Download Relationships Between Invertebrate Phyla Based

AMER. ZOOL., 21:63-81 (1981)
Relationships Between Invertebrate Phyla Based on
Functional-Mechanical Analysis of the
Hydrostatic Skeleton1
WOLFGANG FRIEDRICH GUTMANN
Forschungs-Institut Senckenberg, 6000 Frankfurt am Main, W. Germany
SYNOPSIS. The phylogeny of the major groups of deuterostome coelomates—the chordates, hemichordates and echinoderms—is discussed based on a mechanical-functional
analysis of the hydrostatic skeleton and associated structures. The basic approach is to
first establish transformation series of individual features and of functional complexes of
features and second to determine their "Lesrichtung" by showing the direction of increased economy (i.e., better adaptation) with respect to environmental factors. It is argued that a metameric coelom is primitive with respect to an oligomeric one and that the
ancestral form of the deuterostome coelomates is a metameric, coelomate worm-like animal with a complex set of circular, transverse and longitudinal body muscles. The coelom
plus the complex body musculature formed the hydrostatic skeleton. The sequence of
structural modifications leading to chordates is: (a) appearance of the notochord; (b)
specialization of the dorsal longitudinal muscles with a reduction and disappearance of
the transverse and circular muscles; (c) simultaneous appearance of the dorsal hollow
nerve cord; (d) development of a postanal tail; and (e) appearance and specialization of
the branchial basket with gill slits as a filter feeding apparatus. The primitive chordate
would be most similar to the lancelet (Acrania). Tunicates are advanced chordates specialized for sessile life and lost most chordate features in the adult, but retained them in
the larvae as adaptations for active dispersal. Enteropneusts (acorn worms) are another
advanced group specialized for burrowing in fine sediments and that evolved the anterior
proboscis as a peristaltic burrowing organ. The notochord was lost as was the dorsal nerve
cord and segmented condition of the coelom. A collar originated as a means to prevent
discharged water from re-entering the mouth. Pterobranchs arose from enteropneustlike forms; their major structural changes are reduction of the branchial basket and modification of the collar into tentacles which are associated with life in a closed tube. Finally,
echinoderms arose from a pterobranch-like ancestor by specializing for sessile life and
feeding with tentacles and by final loss of the branchial basket. Groups such as the tunicates, hemichordates and echinoderms could be eliminated as ancestral forms within the
deuterostome coelomates because the evolution of acraniates and vertebrates from each
of these groups would involve the appearance of gill slits before the notochord and/or
the evolution of a metameric coelom from an oligomeric one, both of which are exceedingly improbable. Central to the methods used to establish the transformation series of
features and their direction of evolutionary change (Lesrichtung) are functional (mechanical) analysis and adaptive interpretation of features; hence, functional-adaptive analyses are an integral and essential part of the methodology of phylogenetic investigation.
INTRODUCTION
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the hydrostatic skeleton and on the evoThe phylogenetic relationship of the l u d o n o f t h e c o e l o m i n c l u d i n g t h e q u e s .
phyla and subphyla of animals has been d o n o f t h e pri mitiveness of the metameric
the focus of active research ever since the a r r a n g e r r i e n t of coelomic cavities, I underpubhcationofthe Origin of Species, but t o o k a research project with the cooperawith almost no consensus of opinion de- d o n o f s e v e r a l coll eagues at the Senckenyeloping. Moreover, no methods existed .
Museum (K. Bonik, T. L. Franzen, M.
for choosing in any convincing way be- G r a & s s h o f f ) D . Mollenhauer, D. S. Peters;
tween the various conflicting phylogenetic t h e r e s u k s a r e p r e s e n t e d i n Schafer, 1973,
hypotheses for the invertebrate phyla. Us- 1 9 7 5 i g 7 6 , g 7 8 ) w k h t h e m a j o r
,s o f
ing ideas on the functional properties of e s t a b l i s h i n g m a j o r me tazoan groups and
elucidating their phylogenetic relationships. The basic assumption underlying
'From the Symposium on Functional-AdapUveAnal- ^
ysts in Systematics presented at the Annual Meeting or
the American Society of Zoologists, 27-30 December
1979, at Tampa, Florida.
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lutionary
changes are gradualists and adaptive as
advocated by Simpson (1953) and Bock
63
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64
WOLFGANG FRIEDRICH GUTMANN
(1979) and that a functional-adaptive analysis, as outlined by Bock (1981) in this symposium, is needed in addition to other pertinent evolutionary analyses. Because the
morphological systems used to inquire into
the phylogenetic relationships of the metazoan phyla operate as mechanical ones, it
is essential to use physical laws of mechanics in the functional analysis. Soft bodied
invertebrates possess a hydrostatic skeleton; hence, the physics of hydrostatic systems is needed for the functional analysis
of the skeleto-muscular system of these animals. A last requirement, stemming from
the demands of investigating hydrostatic
skeletons and from general theoretical
considerations advanced by workers as
Dullemeijer (1974), is that the organism
must be studied as a functional whole.
Complete, enclosed structural systems
comprise the functional units of hydrostatic skeletons and are, therefore, the prerequisite units of analysis. Conclusions
about evolutionary changes in one feature
should be made against a background of
the evolutionary modifications and functional properties of the entire complex.
With the use of these principles, my colleagues in Frankfurt and I developed a
new concept for the phylogeny of metazoan phyla and, more importantly, a method for testing the validity of the varied hypotheses available in the literature. In this
paper, I would like to present the central
ideas of our approach using an abridged
analysis of the phylogeny of the deuterostome coelomates as an example. More details my be found in Gutmann (1966, 1967,
1969, 1971, 1972, 1975, 1977); Bonik
1977/78); Gutmann and Bonik (1979);
Bonik et al. (1976, 1977a); Bonik et al.
(1978); Gutmann et al. (1978); Vogel and
Gutmann (unpublished).
BLOMECHANICAL PROPERTIES OF THE
HYDROSTATIC SKELETON
All chemical and physical properties of
life are associated with and tied to liquid
solutions enclosed in membranes. Because
of this inseparable concurrence, every living organism is inevitably a hydrostatic
skeleton construction. In metazoans, the
multitude of cells is aggregated into complex systems mechanically supported by
connective tissue formed in the interstitial
spaces. The metazoan constructional system must not be interpreted as simple aggregations of cells whose functional properties are the sum of the functional
properties of the cells because the mechanQ
ical intactness of the metazoan body is not
provided solely by cells. Every metazoan
has a complex configuration of extracellular mechanical structures (gels, fibers,
etc.) secreted by cells. The organization of
these extracellular materials and their interactions with the cells forms the basis for
the mechanical properties of the metazoan
body. In many (or all) primitive metazoans, the skeleton is built on a grid of connective tissue fibers surrounding the fluidfilled cells (Bonik et al., 1977a). The whole
system may be braced further by internal
muscles or incorporated into a coatlike
muscular and connective tissue sheath.
Muscles are always attached to the connective tissue structures forming a continuous
lattice throughout the entire body of the
metazoan animal.
Unless deformed by internal or external
forces or supported by bracing structures,
fluid filled constructions possess a strong
tendency to assume a globular form. This
shape is, if very few exceptions are permitted, inappropriate for the fulfillment of
useful organismic activities, especially locomotion. For greater efficiency, the vast
majority of biological activities depend on
a body shape other than that of a sphere.
