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Faculty Publications from the Harold W. Manter
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Parasitology, Harold W. Manter Laboratory of
8-1989
The Phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela) The Phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela)
and General Evolutionary Principles and General Evolutionary Principles
Daniel R. Brooks
University of Toronto
, dnlbrooks@gmail.com
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Part of the Parasitology Commons
Brooks, Daniel R., "The Phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela) and General
Evolutionary Principles" (1989).
Faculty Publications from the Harold W. Manter Laboratory of
Parasitology
. 200.
https://digitalcommons.unl.edu/parasitologyfacpubs/200
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J.
Parasitol.,
75(4),
1989,
p.
606-616
?
American
Society
of
Parasitologists
1989
THE
PHYLOGENY
OF
THE
CERCOMERIA
(PLATYHELMINTHES:
RHABDOCOELA)
AND
GENERAL
EVOLUTIONARY
PRINCIPLES*
Daniel
R.
Brooks
Department
of
Zoology,
University
of
Toronto,
Toronto, Ontario,
Canada
M5S 1A1
ABSTRACT:
The
unified
theory
of
evolution is
an
expansion
of
Darwinian
theory
that asserts that evolution
is
driven
by
entropic
accumulation of
genetic
information that is
constrained and
organized primarily by
the
genealogical
effects of
phylogenetic history
and
developmental
integration,
and
secondarily by
ecological
effects,
or natural selection
in its
classical mode.
Phylogenetic
systematic analysis
of the 8
major groups
of
parasitic
rhabdocoelous
platyhelminths
permits
empirical
macroevolutionary
evaluation
of
these
postulates.
Of
the 131
characters
considered,
127
are
phylogenetically
constrained,
and
4
show
evidence
of
1
case
of
convergence
each.
Data
from different
developmental
stages
are
phylogenetically
congruent,
despite
differences
in
ecology among
those
stages. Ecological
diversification,
indicated
by
phylogenetic
association of
definitive hosts and
parasites,
and
by
changes
in
ecological components
of life
cycle
patterns,
is more
conservative
evolutionarily
than diver-
sification
in
developmental patterns,
indicated
by
the
appearance
of
unique
larval
stages,
asexual
proliferation
of
larvae,
polyembryony,
and
heterochronic
changes.
These observations
support
the
macroevolutionary
pos-
tulates
of
the unified
theory.
"The distinction between
fundamental
plesiomorphic
and
derived
apomorphic
characters is basic
for
any
consideration of
the
phylogeny
and
systematics
of
any
group-and
especially
so for
a
parasitic
group"
(Horace
W.
Stunkard,
1983,
in
litt.,
archives
of
the
H. W.
Manter
Laboratory,
Division
of
Parasitology,
University
of Nebraska State
Museum).
Host-parasite systems
often are considered
to
be
interesting
but unusual
examples
of evolu-
tionary
processes.
However,
Price
(1980)
re-
cently argued
that
parasites
could be
good
model
systems
for
studying
general
evolutionary
prin-
ciples.
A
currently
contentious
general
evolu-
tionary principle
is the unified
theory
of evolu-
tion
(Brooks
and
Wiley, 1988).
In
this
paper,
I
will
try
to show how
phylogenetic
analysis
of
a
group
of
parasites
can
help
examine
some of
the
macroevolutionary postulates
of the unified
the-
ory.
Price
(1980)
invoked a
widespread
view of
evolution
in his
studies of
parasite
evolution
when
he
asserted
that
the
evolutionary
"play"
took
place
on a
"stage" organized by
the environment
(an "ecological stage").
Under
this
view,
phy-
logeny
(evolutionary
history)
is
the
passive
ac-
cumulation
of
the effects
of
environmental
se-
lection
over time. The unified
theory
can
be
distinguished
from this
consensus
view
by
ex-
pressing
its
major
postulate
as environmental
se-
Received
17
January
1989;
revised 23
February
1989;
accepted
28
February
1989.
*
Paper
from
Stunkard
Centenary
Session of the
1989
annual
meeting
of the
American
Society
of Parasi-
tologists.
lection
being
the
"play"
that takes
place
on
a
"stage"
whose
organization
is
provided
by "phy-
logenetic
constraints" and
"developmental
con-
straints."
Phylogenetic
constraints is a
synonym
for
persistent
ancestral traits
that have not
evolved
rapidly enough
to be
affected
by
envi-
ronmental
selection
during any
given
episode
of
microevolutionary change.
