until 1954 when
they were found in a soybean growing area
of North Carolina. Because the area was
also a bulb growing area it was postulated
that the cysts were brought to the U.S. A on
bulbs from Japan (Riggs, 1977).
Occasionally an infestation of a cyst
nematode species is discovered for which
no explanation can be derived. This was the
case with the first report in 1974 of cereal
cyst nematode in the U.S.A. on oats and
winter wheat (Jensen et al., 1975). The
species had been known for years to be in
Ontario, Canada, but absolutely no connection could be made between the disjunct
population of the infested Oregon farm
land (where it was also found in a nearby
woods) and the infested areas in Canada
(Jensen, personal communication).
Nematologists are hampered in the study
of biogeography because of incomplete
knowledge of the distribution of known
species. It is instructive even with present
knowledge to look at known distributions of
genera and species groups on the cladograms (Figures 4 and 6). The genera to the
left of Heterodera in Figure 4 are not generally found in cultivated fields, but rather in
natural areas on weed hosts. Nematologists
do not often study nematodes of weeds, so it
is remarkable that we know as much about
weed-feeding nematodes as we do.
sis and G. pallida). These species were first
discovered in Europe, where potatoes were
intensively cultivated. For many years
Europe was thought to be the center of
origin of the potato cyst species, but later it
was assumed that these species originated
in the Andean region of south America
where cultivated potatoes were discovered
and collected by European travelers (Green,
1971; Jones, 1972; Winslow and Willis,
1972; Evans et al., 1975; Mai, 1977). Potato cyst nematodes are now believed to
have been introduced to North America at
three different places including Long Island, N.Y. (detected 1941), Newfoundland
Meloidodera, Atalodera, Thecavermiculatus,
(detected 1962), and Vancouver Island (de- and Sarisodera have all been found in southtected 1965), and at various times to many western U.S.A. (Table 6). This may reflect
1208
V. R. FERRIS
TABLE 7. Summary' of distribution and host plants of species of Heterodera groups and of
Globodera and Punctodera listed in Table 3.
Group
Avenae
Host plants
Distribution
Laurasian*: 6spp. (Europe or Europe
+ U.S.S.R.)
Gondwanian (?): 1 sp. (India, Iran,
Libya, Greece)
Worldwide: H. avenae
Fici-humuli
Goettingiana
Schachtii
Gondwanian (?): 9 spp. (3 spp. India;
2 spp. Africa; 1 sp. Australia;
3 spp. Fla. orLa.,U.S.A)
Worldwide: H.fici (S. Africa,
Australia, U.S.A., U.S.S.R., Italy)
H. humuli (N. Am., EuroAsia, Africa, Australia, N. Zealand)
Laurasian: 4 spp. (Europe, U.S.S.R., +
1 also in U.S.A.)
Laurasian: 6spp. (4 spp. Europe;
1 sp. U.S.A.; 1 sp. U.S.A., Japan,
U.S.S.R.)
Worldwide: H. schachtii
H. trifolii
Cacti
Globodera
Laurasian: 4 spp. (3 spp. N. Am.;
1 sp. Eurasia)
Gondwanian (?): 1 sp. (Caribbean and
southern U.S.A.)
Worldwide: H. cacti (Eurasia, Japan,
Algeria, Israel, Argentina,
Australia)
Laurasian: 7 spp. (N. Am. or N. Am. +
Eurasia or Eurasia)
Worldwide: G. rostochiensis
G. pallida
Punctodera
(Eurasia, Japan, Peru, Argentina,
Chile, Venezuela, Columbia, Israel,
Tunisia, India, South Africa, New
Zealand, N. Am.)
Laurasian: 3 spp. (1 sp. N. Am. + Europe;
1 sp. Saskatchewan; 1 sp. Mexico)
5 spp.—grasses
1 sp.—Chenopodium
grasses
grasses
8 spp.—grasses
1 sp.—legumes
Urticales (Ficus)
Urticales (Humulis)
Mixed dicots: legumes,
Umbelliferae,
Criciferae, Urticaceae
3 spp.—legumes,
1 sp. —Labiatae; 1 sp.