For most lower animals, movement depends on a controlled deformation of the
body. The network of braces formed by
muscular bands and/or of sheaths of muscular and connective tissue structures provide the necessary control of body deformation and form an indispensable
precondition for almost all useful biological activities in soft-bodied metazoans.
All lower animals lacking a rigid skeleton move by deformation of the whole
body; the only exception is those forms
propelled by ciliary strokes. Locomotion
by peristaltic waves and swimming by sinusoidal movements are dependent on the
hydrostatic skeleton and can be most efficiently executed by elongate, bilateral animals, e.g., worms. As a consequence of the
biomechanical properties of the hydro-
PHYLOGENY OF DEUTEROSTOME COELOMATES
static skeleton, which was possessed by the
first metazoans, and the demands of locomotion in a fluid environment, a wormlike body shape evolved in the earliest freeliving metazoans. This body construction
^presumably evolved several times independently if free-living metazoans arose several times. The evolution of a worm shape
is governed by the environmental demands and the structural (mechanical) and
functional (physiological) requirements of
the metazoan body construction.
Compared to the efficiency of typical
rigid skeleto-muscle systems, i.e., those
with a hard, nondeforming skeleton found
in most higher animals, all hydraulic constructions have a relatively poor locomotory performance. The low level of economy results from the need to use actively
all muscular support of the body to prevent deformations that would hinder or
prevent locomotion. Unlike the action of
muscles in rigid skeletal systems in which
much of the generated force contributes
directly to moving the body, a great proportion of the muscles in a hydraulic system cannot contribute directly to propulsion. Movement in metazoans with
hydrostatic skeletons is brought about by
the indirect activity of the entire body musculature which generates pressure on the
fluid filling, thereby making it rigid and
preventing undesired deformations of
body shape. The force produced by a small
part of the active body musculature contributes directly to moving the body at any
time. Improvement of locomotory efficiency in organisms with rigid skeletons
compared to those with a hydrostatic skeleton is usually achieved by the elimination
of those muscular components which do
not contribute directly to locomotion, but
are necessary for maintenance of the hydrostatic skeleton. This reduces the mass
of muscular tissue in the organism {i.e.,
lessens the total mass that has to be moved
during locomotion) and the amount of
metabolic energy required by the muscular
system during locomotion. The result is increased efficiency measured in terms of
amount of energy required to move similar sized animals.
65
tems. Their basic structure is a muscular
and/or fibrous sheath surrounding completely a fluid filling. The outer coat may
contain circular and longitudinal muscles
or longitudinal muscles alone. Additional
bracings of transverse muscles may be
present. The fluid filling may be composed
of a gel from soft (jelly) to stiff consistency
(Bonik et al., 1977a), a liquid-filled sac
(e.g., a coelom) (Chapman, 1958; Gutmann, 1960, 1966, 1967; Clark, 1964,
1979; Trueman, 1975), muscles (e.g., the
mammalian tongue or the cephalopod
arm), etc. These systems vary in properties
such as stiffness and in overall efficiency.
Liquid filled sacs have several advantages
over other hydrostatic skeletal structures,
e.g., soft gels. Evolution of internal cavities
in animals (e.g., coeloms, pseudocoels) has
almost certainly occurred under the action
of selection for a more efficient hydrostatic
skeleton associated with better abilities of
locomotion.
SEGMENTATION OF THE COELOM
Fluid-filled body cavities (coeloms, pseudocoels) occur in two basic forms, the metameric condition and the oligomeric condition. A metameric coelom is one in which
the body, and hence the coelom is subdivided into a large number of units by muscle-bearing transverse septa—the dissepiments—which meet the mesenteries in the
sagittal plane and suspend the gut. Other
organs, e.g., the nephridia, are associated
with the transverse septa. An oligomeric
coelom is one in which the body cavity is
undivided or divided into two or three
large cavities. Transverse septa are lacking; and hence the gut is suspended only
by midsagittal mesenteries. A major difference between the metameric coelom
and the oligomeric coelom is that in the
former, the hydrostatic skeleton in the different body segments can act independently of one another while in the latter,
the hydrostatic skeleton of the whole animal acts as a single unit. Furthermore the
transverse bracing allows additional control of the cross section of the body which
is automatically circular in hydraulic systems lacking an internal bracing.
Hydrostatic skeletons may be achieved
A major question in invertebrate phyby several different morphological sys- logeny is whether the metameric coelom
66
WOLFGANG FRIEDRICH GUTMANN
or the oligomeric coelom represents the
primitive condition in the evolution of
body cavities. Most workers (Siewing,
1972; Reisinger, 1973; Remane, 1973)
have postulated that the oligomeric condition is primitive because it has a simpler
morphology in comparison to the morphologically more complex metameric condition. Evolution from the primitive oligomeric coelom to the advanced metameric
condition would involve the appearance
and gradual enlargement of transverse
septa subdividing the coelom and the appearance of transverse muscles in these
septa. Additional features would have to
evolve in a segmented arrangement, such
as the nephridia which are associated with
the dissepiments and whose tubules usually extend from one body cavity to the
next through the wall of the dissepiment.
The conflicting theory is that the metameric coelom is the primitive condition.
The transverse septa with their transverse
muscles and structures such as the nephridia are present in the acoelomate jelly
supported animal. The internal cavities
appear between the septa and enlarge until successive cavities meet at the preexisting septa, transforming them into muscular dissepiments. Evolution to the advanced
oligomeric condition would occur by the
gradual reduction and disappearance of
the transverse muscles and the dissepiments.
Both hypotheses must be tested by providing, among other arguments, a functional-adaptive analysis for the postulated
morphological changes from the suggested primitive condition to the advanced
one, using the assumption that the evolutionary changes are gradualistic ones (Peters and Gutmann, 1971; Schafer, 1973,
1975, 1976, 1978; Bock, 1979). Possible
reversal of evolutionary change must also
be considered (Gutmann, 1976; Bonik et
al., 1977ft; Bock, 1979).
Origin of the metameric coelom from
the acoelomate condition is postulated to
be by a segmental series of body cavities
within the gridwork of muscles gradually
replacing the jelly and/or parenchymal filling of the body. The existing transverse
muscular bands were condensed between
neighboring coelomic cavities and became
associated with the double-walled transverse mesentery formed when the epithelium of adjoining cavities pressed together.
These transverse muscles continued their
role of maintaining body shape (GutmannjJ
1972; Bonik et al., 1977a). They now
served, in addition, to isolate the individual parts of the segmented hydrostatic
skeleton characteristic of the metameric
coelom (Clark, 1964, 1979). Evolution
from the metameric to the oligomeric coelom involves the disappearance of the dissepiments and their transverse muscles.
This can occur in gradual steps with the
appearance of holes in the transverse septa
by which fluid can move from one coelomic cavity to another. Enlargement of
these holes would increase movement of
fluid from one cavity to another and equalize pressure throughout the entire coelom.
Evolutionary modification from a complete metameric condition to a fully oligomeric coelom can easily be conceived as a
series of gradualistic steps as the change is
a loss of existing features. An oligomeric
coelom is characteristic of metazoans in
which locomotion is reduced or in which
the hydrostatic skeleton had been replaced
by a rigid skeleton; in both cases a hydrostatic skeleton consisting of a series of separate liquid filled sacs is no longer advantageous.