Developmental
con-
straints is a
synonym
for
the
necessary integra-
tion
of
any
new
trait with the
rest
of
the
devel-
opmental
program
in
order to
produce
a viable
organism
that is then
potentially
acted
upon
by
environmental
selection.
The
unified
theory
is
not
non-Darwinian because Darwin
viewed
evolved
diversity
as
resulting
from
a combina-
tion of
phylogenetic,
developmental,
and
envi-
ronmental
effects,
although
his theories
did
not
result in
any
particular
expectations
about the
relative
contributions of
each
of those
classes
of
effects to
overall
evolutionary dynamics.
Neo-
Darwinian
evolutionary theory
has concentrated
almost
exclusively
on the role of
environmental
effects,
or
natural
selection,
in
evolution. The
unified
theory might
be viewed as an
expansion
of
neo-Darwinian
theory
to the
extent that neo-
Darwinism
attempts
to
reduce
all
biological
cau-
sality
to
environmental selection
operating
at the
level of
gene frequencies
in
populations.
As
a
606
BROOKS-CERCOMERIA
PHYLOGENY
607
result of
this
narrowing
of
focus,
research
tra-
ditions
that
originated
prior
to
the
establishment
of neo-Darwinism
often
incorporate
less reduc-
tionist
approaches.
As
I will
show, assessing
the
macroevolutionary
predictions
of
the
unified
theory
requires
a combination
of
systematic,
de-
velopmental,
and
ecological
data.
"Classical"
parasitology,
with
its
emphasis
on a
combination
of
systematics,
developmental biology,
and
ecol-
ogy,
is
one such tradition.
Because the
unified
theory
attempts
to
integrate
a
variety
of
influ-
ences
operating
at
different
rates,
and on
different
temporal
and
spatial
scales,
in
evolution,
it would
seem that
parasitologists
should
be
in a
strong
position
to offer
empirical
evaluations of
these
new ideas.
According
to the
unified
theory,
evolution
re-
sults from
an interaction
between
genealogical
and
ecological
processes.
Salthe
(1985)
and
El-
dredge
(1985,
1986)
have
termed these
the
ge-
nealogical
hierarchy
and
the
ecological
hier-
archy.
Ecological
processes
tend
to have
homeostatic
effects,
forcing
populations
into
equilibrium
conditions.
By
contrast,
the
genea-
logical
processes
are
viewed as
having
develop-
mental,
nonequilibrium,
or
diversifying
effects.
The
impact
of
phylogenetic
and
developmental
constraints
is
to slow
the natural
entropic
ac-
cumulation
of
genealogical
diversity,
providing
an
organized
but
dynamic
"stage"
upon
which
the
environment
can
be seen
as
acting
out
the
"play"
of natural
selection.
Natural
selection acts
to increase the
degree
of
organization
even
fur-
ther.
The
predominant
physical
manifestations
of
the interaction
between
genealogical
and eco-
logical
processes
differ
depending
on the
time
scale chosen
for observation
(Brooks,
1988;
Brooks
and
Wiley,
1988).
For
example,
on ex-
tremely
short time scales the
primary
manifes-
tation is
physiological
loss,
or
the
dissipation
of
heat
due
to
metabolic
activities.
On more inter-
mediate
time scales
the
primary
manifestation
is in
the accumulation
and
maintenance
of
bio-
mass,
evidenced
by
ontogenetic,
reproductive,
and successional
phenomena.
And on the
longest
time
scales,
the
primary
manifestation
is the ac-
cumulation
of
genetic
diversity.
The
longest
time
scale
phenomena
are
responsible
for
phyloge-
netic or
macroevolutionary
patterns (see
also
Funk and
Brooks,
1989).
According
to
the uni-
fied
theory,
phylogenetic
patterns
in
biology
should
have
predictable
properties.
These
prop-
erties occur
in
the form of
particular
correlates
of
phylogenetic
diversification
with
respect
to
phylogenetic
constraints,
developmental
con-
straints,
and
ecological
constraints,
discussed
next.
PHYLOGENETIC
CORRELATES
OF
THE UNIFIED
THEORY
Genealogical
hierarchy
The unified
theory
predicts
3
macroevolution-
ary
aspects
of
genealogical
processes.
First,
the
most
informative
evolutionary
summary
of
data
about similarities
among organisms
will result
from
the use
of
analytical
methods
that
maxi-
mize the
degree
of
phylogenetic
constraints
for
a
given
data set. Brooks
et al.