— Polyganaceae; 1 sp.—
Plu mbaginaceae
Chenopodiaceae,
Cruciferae
legumes
1 sp. — Betulaceae
3 spp.—Chenopodiales
Chenopodiales
Chenopodiales
Solanaceae (1 group)
Compositae (Eurasia only)
Solanum
grasses
a
Based on the literature.
The terms "Laurasian" and "Gondwanian" in this table indicate present day distributions on continents or
land areas that were once part of the Laurasian or Gondwanaland supercontinents prior to the fragmentation
events diagrammed in Figure 3.
b
the habitat of the nematologists who
studied them! Meloidodera, however, has
also been reported from throughout the
U.S.A., from U.S.S.R., and from India; and
Cryphodera approaches a worldwide (panPacific) distribution. Hylonema was discovered in a native forest on the Ivory Coast of
Africa, and Sarisodera has also been found
in Africa. A vicariance interpretation would
suggest that the ancestor of Sarisodera and
the Hecterodera sensu lato (ancestor 5 +on
Fig. 4) was widely distributed on the Gondwanaland supercontinent prior to fragmentation. It may have even been present
in Pangaea prior to 180 m.y.b.p. (Fig. 3).
The data suggest that ancestor 1 (Fig. 4)
which gave rise to Cryphodera, and the ancestor of Meloidodera were in Pangaea. This
vicariance view assumes that future collecting and study will demonstrate the kinds of
relationships between Indian heteroderid
fauna and the heteroderid fauna of other
CLADISTIC APPROACHES IN STUDY OF NEMATODES
1209
land areas which resulted from the frag- appear to be quite similar, but there are
mentation of Gondwanaland (Fig. 3), that marked differences between these and the
we found for Leptonchoidea. Support for Australian form (Thorne, 1961; McLeod
the vicariance view, or falsification, andKhair, 1977).
will come from these future studies. If anBiogeographical analysis is also made
giosperms did not appear until the end of more difficult by the fact that nearly every
the Jurassic (Raven and Axelrod, 1974; species group on the cladogram (Fig. 6) has
Valentine, 1978), then plant parasitic one or more species (noted in Table 7)
nematodes arising earlier must have which seem to be worldwide in distribution.
parasitized some other kind of higher land If we assume for a moment that these displant, possibly a seed fern, and later shifted tributions are indeed the result of dispersal
to suitable angiosperm hosts. Cryphodera is by man and constitute potential "noise"
known to parasitize Eucalyptus, a member of (Platnick, 1976a) and we exclude these
the Myrtaceae, thought to have developed species from the analysis, then considera70 — 75 m.y.b.p. (Raven and Axelrod, tion of only the remainder of the species
1974).
reveals the following pattern 1) all species
A dispersalist alternative interpretation groups except the Fici-humuli group are
of present-day distributions is that migra- almost entirely in Laurasian countries, and
tion of the genera between southern and 2) members of the Fici-humuli group occur
northern hemispheres occurred via inter- on continents which resulted from the
mittent land connections across the Tethys fragmented Gondwanaland (Fig. 3). (The
Sea (separating Eurasia and Africa) in the three new-world species restricted to
Cretaceous and Early Tertiary (Raven and Florida or Louisiana, U.S.A., suggest a simiAxelrod, 1974). The occurrence of Cry- larity to the generalized tracks of Rosen
phodera in Australia and New Zealand, how- (1975) in which primarily southern Gondever, introduces problems with this expla- wanian biota are found in southern North
America and the Caribbean area.)
nation for Meloidodera and Cryphodera.