Origin of an oligomeric coelom would
be by the appearance of fluid-filled sacs,
but these would enlarge and merge into a
single large cavity within the body. The lining epithelium of individual coelomic sacs
would break down wherever they merged
resulting in the joining of separate cavities
upon meeting. Existing bands of transverse muscles in the acoelomate ancestor
disappear in the primitive oligomeric
metazoan. Although an oligomeric coelom
could serve as a hydrostatic skeleton, it is
less advantageous than that formed by a
metameric coelom because the entire body
acts as a single unit. Although the fully
developed oligomeric coelom can serve as
a hydrostatic skeleton, the intermediary
stages in its evolution cannot be reasonably
explained. Locomotion in worm-like organisms depends on a homogeneous body
PHYLOGENY OF DEUTEROSTOME COELOMATES
67
structure over the whole length. Emer- ties operate only when the septa are comgence of few fluid-filled cavities would plete. I know of no other functional prophave produced very heterogeneous seg- erties and associated selection forces which
ments which would have functioned to- could be responsible for a gradual evolugether as an integral unit with difficulty, tion of the dissepiments from an ancestral
win addition, evolution from the oligomeric oligomeric condition. Unless one is willing
to the metameric coelom requires the for- to accept the possibility of a single step salmation of segmental transverse septa, tatory evolution of complete dissepiments,
transverse muscles and associated segmen- an adaptive gradual evolution of the metal features as the nephridia which have a tameric coelom from the oligomeric coecomplex relationship with the transverse lom appears highly improbable.
dissepiments. The segmental arrangement
Several conclusions may be offered:
of the septa must be regular for greatest
efficiency. Considering only the septa and a) The metameric coelom is primitive and
the oligomeric coelom is advanced in
transverse muscles, serious problems exist
coelomates.
for a gradualistic explanation of their apb)
The oligomeric coelom can evolve
pearance in an oligomeric coelom and of
gradually and adaptively from the
their evolution to the metameric condition
metameric coelom by loss of the dissep(Clark, 1964, 1979; Mettam, 1971; Schafer,
iments and transverse muscles, but the
1973). The important function of the
reverse change is highly improbable.
transverse septa is to subdivide the coelom
into separate hydraulic chambers; this c) The oligomeric coelom probably
evolved independently in several groups
works only when the septa are complete.
of metazoans.
No functions and adaptive advantages
have been suggested for incomplete septa
and for the adaptive evolution from ruEVOLUTION OF CHORDATE FEATURES
dimentary septa to complete ones. TransAmong the coelomate metazoans is a
verse muscles must evolve from existing complex of groups known as the deuterosets of muscles and it is difficult to explain stomes which include the hemichordates,
the origin of transverse muscles from ex- tunicates, acrania, vertebrates and echiisting longitudinal or circular muscles. noderms. A strong consensus exists that
Moreover transverse muscles must extend these taxa form a monophyletic group
across the body to function properly, i.e., within animals, but little agreement exists
they must attach to resisting structures at on the phylogeny within the deuteroeither end and actively contract during the stomes. I would like to present a model for
life of the individual organism. Nonfunc- the evolutionary origin and subsequent
tioning muscles atrophy rapidly during the change for the major features in this
life of an individual. Transverse muscles group and to compare this model with othwould possess little or no functional or er hypotheses. Because I believe that the
adaptive significance in a rudimentary sep- chordates are the primitive stock of these
tum. Lastly, the set of transverse muscles deuterostomes, I will be concerned with
must be well developed in the fully formed the evolution of the major chordate feadissepiments if the transverse septa are to tures. These will be discussed in the seisolate the coelomic cavities into indepen- quence of their presumed evolutionary ordent hydraulic units.
igin.
The deuterostome coelomates evolved
The transverse dissepiments are complex morphological systems of coelomic from a worm-like acoelomate ancestor posepithelium, transverse muscles, nephridia, sessing a hydrostatic skeleton consisting of
etc. which had to evolve as a unit. They a complex, dense muscular grid (longitucould not evolve adaptively and gradually dinal, circular and transverse) surroundunder the control of selection forces asso- ing a gel filling. The metameric coelom
ciated with properties of the metameric developed from inflated regions of a canal
coelom because these functional proper- system with the newly developed coelomic
68
WOLFGANG FRIEDRICH GUTMANN
FIG. 1. Model of the hydraulic body construction in coelomates. The emergence of fluid-filled cavities in
lower animals required the preceding existence of jelly-like support of the body frame, a situation well known
from ctenophora. Jelly-like connective tissue was the mechanical condition for the functioning of muscles and
the precondition for the formation of canals by which digestion and distribution of food could be effected.
A. Bending movements serving for improved food uptake into the canals could gradually change into locomotion by bending movements.
B. The elongate worm shape (the stages are depicted in a shortened form) is mandatory for all possible
locomotor activities because it compensates momenta generated by the movement of one body region by
counteractions of other segments.
C. Enlargement of some portions of the canal system provided fluid-filled spaces that reduced the rigidity
of the jelly and resulted in the formation of fluid-filled hydraulic constructions.
D. The muscular grid enforcing control of the elongate body shape permitted the emergence of many small
fluid-filled cavities. Thus metamerism of the coelomic cavities was the result of the biomechanical requirements of the system.
E. The enlargement of canal portions in the lateral position offered maximal benefit for worms swimming
by horizontal bendings because of the reduction of rigidity in the flanks which are subject to maximal
deformations. The nephridial canals of metameric coelomates are explained as remains of the ancestral
canal system.
F. The chordate is characterized by a flexible fluid-filled rod, the notochord (Cd), that keeps the body
constant in length.
cavities fitting into the muscular grid (Fig.
1A-C). These chambers were arranged
lateral to and around the gut and developed along the length of the body (Bonik
et ai, 1977a). The lateral position of the
paired coelomic cavities provide support
against lateral deformations of the body
and indicate the importance of improving
the hydrostatic skeleton with respect to lateral bending of the body—the use of lateral waves for locomotion. Formation of
coelomic cavities as a series of small chambers within the existing muscular grid
along the entire length of the body was
necessary to preserve a homogenous hydrostatic skeleton throughout the body
during the evolutionary transformation
from a gel-filled to a fluid-filled hydrostatic
skeleton. Evolution of the coelom by large
widely spaced fluid-filled sacs separated by
regions of gel filling would result in a heterogeneous hydrostatic skeleton in the animal. An elongated animal with such a heterogeneous hydrostatic skeleton—regions
of large liquid-filled cavities separated by
wide areas of gel filling—would have a dis-
PHYLOGENY OF DEUTEROSTOME COELOMATES
advantage because the properties of these
two systems differ greatly and it would
be difficult to integrate them into a single
functional unit. Consequently the coelom
evolves in a metameric fashion leaving inWact the muscular control of the body.