(1986)
demon-
strated that
phylogenetic
systematics
(Hennig,
1966)
is an
analytical
method that
conforms
to
this
prescription.
Further,
they
presented
an
in-
formation
theoretic
measure,
the
D-measure,
that
allows
one
to
discriminate
quantitatively
for a
given
set of
data
the
phylogenetic
tree that
has
the
greatest
information
content
about
phylo-
genetic
constraints.
Second, application
of
phylogenetic
systematic
methods to
data
derived
from
relatively
inde-
pendent
sources,
such as
ecological,
behavioral,
anatomical,
and
biochemical
characters,
will
re-
sult
in
highly
concordant
phylogenetic
trees.
This
area
of
research
is
known
as
"congruence
stud-
ies"
in
systematics.
An
excellent
example
of
phy-
logenetic
congruence
among
different data
sets
is the
study by
Hillis
and Davis
(1986),
who
demonstrated
congruence
among immunologi-
cal,
allozyme
electromorph,
ribosomal
DNA se-
quencing,
and
morphological
data for
North
American
ranid
frogs.
Finally,
the
necessity
for
developmental
inte-
gration
of all
evolutionary
innovations
means
that
phylogenetic systematic
analysis
of data
from
different
portions
of
the
developmental
program
(such
as larvae and
adults)
will
result
in
highly
concordant
phylogenetic
trees.
This
will
be
true
even
if
the larvae and adults have
markedly
dif-
ferent
ecologies
and habitats.
This has been found
to
be true
for the
relatively
small
number of such
studies that have been
performed
to date
(see
Brooks and
Wiley,
1988:
172).
Ecological
hierarchy
If
the
ecological
hierarchy
exerts
an
organizing
influence
by acting
as
a
homeostatic
rather than
developmental
force on
biological
systems,
the
unified
theory
predicts
that the
ecological
and
behavioral
(functional)
correlates
of
phylogeny
should be
conservative relative
to
the
morpho-
608
THE
JOURNAL OF
PARASITOLOGY,
VOL.
75,
NO.
4,
AUGUST 1989
logical
and
developmental
correlates
of
phylog-
eny.
Hence,
it
is
expected
that
most
closely
re-
lated
species
will
be
morphologically
distinct
from
but
ecologically
and
behaviorally
similar
to each
other and their common
ancestor.
In
addition,
suites of
ecological
and
behavioral
traits
for taxa
should
be
congruent
with the
phylogenetic
re-
lationships
derived from
structural
data,
such
as
anatomy
or
macromolecules.
This has
also been
found to
be true for
studies
performed
to
date
(see
Brooks and
Wiley
[1988:
338-340]
for ex-
amples
of
phylogenetic
constraints and
conserv-
atism
in
ecological
traits
for
free-living
taxa;
see
McLennan
et al.
[1988]
for
an
example
of
phy-
logenetic
constraints
in
behavioral
evolution).
Among
parasitic taxa,
a
high
degree
of conserv-
atism and
phylogenetic congruence
in
ecological
life
history
traits has been
documented
for
2
groups
of
copepods
parasitic
on
elasmobranchs
(Deets,
1987;
Deets and
Ho,
1988).
Interaction of
the
hierarchies
The
genealogical
hierarchy
exerts an
organiz-
ing
influence
on
biological systems
through
phy-
logenetic
and
developmental
constraints.
How-
ever,
because
increasing
diversity
and
complexity
is
an
entropic
phenomenon,
evolution
will
occur
despite
the
various
constraints
on its
expression.
That
is,
the
developmental
"rules"
of the
gene-
alogical hierarchy
appear
to
be
relatively
inde-
pendent
of,
and able
to
supersede,
the homeo-
static
"rules" of
the
ecological
hierarchy.
Therefore,
ecological
and behavioral
diversifi-
cation
should
lag
behind
developmental
and
morphological (including
macromolecular)
di-
versification on a
phylogenetic
scale.
THE CERCOMERIA:
A
TEST CASE
During
the
past
5
yr,
an extensive
phylogenetic
database for
the
cercomerians,
a
clade
containing
the
major groups
of
parasitic
platyhelminths,
has
been assembled
(Brooks
et
al., 1985a,
1985b,
1989;
Bandoni and
Brooks, 1987a, 1987b;
Brooks, 1989).
It
is
my
intention
to
show that
this
database,
including
additions
and modifi-
cations
to
come
in
the
future,
can be used
to
evaluate the
macroevolutionary postulates
of
the
unified
theory.