The biogeography of Heterodera sensu lato
If we now include data (Table 7) from the
is complicated by 1) the fact that we do not species we excluded as possible "noise" and
know the range of plant species (e.g., weeds) continue the vicariance hypothesis sugparasitized by a given nematode species, gested above for heteroderid genera, the
and 2) the knowledge that we cannot always following is suggested. The ancestor of the
trust the distributional reports in the litera- Heterodera sensu lato group was distributed
ture because of misidentifications. Misiden- on the supercontinent Pangaea. The Avtification occurs because identification is enae group developed on monocots, priinherently difficult, and also because we are marily in Laurasia; but it is possible that "H.
just now learning that what we used to con- avenae" will be shown to be a complex of spesider one species may indeed actually be a cies with Laurasian and Gondwanian comcollection of similar species. Careful anal- ponents. If future collecting and study of
ysis showed that two species of the Avenae relationships demonstrate that the Ficigroup (Table 3), H. hordecalis and H. lati- humuli group is indeed comprised of rempons, formerly thought to coexist in the nants of ancient populations that extended
same areas, are really geographically sepa- across Gondwanaland, whereas the Goettinrated (Sturhan, 1978 and personal com- giana and Schachtii groups are Laurasian,
munication), the former a northern species then a Pangaean ancestor for these groups
which occurs throughout Europe, and the (ancestor 5 in Fig. 6) is indicated. The two exlatter restricted to more southern areas in- ceptions in the Fici-humuli group which
cluding Libya, Israel, Greece, Iran, and In- have worldwide distribution (Table 7) are
dia. The potato cyst nematode, as noted both found on members of the Urticales, an
above, is now known to comprise at least early group (Raven and Axelrod, 1974). A
two species. Similarly, data reported for the conservative explanation of their distribucereal cyst nematode (H. avenae) suggest tion, which depends on early dispersal,
that it may actually comprise several spe- might be that they developed in Gondwana
cies. Specimens from Europe and Canada and moved into Laurasia across the
1210
V. R. FERRIS
Africa-Europe connection which existed
during the late Mesozoic-early Paleocene, a
route postulated for plant species by Raven
and Axelrod (1974). However, a subsequent study of the Fici-humuli group
might reveal that it should be subdivided
into two groups—one that developed early
in Pangaea, and another later in Gondwanaland. The Fici-humuli group seems to
have shared (with the Avenae group) the
genetic constitution to enable it to shift to
monocots.
It seems reasonable to postulate a Laurasian origin for the ancestor (parasitic on
dicots) of the Goettingiana and Schachtii
groups. The Goettingiana group is completely Laurasian. Two species of the eight
listed for the Schachtii group are worldwide
in distribution, and these are good candidates for transport by man from the native
Laurasian continents to southern areas.
The fact that//, trifolii is found in Hawaii is
evidence that would support this view,
based on our present state of knowledge.
(However, see Nelson's (1975) discussion of
the possible mesozoic roots for Hawaiian
biota, and the papers of Wouts (1978) and
Wouts and Sturhan (1978), on the heterogeneity of"//, trifolli") In any event, primary radiation of these groups has clearly been Laurasian.
On the right hand side of the cladogram,
Figure 6, the history seems to be similar,
with the ancestral form in Pangaea, followed by primary development in Laurasia.
Further study of H. cacti from different
areas may provide a plausible explanation
for the presence in southern areas of H.
cacti on wild species of the Chenopodiales
(a West Gondwana group according to
Raven and Axelrod, 1974). Heterodera
amaranthi which parasitizes Amaranthus of
Chenopodiales is found in Cuba and southern U.S.A, and, as noted for Fici-humuli
species, this distribution is reminiscent of
the generalized tracks of Gondwanian biota
of Rosen (1975). Three Laurasian species
are also found on plants of Chenopodiales.
Heterodera betulae (U.S.A.), placed in the
Cacti group by most authors, may provide a
key to further development of this part of
the cladogram. It is the only member of the
group with a non-Chenopodiales host list;
and it parasitizes Betulaceae, a Laurasian
family thought to exist by upper Cretaceous (Raven and Axelrod, 1974). Golden
and Raski (1977) comment on the fact that
cysts of H. betulae are rounded or pearshaped, with only a button-like protrusion,
a shape approaching that of Globodera and
Punctodera. In avicariance view the Cacti
group seems to consist of both Gondwanian
and Laurasian components.