The primary advantage obtained by the
formation of the metameric coelom is the
decrease in stiffness in the body construction when the gel filling is replaced by segmental fluid chambers. The skeleton remains a hydrostatic one dependent upon
the action of the entire body musculature
for maintaining the skeleton during locomotion and hence remains at a low level of
efficiency. A gel-filled hydrostatic skeleton
permits the animal to crawl on the substrate or swim, by sinusoidal waves, in a
fluid; however, burrowing in soft, finegrained sediments is not possible. The lateral position of the coelom indicates its
adaptive advantage in an animal locomoting with lateral bends of the body. Once
the coelom became fully developed, the
animals could burrow in soft, fine-grained
sediments. So the evolution of the coelom
and its metamerism in burrowing organisms as sometimes suggested (Clark, 1964,
1979) is highly improbable.
Evolution of the coelom was the first
step in the evolution of features in the deuterostome coelomates from their acoelomate ancestors (Fig. 1D-E). The animal at
this point would be an elongated worm
with a metameric coelom and a complete
set of body musculature (i.e., transverse,
circular and longitudinal). Although the
main locomotory performance might have
been swimming, these forms could burrow
as well as creep on the substrate. Reduction of stiffness in the lateral direction
leading to more efficient locomotion appears to be the adaptive significance of this
step.
The second step is a continuation of the
first in that the adaptive significance is further increase in efficiency of locomotion.
The important change was the evolution
of a stiff rod—the notochord—dorsal to
the gut as the major axis of support for the
body (Fig. IF). Although the notochord
operates as a hydrostatic skeleton, it is intermediate between hydrostatic skeletons
69
FIG. 2. Upper stage: biomechanical preconditions
for the development of the notochord lie in the existence of transverse dissepimental bracings of a metameric worm. Dissepiments prevent bending of the
body axis within the body cavity. Lower stage: the
consequences of lacking dissepiments is shown in the
worm-like organism in which the notochord would
be useless because it could not contribute to the maintenance of the body length.
formed by fluid filled sacs and rigid skeletons formed of cartilage or bone. It has
several advantages over a coelom as a body
skeleton. First, it is smaller and requires
less space within the body, being composed
of cells filled with a stiff gel and surrounded by a heavy fibrous sheath. Second, it
does not require the action of the body
musculature to maintain its constancy of
body length.
Prior to the evolution of the notochord,
the animal could locomote by sinusoidal
undulations in which the body is held constant in length by the circular and transverse muscles and by peristalsis in which
the length of the body changes by the alternate contraction of the longitudinal and
circular muscles. With the evolution of the
notochord, body length is held constant by
this rod and movement by peristalsis is entirely eliminated (Fig. 2).
Evolution of the notochord is dependent
upon the presence of the transverse dissepiments. These structures support the
notochord in its position dorsal to the gut
and prevent it from bending within the
animal. Basically the dissepiments anchor
the notochord to the system of body musculature which is an essential requirement
if the notochord serves as the central, noncompressive support of the body. If the
70
WOLFGANG FRIEDRICH GUTMANN
FIG. 3. Phylogenetic model for the evolution of the chordate body construction starting with a worm-like
metameric organism.
A. Metameric coelomate equipped with paired coelomic cavities (C) which are integrated into the three
dimensional muscular grid. The whole system works as a hydrostatic skeleton. Shape control is exerted
by the muscular bracings. The gut (D) is suspended in the mesenterium (Me) and held in its position by
transverse muscles bearing tissue sheets (Dis).
B. The notochord (Cd) arises above the gut in the muscle-connective tissue grid of the mesenterium. The
fluid filling in the emerging notochord is held in its position. The muscular and connective tissues controlling the shape of the notochord aid the muscular bracing in ensuring constancy of length while the
worm swims by lateral undulations.
C and D. As the function of the notochord to ensure constancy of length is improved, the circular muscles
of the muscle coat of the body wall and the transverse muscles of the dissepiments are reduced. The
dissepiments persist as connective tissue sheets (My) which connect the strengthened longitudinal muscle
packages to the body axis.
E, F and G. Deepening mouth slits allow water to flow out of the mouth after being used for filtration. The
gill slits of the branchial basket (Ks) develop by subdivision of the slits by dorsoventral bars. This is
necessitated by the weakening of the body flanks.
H. Typical chordate construction as represented in the acrania. All characteristic organs of the chordates are
depicted: notochord (Cd), metameric muscle packages (My), branchial basket (Kd), dorsal nerve chord
(Nr). Whereas the body cavity containing the gut is devoid of subdivisions, the coelomic cavity shows
segmental vestiges in the form of fluid filled compartments in the niyotomes (St).
notochord bends internally in the body as
the longitudinal muscles contract, it will no
longer maintain the constant length of the
body. Constant length of the body is an
essential requirement for locomotion by
lateral undulations.
Subsequent to the evolution of the notochord, the transverse and circular muscles could disappear as they are no longer
essential for the integrity of the hydrostatic
skeleton and because peristalsis is no longer possible (Fig. 3A-D). Reduction of these
muscles was advantageous as it reduced
the bulk of the animal and the amount of
energy needed for muscle contraction and
maintenance. Loss of these circular and
transverse muscles presumably occurred
soon after the evolution of the notochord.
Together with the reduction of the circular and transverse muscles, the dorsal
part of the longitudinal muscles enlarged
and became the major set of locomotory
muscles. These muscles and only these
muscles could enlarge because they are
positioned next to the notochord which is
now the only anticompressive structural
element in the body. The notochord can
resist effectively the compressive forces
placed on the body axis by the locomotory
muscles only if these muscles lie close to it.
With the enlargement of the dorsal longitudinal muscles, development of the central nervous system in a dorsal position is
advantageous because it reduces the
length of the peripheral nerves to the muscles. Thus the dorsal nerve cord evolved
PHYLOGENY OF DEUTEROSTOME COELOMATES
71
in conjunction with the dorsal longitudinal
musculature. Shift of the dorsal nerve cord
from a superficial position to the present
position just dorsal to the notochord provided greater mechanical protection (Fig.
WH).
Metamerism of the body was retained at
the chordate level because the thick package of segmental longitudinal muscles
(myotomes) had to remain connected to
the body axis. The dissepiments evolved
into myosepta with the loss of transverse
muscles. The myosepta subdivide the longitudinal muscles into metameric units
which are retained throughout the vertebrates.
The metameric arrangement of the peripheral spinal nerves was a consequence FIG. 4. Model for the evolution of the craniote conof the mechanical system of muscles and struction. The two stages continue the model of Figtransverse septa. The peripheral nerves ure 1, H, into the craniote level of organization. The
could fit readily into a segmental subdivi- major changes consist of the formation of a cephalic
region (K) equipped with large sense organs and the
sion of myotomes and myosepta.
brain in which bending movements are suppressed
After the evolution of the notochord, by stiffening skeletal structures. The efficiency of the
enlargement of the dorsal longitudinal motoric apparatus, the precondition for the emermuscles and the specialization of the cen- gence of a stiff head region, is increased by the deof stabilizing osseous scales (S) which in
tral nervous system as a dorsal nerve cord, velopment
the next stage of vertebrate evolution are replaced by
this complex of features could be extended a more economical internal grid of skeletal elements.
beyond the end of the digestive tract as a
postanal tail (Fig. 3H). This locomotory
system, which is unique to chordates, is
dependent upon the evolution of the no- turgid throughout the entire hydrostatic
tochord as the central support of the body skeleton containing fluid filled cavities unand the subsequent development of the der pressure. Either the gill slits would be
dorsal musculature and nerve chord. A forced closed by the turgid hydrostatic
postanal tail could not evolve so long as skeleton, or the open gill slits would disbody support was provided by a coelom- rupt the turgidity of the hydraulic system
and the anterior end of the body would be
based hydrostatic skeleton.