Phylogenetic
constraints
Brooks
et al.
(1985a)
performed
the
first
phy-
logenetic systematic
analysis
of the cercomerians
based on 39 anatomical
characters
that
had
been
used
previously by
workers
in
major
discussions
of
the
phylogeny
of
the
group.
The
resulting phy-
logenetic
tree
had a
consistency
index of
95%,
due to
2
postulated
cases
of
convergent
evolu-
tion. Brooks
(1989)
presented
an
updated
anal-
ysis
based
on a
total
of 120
characters.
The
re-
sulting
tree was identical
to the one
presented
by
Brooks
et al.
(1985a)
and
had
a
consistency
index
of
96.8%,
due to
4
postulated
cases
of conver-
gence.
That
study
demonstrated
a
high degree
of
phylogenetic congruence
between
anatomical and
ultrastructural
data
gathered
by
different
re-
search
groups.
Brooks
et
al.
(1985b)
presented
a
familial-level
phylogenetic
systematic analysis
of
the
Digenea,
based
on 158 characters
with a con-
sistency
index of
73.5%
(215
transformations
for
the 158
characters).
Brooks
et
al.
(1989)
reex-
amined
the
database
for
the
digeneans
and
their
sister
group,
the
aspidobothreans,
and
added
22
new
characters,
only
2
of
which showed
any
con-
vergence.
This
increased
the
database
for
the di-
geneans
to 180 characters
with
a
consistency
in-
dex of 75%
(239
transformations
for the
180
characters).
The
topology
of
the
phylogenetic
tree
presented by
Brooks et al.
(1985b)
was
not
al-
tered
by
the additional characters.
The
study
by
Brooks et
al.
(1989)
also
allowed
reconsideration
of
traits
relating
to the
phylo-
genetic relationships among
the
major
groups
of
cercomerians.
For
example,
Brooks
et
al.
(1985a)
and
Brooks
(1989)
assumed
that
the bifurcate
condition
of the
gut
in
digeneans
and
in
mono-
geneans
was
a
convergent
trait.
However,
Brooks
et al.
(1989)
demonstrated that available
data
supported
an
interpretation
that the
bifurcate
gut
is
also
plesiomorphic
for the
aspidobothreans.
This
being
the
case,
the
phylogenetic
interpre-
tation
is that
the bifurcate
gut
originated
in
the
ancestor
that
gave
rise to the trematodes
and
the
cercomeromorphs,
and has been
lost
in
more
highly
derived
groups
of
aspidobothreans.
This
actually
reduces
the number
of
homoplasious
characters
postulated
by
Brooks
(1989)
from
4
to 3 at
the
level of the
major
cercomerian
groups
(it
adds
1
homoplasy
to
analyses
of
relationships
within the
aspidobothreans
[see
Brooks
et
al.,
1989]).
In
addition,
the
presence
of
elongate
uteri
with
transversely
coiled
loops appears
to be
ple-
siomorphic
at the
same level.
The
presence
of
amphistomous juveniles
discussed
by
Gibson
(1987)
and
Brooks
et
al.
(1989)
is
plesiomorphic
for all cercomerians.
The orientation
of
the
pos-
teroventral adhesive disc
(the
cercomer
sensu
lato)
toward the ventral
surface rather
than
posteriorly
is
plesiomorphic
for the
cercomerians,
whereas
BROOKS-CERCOMERIA
PHYLOGENY
609
the
strictly
ventral
orientation
and
relatively
ses-
sile
nature of
the
cercomer
is
plesiomorphic
for
the trematodes.
Finally,
Brooks
et al.
(1989)
pre-
sented
a familial-level
phylogenetic
tree
for
the
aspidobothreans.
That tree
included
the
follow-
ing
traits
postulated
to
be
plesiomorphic
for the
aspidobothreans
as
a
group:
anteriorly
fused
suckers,
hypertrophy
and
linear subdivision
of
posterior
sucker
by
transverse
septa,
and
atrophy
of
the
oral sucker.
The
first
2
characters
replace
a
single
character
descriptor
of the
ventral
disc
of
aspidobothreans
used
previously
by
Brooks et
al.
(1985a)
and
by
Brooks
(1989).
The current
database
at this
level
of
phylo-
genetic
resolution
comprises
131
characters,
4
of
which
exhibit
1
instance
of
homoplasy
each,
giv-
ing
a tree
length
of
135 for
the
phylogenetic
hy-
pothesis (Fig.