Published data on Globodera and Punctodera might indicate that their ancestor (Fig.
6) was a Laurasian parasite of dicots. All
except the two potato cyst species are restricted to Laurasian areas, with one widespread group of Globodera parasitic on Solanaceae, and the other (restricted primarily
to U.S.S.R.) parasitic on various Compositae. {Punctodera is known only from
Laurasia areas and has shifted to Gramineae.) I am told, however, that another group
of Globodera species exists in South America
which parasitizes non-Solanaceous plants
including Oxalis of Oxalidaceae (P. Jatala,
personal communication). In a strict vicariance view this suggests a Pangaean ancestor
for the group, with Laurasian radiation of
the groups now restricted to Solanaceae
and Compositae. This view would be greatly strengthened by the finding of populations on Oxalidaceae in other geographic
areas of Gondwanian origin.
The vicariance hypothesis (which depends on the cladistic analysis) of the evolution of Heteroderidae in time and space is
amenable to testing. As falsifying evidence
is found, the model can be modified and
improved. An obstacle to our understanding has been our somewhat egocentric view
that the species we know from cultivated
crops evolved on the plant species we wish
to cultivate. The alternative view is that the
species evolved on wild relatives of our cultivated species and moved into the species
of interest to us as cultivation of these crops
became extensive and intensive. It is widely
assumed that the potato cyst nematodes
developed on the Solanum species we cultivate, which seem to have originated in the
Andes of South America. The Solanaceae,
including Solanum, however, have definite
Laurasian affinities, and seem to have been
represented in North America already by
taxa derived from Eurasia when other
floral elements arrived from South Amer-
CLADISTIC APPROACHES IN STUDY OF NEMATODES
1211
ica in the Pliocene (Raven and Axelrod, developed in the U.S.A. Data which cannot
1974). The tuber-bearing species probably be ignored include the fact that soybean
originated in the region of Mexico and cyst nematode was first discovered in the
southern U.S.A during late Cretaceous to Orient where soybeans were long an impor, early Tertiary times (Hawkes, 1958, 1972). tant cultivated crop. It was found in the
Movement of a Laurasian Globodera on wild U.S.A after soybeans became a major crop
Solanum species, southward to the Andes planted on 6.9 million hectares. The H.
across lower Central America (no earlier glycines from the Orient is slightly different
than the Pliocene), and development on the morphologically from the original (North
Solanum species in the Andes (with the sub- Carolina) U.S. population (Riggs, 1977). It
sequent development of resistant strains of is likely that soybean cyst nematode was
Solanum) makes more sense to me than the widely distributed in Laurasia, and surprevailing view. The vicariance interpreta- vived on weed hosts as a relict species until
tion provides a more satisfying explanation intensive and extensive cultivation of soyof the occurrence in Laurasian countries beans began in several areas. This hypothe(including North America) of so many sis is a more satisfactory explanation of the
Globodera species (Miller and Gray, 1968, frequent discovery of disjunct populations
1972; and L. I. Miller, personal communi- on soybeans in central U.S.A. (particularly
cation).
in fields which followed long years in weeds
This leaves unsolved the problem of the and wild lespedezas resulting from Federal
distribution of potato cyst nematodes of the Land Bank non-cropping agreements)
genus Globodera in India, South Africa and than is the notion that this species spreads
New Zealand, unless we assume they were like wild fire despite valiant efforts to recarried by man, which appears to be the strict its spread by quarantine.
case for New Zealand (Wouts, 1976). I suspect that comparative study of populations
CONCLUSIONS
from India and South Africa with the Globodera species from South America said to The foregoing hypotheses based on
parasitize non-Solanaceous plants as well as cladistic principles can be a point of deparpotatoes will be instructive. We can only ture for future research in the Heteroderiwait and see.