limp. Thus only after the establishment of
The last major chordate feature to ap- the notochord and the myotomes had propear was the branchial basket. This filter vided the needed support in the dorsolatfeeding structure is dependent on a series eral part of the body, could the branchial
of gill slits through the body wall connect- basket evolve. The incipient stages of this
ing the anterior end of the digestive system filter feeding system consisted of slit-like
with the outside (Fig. 3E-G). These slits in deepenings of the mouth which gradually
the body wall could only appear and be- became subdivided into separate gill clefts.
come specialized after the notochord
To summarize: The evolution of the
evolved and assumed the full role of axial major chordate features from a worm-like
support. At an earlier stage in deutero- metameric coelomate ancestor are in the
stome evolution when body support was following order:
provided by a hydrostatic skeleton, regardless of whether it was a gel-filled system or a) notochord;
a metameric coelom, the slits in the lateral b) specialization of dorsal longitudinal
body wall would have completely disruptmuscles together with reduction of the
ed the hydraulic system in the anterior end
transverse and circular muscles;
of the body. The body wall has to remain c) a simultaneous specialization of the
72
WOLFGANG FRIEDRICH GUTMANN
FIG. 5. Phylogenetic model for the evolution of hemichordates and echinoderms from acrania-like chordate
ancestors.
A. Chordate construction which can live and filter feed in the sediment because the water current is driven
through the branchial basket (Ks) by the cilial lining. In compensation for the locomotor activity the
branchial basket is enlarged by multiplication of the gill slits.
B. Formation of muscular proboscis (R) allows the intermediate stage to move in the sediment. The notochord
(Cd) and the spinal chord (Nr) are reduced in the posterior part of the body. The cross section shows the
reduction and opening of the atrium from the atrioporus.
C. Enteropneust-like construction showing vestiges of notochord (Cd), nerve chord (Nr), and longitudinal
muscles (Lm) in the hind part of the body. Metamerism is entirely reduced because the suspensory
structures for the notochord are no longer required. The body became divided into three compartments:
the proboscis (R), the collar (Kr), and the posterior part.
D. The pterobranch-construction arose by transformation of the collar region into a tentacular apparatus
(T) which was protruded from the burrow. Its emergence was accompanied by the almost total reduction
of the branchial basket (Ks—vestigial gill slits).
E. Transitory stage to echinoderms. The tentacular apparatus that corresponds to the collar region is arranged in a radial way. Some (Ks) gill slits are still present. The proboscis becomes reduced.
F. Primitive echinoderm construction. The body frame is supported by a calcareous skeleton (Cs), the tentacular apparatus (T) continues to function as a hydraulic system.
Whereas the primitive echinoderms were sedentary organisms, the advanced eleutherozoans lost contact with the substrate and became freely moving forms: G. Asteroid; H. Echinoid.
central nervous system as a dorsal
nerve cord;
d) development of a postanal tail;
e) origin and specialization of the branchial basket with numerous gill slits as
a filter feeding apparatus (follows "c").
The chordate group which has the structure seen at this stage of chordate evolu-
tion is the lancelet (Acrania) which can be
considered as representing the most primitive group of known chordates and the
stock from which other deuterostome coelomates have evolved. I will not trace the
evolution of vertebrates from their acrania
ancestor (Fig. 4) as this evolution is mainly
a further specialization of the features
present in the lancets and little disagree-
PHYLOGENY OF DEUTEROSTOME COELOMATES
ment exists about this aspect of chordate
phylogeny (Gutmann, 1972, 1975, 1977).
FROM ACRANIA TO HEMICHORDATES
Typical chordates (e.g., lancelets) might
€bt be considered as real candidates for
burrowing in the mud. The notochord and
the longitudinal muscles arranged in myotomes do not enable these animals to penetrate into fine sediment because only lateral undulations are possible. These
movements are, of course, sufficiently effective to allow wriggling into coarse sediment (sand) in which filter-feeding could
be continued. The coarse sediments allow
the water currents to pass through its interstices. Organisms such as Branchiostoma, which are fully equipped for active locomotion, have acquired a sessile way of
life in coarse sediments. Energy used for
locomotion could be saved when trapping
of food was improved by enlargement of
the branchial basket. The long extension
of the branchial basket and the large number of gill slits have been considered to be
an adaptation to a sedentary mode of life.
These features and others not mentioned
here are not typical for the chordate construction ancestral to the other branches of
deuterostomes (Gutmann, 1966, 1967,
1972; Bonik and Gutmann, 1977; Gutmann and Bonik, 1979).
In some acrania-like group, the animals
started to burrow in finer and finer sediments in which lateral undulations were
less suitable for movement. Moreover as
the sediments became finer, the animal
had to form a tube for water flow (Fig. 5A).
In one of these groups, the anteriormost
end of the body (anterior to the mouth and
branchial basket) must have modified into
a hydrostatic organ that allowed the animal to burrow in muddy sediments by
peristaltic movements (Fig. 5B). The original function of the rudimentary proboscis
may have been the opening of a hole in
the sediment through which the inhalent
current of water could enter the mouth.
With further development of the proboscis, penetration into mud and active locomotion through it were achieved gradually. A burrow is formed by the animal in
which it lives and through which the cilia
of the branchial basket drive a water cur-
73
rent. The proboscis has a hydrostatic skeleton with a complex arrangement of muscular braces. It lacks a notochord-like axial
support and hence can move by peristaltic
action. It permits active but slow locomotion in muddy sediments of a worm-like
animal.
The notochord was reduced because its
stiffness and its function to preserve constancy of body length were disadvantageous
in the new environment. The animal
evolved a worm-like body which is suitable
to life in an U-shaped tube. Longitudinal
muscles were retained as they serve to
shorten and pull along the elongated posterior part of the body which drags behind
as the anterior end moves forward by active burrowing action of the proboscis.
Muscles are not needed to stretch the body
which is pulled out passively as it contacts
the walls of the burrow during locomotion.
Metamerism of the longitudinal muscles
was lost and the metameric coelom evolved
into an oligomeric one as the function of
the transverse septa to suspend the notochord in the body became obsolete as a
consequence of reduction of the notochord and the septa. Vestiges of the
notochord persist as the stomochord (Fig.
5C). In addition to this vestige of the
notochord, a short piece of neural tube remained in the collar region of the body.
The preponderance of longitudinal muscles, the vestiges of the notochord and
neural cord are strong evidence for the
chordate origin of the hemichordates.
Their advanced position relative to primitive acrania is shown by the oligomeric
coelom, the unsegmented longitudinal
muscles and the vestiges of the notochord
and neural cord.
These worm-like chordates are the enteropneusts (acorn worms) which are usually placed in a distinct group—the hemichordates—which retained the filter
feeding branchial basket possessed by typical chordates. The profound modification
of the body architecture is an adaptation
to active burrowing in muddy sediments.
The three body regions of the enteropneusts fulfill specific functions in these
burrowing animals. The proboscis is the
active hydraulic system for burrowing.