1
and
following
synoptic
classifi-
cation);
therefore,
the
consistency
index
(CI)
for
this
database
is
97.0%
(131/135).
In
addition,
data
from ultrastructural
and
light
microscopical
anatomical
sources,
and
from life
cycle
studies,
support
the
same
relationships
whether
consid-
ered
separately
or in combination.
These
findings
suggest
a
high
degree
of
phylogenetic
constraint
in
the
data as
a whole.
If
Figure
1
does
not
rep-
resent
the
phylogenetic
relationships
among
these
taxa,
we
must
explain:
(1)
why
the
characteristics
of
these
ecologically
and
developmentally
di-
verse
taxa are
so
well
organized,
and
with
respect
to what
they
are
organized,
and
(2)
if
97%
of the
evidence
suggests
an
incorrect
pattern,
how "cor-
rect"
evolutionary
patterns
are
discerned
in
a
scientific
manner.
The unified
theory
explains
such
a
high
degree
of
organization
by
suggesting
that
the
pattern
shown
in
Figure
1
represents
the
phylogenetic
relationships
of the taxa
and that
similarities
among
taxa are
due
more
to the
ef-
fects
of shared
ancestry
(phylogenetic
con-
straints)
than
to
the
effects
of individual
ecolo-
gies.
A
synoptic
phylogenetic
classification
of the
major
groups
of
parasitic
platyhelminths
follows,
modified
from
that
given
by
Brooks
(1989),
with
diagnoses
based
on
the additions
and
changes
to
the database
discussed
above.
The
diagnoses
are
lists of
traits
that are
hypothesized,
on the
basis
of
outgroup
comparisons,
to
have
characterized
the ancestor
of
each
group.
Shared
primitive
con-
ditions
are
not
listed, except
at the
base
of the
tree,
where
the exact
relationships
among
the
members
of
the
paraphyletic
Dalyellioidea
(used
as a
composite
outgroup)
are
not well
known.
Hence,
some
of the
traits
listed at
that
level are
II
III
IV
V
VI VII
VIII
FIGURE
1.
Phylogenetic
tree
depicting
relationships
among
the
major
groups
of
cercomerian
platyhel-
minths.
I
=
Temnocephala;
II
=
Udonellidea;
III
=
Aspidobothrea;
IV
=
Digenea;
V
=
Monogenea;
VI
=
Gyrocotylidea;
VII
=
Amphilinidea;
VIII
=
Eucestoda.
Numbers
accompanying
the
slash marks
refer
to
the
number
of
putative synapomorphies
supporting
each
branch
(refer
to
synoptic
classification
in
text
for
iden-
tities
of each
synapomorphy).
Each asterisk
(*)
repre-
sents
a
putative
homoplasy
(also
indicated
in
synoptic
classification
in
text).
undoubtedly
symplesiomorphies
for the
cerco-
merians
plus
other
"dalyellioids."
Homopla-
sious
characters
are
indicated
by
an asterisk
(*).
The
total
number
of
apomorphic
traits
for each
group
is reflected
in the
number
accompanying
the
appropriate
branch
in
Figure
1.
Traits that
have been
modified
from
the condition
diag-
nostic
for each
group
are
not listed either.
Such
modifications
are detected
by phylogenetic
sys-
tematic
studies
at levels of
greater
resolution
(e.g.,
Brooks
et
al.,
1985b,
1989;
Bandoni
and
Brooks,
1987a,
1987b).
The
nomenclature
represents
a
compromise
between
that
used
by
2
groups
of
phylogeneticists
(see
Brooks, 1989).
I
believe
it
is
compatible
with
nomenclatorial
traditions
at
the
ordinal
level
and below
for
most
groups
of
parasitic
platyhelminths.
Synoptic
classification
of the Cercomeria
Subphylum
RHABDOCOELA
sensu
Ehlers,
1984
Infraphylum
TYPHLOPLANOIDA
sensu
Ehlers,
1984
Infraphylum
DOLIOPHARYNGOPHORA
sensu
Ehlers,
1984
Superclass
CERCOMERIA
Brooks,
1982
Diagnosis:
(Doliiform
pharynx
and
reduction
of
the
dual-gland
adhesive
system
indicate mem-
bership
in
Doliopharyngophora.)
Rhabdocoe-
lous
platyhelminths
lacking
a
vagina
(1);
with
single
ovary
and
paired
testes
(2);
with
paired
1