dae. New taxa as they are discovered can be
My hypothesis suggests an explanation added, and higher taxonomic categories
for the peculiar characteristics of H. avenae can be applied on the basis of something
(which may be a complex of species as dis- other than grade groupings. The much decussed above). As with other species, re- bated principle of Hennig (1966) that
ports of its occurrence follow intensive cul- groups which arose within a given time
tivation of favorable crops, but it appears segment in the history of the earth should
to be indigenous to many countries (Kort, be given the same absolute taxonomic rank
1972). The H. avenae populations in Aus- can probably be applied with relative ease to
tralia and India primarily parasitize wheat, the Nematoda because of their antiquity,
and may be a remnant of a Gondwana pop- relative simplicity, and conservative evoluulation. H. avenae is not known to be present tion (=reduced anagenesis) as compared
in the ancient centers of wheat production with other phyla such as the Arthropoda. In
in Asia Minor, which areas are of Laurasian fact, it is just these characteristics which I
origin. Furthermore, H. avenae can main- believe are responsible for the superior retain itself on many genera of wild grasses. sults which may be obtained in the
The behavior of//, glycines, the soybean Nematoda using cladistics rather than
cyst nematode, also is explained by my evolutionary or phenetic methods.
The continued study of known species or
hypothesis, which was anticipated by Riggs
(1977) who noted that//, glycines has many species groups in areas where they are
wild hosts. He suggested that one of these known and those where they are yet to be
hosts in North America may have carried discovered will contribute greatly to my
an endemic population which served as an hypotheses and be a source of valuable poinoculum source as soybean cultivation tential falsifying evidence. Moreover, the
1212
V. R. FERRIS
continued investigations (Krall and Krall,
1970; Stone et al, 1976) into coevolution of
host and parasite will be fruitful, as will
additional knowledge about the evolution
of host groups. The perils of transmigration of parasites between hosts, and of incomplete parallelism of speciation in host
and parasite groups, must be kept in mind;
nor should one assume that chemical and
serological analyses automatically give
more insight into phylogenetic relationships than other types of phenetic characters (Hennig, 1966).
That sister groups display spatial replacement is an assumption of cladistics. I
have suggested this for the Fici-humuli
group of Heterodera species and the Goettingiana + Schachtii groups. In fact, cladistics has been termed by several authors as
"the search for sister groups." Populations
of Heterodera sensu lato may be prime candi-
dates for sympatric speciation on new hosts
(Bush, 1975; Endler, 1977; Price, 1977;
White, 1978). This would result in local
phenomena similar to geographic spatial
replacement, which might be considered
ecological replacement, and would explain
the sympatric sibling species of Globodera in
North America and elsewhere. If so, it
would mean that in this group we can find
evidence of spatial replacement related to
plate tectonic events plus ecological replacement which is the result of the particular ecological strategy evolved by the Heterodera sensu lato group, in response to the
durational stability and resource level and
constancy of their habitats as discussed by
Southwood (1977). These ideas are amenable to testing and experimentation, and
their elucidation would help in further
development of my hypothetical model of
the evolution of the Heteroderidae.
The more tenuous parts of my hypothesis of relationship will be clarified by a more
precise knowledge of the species themselves, how they are distributed around the
world, and their weed hosts. In addition,
new geological discoveries will lead to
paleogeographic explanations of vicariances that now seem difficult to explain.
Certainly new information from the Caribbean area (Rosen, 1975, 1978; Raven and
Axelrod, 1975) will be welcome, as well as
information about early history of islands
of all kinds. I am particularly interested in
the suggestion of a Pacific land mass following the breakup of Pangaea, which might
provide a tectonic explanation for panPacific biotas (Croizat, 1958, 1962; Nelson,
1975; Martin, 1976; Nur and Ben-Avraham, 1977). Certain of the relationships in
Heteroderidae appear to conform to this
pattern.
It is my hope that the hypotheses suggested here will provide a point of departure for a new way of thinking about the
Heteroderidae and plant parasitic nematodes generally. I am aware of the shortcomings of my analyses, and only wish that I
had the knowledge to develop them more
completely. A complete theory is unattainable because we can never know everything,
but we can provide an up-to-date theory by
making it reflect our present state of knowledge as completely as possible (Nelson
1970). This is what I have tried to do.
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