The collar maintains contact with the wall
74
WOLFGANG FRIEDRICH GUTMANN
of the tube and prevents the water discharged from the gills from reentering the
mouth (Fig. 5C). The hind part comprises
most of the body and houses the branchial
basket and the gut; it is dragged along passively when the animal burrows with its
proboscis.
The oligomeric coelom of the enteropneusts corresponds to the reduction of the
notochord and of the muscular system of
these animals and evolved with the burrowing mode of living. It still serves as a
hydrostatic skeleton but is a much poorer
one than the metameric one of its ancestors. In contrast to other burrowing worms
that possess a hydrostatic skeleton, such a
system could not have arisen de novo in the
enteropneusts because the gill clefts perforate the body wall and because the necessary circular muscles for an efficient system could not develop gradually from the
longitudinal ones. Therefore the morphological and functional properties of their
chordate forerunners (acrania-like forms)
restricted the possibilities of of the enteropneusts.
Enteropneust-like organisms gave rise to
the pterobranchs which still possess characteristic chordate features. They have an
oligomeric coelom, only longitudinal muscles in the posterior region of the body,
and vestiges of the notochord in the anterior part of the body. These sessile forms
live in a permanent tube secreted by the
animal. The proboscis is the only part that
can actively move in this tube and pulls the
animal out for feeding. The hind region
is passively stretched and can only shorten
actively to pull the pterobranch back into
its tube. This feature supports the hypothesis of the origin of pterobranchs from
chordate ancestors possessing only longitudinal muscles.
Whereas in the enteropneusts the chordate branchial basket still functions in essentially the same way as in the typical
chordates, the gill clefts of the pterobranchs are reduced to a single pair. Even
this pair of gill slits is closed in some genera. In exchange for the gills, filter-feeding is performed by tentacles which have
developed from the collar of the enteropneust-like ancestors (Fig. 5D). In the
acorn-worms, the inner lining of the collar
is able to collect food particles on its surface. When the collar was enlarged in
pterobranchs it was gradually transformed
into a tentacular apparatus which became
the primary feeding apparatus with redu0
tion of the gills. The branchial basket can
function as a filter feeding apparatus for
animals living in a tube open at both ends,
but it cannot operate in an organism living
in a closed tube. Change from the branchial basket to the tentacular feeding apparatus took place with the change in life
from a burrowing animal in an open tube
to a sessile one in a closed tube.
THE ECHINODERMS
Although the body construction of adult
echinoderms is radically different from
that of chordates, these phyla share a number of embryological and biochemical features, and most workers agree that they
are closely related. A reasonable transformation series was indicated by Grobben
(1924), but was never described in detail;
only a very sketchy model touching on the
major points will be presented here.
The evidence for the existence of gill
clefts in primitive echinoderms was presented by Jefferies (1975). Based on this
evidence, it may be concluded that ancestral echinoderms possessed a branchial
basket inherited from their chordate
ancestors, but that this filter feeding apparatus, together with the gill slits, was lost
early in the phylogeny of the echidoderms.
Because the adult morphology of echinoderms is so profoundly modified from that
of typical acrania-like ancestors, it is difficult to suggest a reasonable transformation
series and to link possible intermediate
stages with known groups. Most evidence
suggests a very close link between echinoderms and hemichordates so that I will assume that the pterobranchs or at least the
enteropneusts represent the chordate construction from which echinoderms evolved.
The ancestors of echinoderms left the
sediment and sedentary life in tubes in
which their forerunners lived and attached
themselves onto firm surfaces. Specialization to sessile life resulted in transformation of bilateral symmetry, still seen in
PHYLOGENY OF DEUTEROSTOME COELOMATES
pterobranchs, to radial symmetry. In addition, a stiff framework of superficial calcareous skeletal plates evolved for mechanical protection, another adaptation
for sessile life. These calcareous plates
firmed the basis of the rigid skeleton of
echinoderms by which they were able to
overcome the mechanical limitation inherent in the possession of the oligomeric coelom and only longitudinal muscles in the
hind region of the body in their hemichordate ancestors (Gutmann, 1972; Gutmann and Bonik, 1979).
The tentacles that had evolved in the
pterobranch-like forerunners continued to
function as filter-feeding organs and were
held upwards into the water current to
trap small particles. The tentacles were reorganized into a pentaradial pattern in
correspondence with the radial symmetry
of the body (Fig. 5E). The hydrostatic
mechanism of the tentacles reflects the
pentaradial configuration and is present in
all echinoderms. It is connected to the collar coelom in which hydrostatic pressure
is developed that expands and stiffens the
tentacles. This coelomic system is separated from the body wall and is, therefore,
able to contract freely and independently
of the stiff body wall when pumping fluid
into the tentacles.
Primitive echinoderms were stationary
animals of the crinoid type (Fig. 5F), but
the advanced echinoderms, the eleutherozoa, evolved the ability to move actively
on their tentacles (Fig. 5G-H). This
change was achieved when sedentary, radial forms turned over onto their oral surface, whereby the tentacles contacted the
ground and were able to perform locomotory movements. This astonishing
transformation could occur gradually
when crinoid-like forms with flexible stalks
bent their tentacle crown down to collect
food from the bottom. Walking on the substrate with the tentacles improved the efficiency of feeding and was continued after
the stalk lost contact with the substrate.
The evolution of echinoderms from an
ancestral pterobranch-like chordate stock
can be summarized with the following
large groups from most primitive to most
advanced:
75
a) The branchio-echinoderms (Bonik et
al., 1978) which are groups still possessing a fully developed branchial basket, presumably possessing tentacles,
which were secondarily reduced. The
stalk which is still present in some
forms has lost contact with the substrate;
b) the pelmatozoans which are sessile
groups with a stalk, pentaradial symmetry, tentacles, but have lost the branchial basket including the gill slits;
c) the eleutherozoans which are free-living groups that have lost the stalk and
have turned over onto the oral surface.
This sketch of echinoderm evolution
from chordate ancestors is admittedly
brief as I am currently undertaking a detailed analysis of this question in cooperation with paleontologists. The results
which will be based on a functional-adaptive analysis of living and fossil forms, will
be presented in future papers. We are especially interested in determining whether
some of the soft-bodied fossils of the Burgess shale formation belong to the transformation series leading from the chordates to the echinoderms (Conway Morris
and Whittington, 1979).
THE TUNICATES
The phylogeny of the deuterostomes
would be incomplete without mentioning
the tunicates. The transformation series
leading to these animals will be sketched
only briefly herein; details can be found in
Gutmann (1975). Tunicates can be derived
easily from typical chordates; they are advanced, not primitive members of this phylum. The acrania-like forerunners of tunicates became stationary and anchored
their body to the ground. By avoiding locomotion, they economized on energy
needed to maintain a locomotory system
and for active locomotion. The whole locomotory apparatus, including the notochord, metameric coelom and most of the
central nervous system, was lost in the
adult organism (Fig. 6). The lack of locomotion was compensated for by an enormous enlargement of the branchial basket
and a more effective pumping mechanism.
76
WOLFGANG FRIEDRICH GUTMANN
FIG. 6. Evolution of the tunicate construction. The
tunicates arose from typical chordate ancestors as depicted in Figure 1 stage H by enlargement of the
branchial basket and reduction of the propulsive system of notochord (Cd) and myotomes (M) in the adult
stages. The notochord and the non-metameric longitudinal muscles are retained in the larvae of many
tunicates as mechanism of dispersal. The sequence
shows, A, the enlargement of the branchial basket in
a hypothetical stage in which locomotor activity is reduced. B, the shift of mouth and anus together with
the opening of the atrium to the dorsal side. C, the
typical ascidian construction. (Md)—mouth; (Af)—
anus; (Da)—intestinal canal; (Ka)—branchial basket;
(Ks)—gill slits; (Pb)—atrium; (Ed)—endostyle; (E)—
atrial pore; (Nr)—dorsal nerve chord; (M)—longitudinal muscles; (St)—statocyst; (G)—dorsal ganglion;
(Go)—gonads; (M)—mantle.
FIG. 7. Larval stages of the development of tunicates
(after Bone, 1972, from Gutmann, 1975).
A. Larva with tail (Sw), notochord (Cd), dorsal nerve
cord (Nr), gill slits (Ks).
B. Transitional stage. The tail is already reduced,
only minor remains (R) are visible. Gut (Da),
mouth (Md), vitelline mass (Do), heart (He),
atrium (Pb), atrial siphon (E).
C. Adult tunicate.
tionary novelty that lead the way to the
evolution of other chordates.
DISCUSSION
A tunic developed as an outer layer of
tough material protecting these immobile
animals. Although the locomotor system is
reduced in the adult stages, the notochord
and longitudinal muscles exist in the larval
tail, thus providing for dispersal (Fig. 7).
With its ability to swim actively for a short
period, the larva can select the substrate
site for settling. This action has high selective value because the adult animal is fixed
to the site selected by the larva. The tail is
a special larval adaptation, but one evolved
from features present in adults of the
ancestors of tunicates. It is not a new feature originating in tunicates as an evolu-
The model for the phylogeny of deuterostome coelomates presented herein is
based on the establishment of transformation series of individual features and of
similar series for the whole organism; the
latter may be regarded as phylogenetic
diagrams of taxa. A summary of this model would be useful before comparing it
with others.
Most of the groups mentioned possess
hydrostatic skeletons in which those composed of fluid filled sacs (coeloms) are advanced and advantageous to those with a
solid gel filling. Primitive coeloms are metameric with oligomeric coeloms being ad-
PHYLOGENY OF DEUTEROSTOME COELOMATES
vanced. The ancestral stock of the deuterostomes is postulated to be a worm-like
animal with a metameric coelom.
Evolution of the basic chordate features
occurred in the following order:
T?) the notochord;
b) reduction of the transverse and circular
muscles and specialization of the dorsal
longitudinal muscles in a metameric arrangement;
c) specialization of the nervous system
into a dorsal nerve cord and segmental
peripheral nerves;
d) evolution of a postanal tail; and
e) origin and specialization of a branchial
basket with gill slits.
The last feature could have evolved only
after the evolution of the notochord which
replaced the coelom as the axial support
and the specialization of the dorsal longitudinal muscles. The primitive chordate
stock possessing these features would be
an animal similar to the lancelet (acrania).
Vertebrates evolved from acrania by
further specialization of the traits in the
latter group and the evolution of rigid
skeletal structures.
Hemichordates evolved from acranialike ancestors by specializing for burrowing in soft sediments. A peristaltic
structure—the proboscis—evolved for
penetration and burrowing in mud. The
notochord became reduced, as did the
dorsal nerve cord, the coelom evolved to
an oligomeric one with loss of transverse
septa and the body muscles became elongated, nonsegmented longitudinal muscles. The pterobranchs became specialized
for life in closed tubes in which the branchial basket became reduced to a vestige
and replaced by tentacles evolved from the
enteropneust collar.
Tunicates evolved from acrania-like
ancestors by attaching to the substrate and
abandoning active locomotion in the adult.
These animals lost the notochord, most of
the central nervous system, most of the
musculature and the metameric condition
of the coelom. The muscular tail in larvae
is an adaptation for dispersal, but is derived from structures present in the acrania-like forerunners.
77
Echinoderms are considered to have
evolved from chordate ancestors from a
pterobranch-like stage. Intermediate forms
possessed a branchial basket and tentacles,
but the former were lost and the latter specialized early in echinoderm evolution. A
superficial layer of calcareous plates
evolved for protection, and subsequently
became a rigid skeleton compensating for
the poor mechanical system of an oligomeric coelom and only longitudinal muscles in the ancestor. Radial symmetry
evolved in the early sessile echinoderms,
and lastly the advanced echinoderms became free-living by turning over onto the
oral surface and walking with the tentacles.
This concept of deuterostome phylogeny is very different from many others presented earlier in the literature in which
groups such as the tunicates (Berill, 1955),
the hemichordates (Siewing, 1972; Remane, 1973) and the echinoderms (Jefferies, 1975) are regarded as the primitive
stock within the deuterostomes or the
chordates rather than advanced members.
Presentation of models or hypotheses for
deuterostome phylogeny is only part of the
analysis. More important is the development of methods by which the several theories can be tested and thereby falsified or
further verified. The importance of the
functional-adaptive analysis developed together with studies of hydrostatic skeletons
is that it provides one way to test these conflicting theories.
The functional study includes a mechanical analysis of complex sets of morphological structures which must be consistent
with the laws of physics (e.g., mechanics).
The advantage of this approach is that at
least part of the test is based on laws outside of biology and to that extent is independent. The adaptive and evolutionary
segment of the method is based on the
concept of gradual macroevolutionary
modification (e.g., Simpson, 1953; Bock,
1979) in distinction to concepts of saltation
as postulated by earlier workers (e.g.,
Goldschmidt, 1940; Schindewolf, 1950). It
is necessary to postulate, in detail, the sequence of change in features, to provide
an adaptive explanation for their evolution, to show that the organisms at all in-
78
WOLFGANG FRIEDRICH GUTMANN
termediate stages are functional and adap- a) The tunicate model. The commonest
theory places the tunicates as the primtive to their environments, and to postulate
itive group of chordates. The branchial
a series of environmental interactions that
basket and gill slits are considered to be
could be responsible for the adaptive evothe first chordate features to appear in
lutionary changes.
an animal possessing an oligomeric c o ^
The demands required in the functionlorn. Subsequently, the notochord, doral-adaptive method of testing have been
sal nerve cord and segmented longitumet for the hypothesis of deuterostome
dinal muscles appeared as larval
phylogeny proposed herein for the evoadaptations for active swimming needlution of chordates from a metameric
ed for dispersion. These features were
worm-shaped coelomate with the sequence
incorporated into the adult stage of deof evolutionary changes being the origin
scendent forms (acrania, vertebrates)
of the notochord, myotomes of dorsal lonby neoteny.
gitudinal muscles, and myosepta, loss of
transverse and circular muscles, the dorsal b) The hemichordate model. This theory
nerve cord, the postanal tail and lastly the
places the hemichordates (enteropbranchial basket and gill slits. Morphologneusts) as the primitive group of chorical construction of the most primitive
dates. The branchial basket and gill slits
chordate is shown by the acrania. Subseare again considered to be the first
quent loss of most of the notochord and
chordate features to appear in an anidorsal nerve cord, loss of metamerism in
mal possessing an oligomeric coelom
the coelom and longitudinal muscles, and
with unsegmented longitudinal musappearance of the proboscis occurred in
cles. Subsequently the notochord, dorthe hemichordates with their invasion of
sal nerve cord and metamerism, both
soft substrates and adaptation to life in
in the muscles and the coelom, evolved
tubes open at each end. Appearance of
as features for improved locomotion.
tentacles from the enteropneust collar and c) The echinoderm theory. This theory
eventual loss of the branchial basket took
consideres the echinoderms to be the
place in the evolution of pterobranchs
primitive members of the deuterowhich left the soft substrate for a sessile
stome coelomates. Again a branchial
life in closed tubes. Similar changes ocbasket and gill slits are believed to have
curred in the evolution of echinoderms
appeared first in an animal with an
from a hemichordate-like ancestor with
oligomeric coelom, possibly lacking
the addition of an armor of calcareous
even longitudinal body muscles (as seen
plates which became a rigid skeleton. Loss
in the chordates), but having a rigid
of the notochord, the locomotory muscuexoskeleton and associated musculalature and the dorsal nerve cord occurred
ture attached to the skeletal plates. The
in the evolution of tunicates as they beearliest group would be a branchoechicame sessile animals attached to hard surnoderm. Later the exoskeleton would
faces. These features were retained as larbe lost and replaced by a hydroskeleton
val specializations in some tunicates and
and body musculature, which would
became reincorporated in the adult form
later be segmented by transverse septa
of some derived, free-living groups of tusubdividing both the coelom and lonnicates by neoteny.
gitudinal musculature. A dorsal nerve
chord
evolved, presumably with the
Proponents of alternative hypotheses
muscles
and finally the notochord apfor deuterostome or chordate phylogeny
peared and acquired the role of the
have not attempted to test these ideas by
body support. Many of these points are
means of a functional-adaptive analysis. I
not mentioned by Jefferies (1975) but
would like to outline each of these alterthey are a definite consequence of a
native models giving attention only to the
model for the evolution of chordates
critical evolutionary changes to be tested
from echinoderm ancestors.
functionally and adaptively.
PHYLOGENY OF DEUTEROSTOME COELOMATES
Although these theories differ in the
conclusion on the primitive group and in
many details on the phylogeny and the sequence of evolution of features, they all
include two postulated evolutionary steps
0rrhich cannot be explained by a functionaladaptive analysis within gradual macroevolutionary change. These are:
a) The postulated origin of an oligomeric
coelom as the primitive one and the
evolution of a metameric coelom from
the oligomeric condition with the evolution of dissepiments and segmentation of the longitudinal muscles and
b) the evolution of a branchial basket with
gill slits in the body wall in an animal
possessing a hydrostatic skeleton and
prior to the evolution of the notochord
and specialization of the dorsal longitudinal muscles.
These changes which are essential to
each of the alternate models mentioned
above could occur only by saltations. This
is at variance with generally accepted evolutionary theory, including that accepted
by most proponents of these alternate
models. It may be possible with future
knowledge to provide a gradual functional-adaptive analysis for these changes with
greater knowledge about possible systems
of biological construction and relationships between these animals and their environments. However, the organisms are
still subject to the laws of mechanics which
are not likely to change radically. At this
point in our knowledge of the functional
morphology of the deuterostomes, I can
only conclude that a vanishingly small
probability exists for the occurrence of the
critical evolutionary changes, gradualistic
ones, in these alternate models for the
phylogeny of the deuterostomes, and
hence I would conclude these models have
been falsified strongly.
Special mention should be made of the
neoteny idea for the origin of higher chordates from ancestral tunicates because this
model has been presented most persuasively (Garstang, 1928; Berill, 1955; Bone,
1960) and has been widely accepted. No
79
question exists that neoteny has occurred
in the evolution of several groups of freeswimming tunicates which have lost the
sessile adult stage in their life history. And
it is entirely possible that existing chordate
groups, such as the vertebrates, evolved
from tunicate ancestors by neoteny. The
problem is how the chordate characters
evolved in the evolution of the tunicates.
A hypothesis for the appearance of new
features as larval specializations and their
subsequent incorporation into the adult
stage of descendent groups by neoteny.
does not eliminate the requirement to provide a functional-adaptive analysis for
these changes. Not only has this never
been attempted for the tunicate neoteny
hypothesis for higher chordates, but this
model does not rest on solid morphological description of the tunicate larvae.
The larval tail of tunicates is a connective tissue sheath filled with cells and fluid,
and constitutes a hydraulic apparatus. The
few muscle cells are not arranged segmentally, but are attached directly to the connective tissue sheath and generate thrust
by bending the axial support. The hydraulic organ and longitudinal muscles require
definite preconditions for their evolutionary origin as discussed above. These preconditions have not been mentioned by
advocates of the neotenic tunicate model
and it appears unlikely that they could exist.
The neotenic tunicate model suffers,
moreover, from the problem of the origin
of the branchial basket in an animal with
a hydrostatic skeleton and need not be
mentioned again here.
Evolution of a tail in a larva, including
all the specialized features of the tail locomotory system of tunicates, appears
highly improbable. The use of a tail as a
propulsory organ depends on a certain
degree of perfection and the attainment of
a minimal length. A functional explanation, other than locomotion, would have to
be postulated for the adaptive significance
of the incipient stages in the de novo evolution of a propulsive larval tail. Such explanations have not been offered, and reasonable nonlocomotory arguments for the
80
WOLFGANG FRIEDRICH GUTMANN
de novo origin of the tunicate tail are not
apparent.
The neotenic tunicate larval model fails
to mention that not all sessile tunicates
have a tailed larva, but some have one that
swims by cilia covering the body. Are these
primitive forms advanced degenerate
forms or ones on a side branch? Moreover
the tailed larva in sessile tunicates have a
short existence, just long enough to disperse and locate a suitable site for attachment. It does not feed in all species possessing a tailed larva. This model must
postulate two steps, each with adaptive explanations. First, is the evolution of feeding in the tailed larva, and the second is
neoteny with elimination of the sessile
adult form.
The tunicate tail is, indeed, a specialized
larval adaptation, but it is dependent on
all of the essential structures being present
already in the ancestors of the tunicates. It
is not necessary to postulate the de novo
appearance of any features in the evolution of the specialized larvae as they simply
retained features present in the adult of its
ancestors.
In conclusion, if the entire set of chordate features is present in the ancestors
of the tunicates, then it is equally reasonable to postulate that the higher chordates
(vertebrates) evolved directly from an
acrania-like ancestor than from a specialized tunicate larva through neoteny.
The conclusion to be drawn from this
case study of deuterostome phylogeny is
that a functional-adaptive analysis is an essential part of the testing of phylogenetic
models. This approach provides a strong
efficient method for the falsification and
rejection of alternate models. Such a method had been lacking in earlier discussions
of the validity of diverse models of invertebrate phylogeny. It is my belief that with
the application of proper functional-adaptive analysis our understanding of invertebrate phylogeny will improve rapidly.
ACKNOWLEDGMENTS
The illustrations were skilfully executed
by Mrs. Renate Klein-Rodder to whom I
am very grateful. The English manuscript
was virtually rewritten bv Professor Bock.
In addition to this time and energy consuming help I owe to him a careful check
of the arguments and valuable advice for
the presentation of the phylogenetic reconstruction.
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