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AMER ZOOL. 16:277-291 (1976)
Spiralian Development: A Perspective
DONALD P. COSTELLO AND CATHERINE HENLEY
Department ofZoology, University of North Carolina, Chapel Hill, North Carolina 27514
s\ \ORSIS Three basic t\pes of spiral cleavage are described: spiral cleavage by quartets, by
duets, and b\ monets. Following F R. Lillie's concept of adaptation in cleavage, the relation
of each of these cleavage modifications to the structure of the lar\a or juvenile, which
develops therefrom, is considered. These comparisons lead to the conclusion that Lillie's
concept of adaptation in cleavage can be extended beyond such details as cell contents, cell
size, tempo of diwsion, etc., to include even the oblique character of spiral cleavage and its
general basic form.
INTRODUCTION
Seventy-five years ago, one of the most
eminent students of the emerging field of
cell lineage wrote the following prescient
words: "It has happened, very naturally,
that writers on the subject of cell-lineage
have laid special emphasis on the resemblances, which are nothing short of
marvelous, . . . between the cleavage of the
eggs of even widely separated forms.
. . . But . .. one of the most instructive
aspects of cell-lineage is thus lost sight of,
namely, the special features of the cleavage in
each species, which are, 1 believe, as definitely
adapted to the needs of the future larva as is the
latter to the actual conditions of its environment"
(Lillie, 1899; p. 43). In this perspective, we
propose to examine Lillie's concept more
closely, and to relate it to modified forms of
spiral cleavage as it occurs in several
groups. Before we do so, however, it is appropriate to consider briefly what is meant
by spiral cleavage and, interestingly, the
very origin of the descriptive term
"Spiralia."
"SPIRALIA" AND SPIRAL CLEAVAGE
Schleip, in 1929, defined Spiralia as those
animal groups showing spiral cleavage during early development. However, since the
primary basis for setting up phyla is comAided by a grant from the National Institutes of
Health, GM 15311. We thank Miss Barbara G. Cain for
her efficient assistance with the illustrations.
parative anatomy rather than comparative
embryology, the term "Spiralia" has no obvious supraphyletic significance. The
difficulty arises from the fact that all representatives of the phyla involved do not
show spiral cleavage. It is generally agreed
that the forms showing clear-cut spiral
cleavage by quartets include the polyclad
turbellarians, the annelids, the rhynchocoels, the molluscs (with the notable exception of the cephalopods), the
echiuroids, and the sipunculoids. Modified
forms of spiral cleavage are characteristic
of the acoel turbellarians, of at least one
group of arthropods (the cirri pedes) and of
the rotifers.
The view that cleavage homologies are a
criterion of phylogenetic affinities dates
back to the earliest studies of spiral patterns
of annelids and molluscs, to which that of
the polyclad turbellarians was soon added.
There was the general idea that a primitive
coelomate ancestor, with spiral cleavage of
the quartet type, gave rise to a turbellarian
archetype, from which higher forms were
evolved. This was discussed as early as 1914
by Heider, although we do not find the
term "Spiralia" in Heider's paper. Heider's
ideas had been strongly influenced by
Hatschek's (1886) trochophore theory,
which stressed the affinities between the
annelids and molluscs, as indicated by features common to their larval forms. Aside
from the chapter heading in Schleip's
(1929) book, the chief expositions that we
have found dealing with the "Spiralia" are
by Ulrich (1951), Remane (1952, 1957,
277
278
DONALD P. COSTELLO AND CATHERINE HENLEY
1963) and Marcus (1958). Marcus speaks of more thorough investigation is completed.
Remane, Ulrich and himself as being in It is clear that Blochmann (1881) used a
"common zoological descent from Karl fully developed system of capital and lower
Heider," in relation to their views on the case letters, plus numbers and exponents,
evolution of animal phyla. Peter Ax (1963) to describe the spiral cleavage pattern of
stated that in his view the spiralian theory the developing embryo of Neretina. Fol
was clearly the most probable interpreta- (1875) had earlier employed a system based
tion of the phylogenetic position of the on the Roman numerals I-IV for the four
Turbellaria.
macromeres and the Arabic numerals 1-4
Spiral cleavage is characterized by a rota- for the first micromeres, in his description
tional movement of cell parts around the of pteropod cleavage. Whitman (1878)
egg axis, leading to an inclination of the who, perhaps more than any other invesdivision spindles with respect to tigator, may be said to have founded cell
symmetrically-disposed radii. It could, lineage, used the letters a, b, c, and x for the
more properly, have been called oblique four basic blastomeres of Clepsine. Wilson
cleavage. These rotational movements fol- (1892) and Conklin, prior to 1897, had delow a regular alternation of direction, vised usable, slightly dissimilar systems for
clockwise (right-handed, or dexiotropic) Nereis and Crepidula, along lines akin to the
and counterclockwise (left-handed or laeo- terminology of Blochmann. Robert (1904)
tropic [ = leiotropic or laevotropic]), in suc- improved Conklin's scheme by identifying
cessive cleavages. Post-cleavage rotations of the macromeres with capitals and prefix
cell parts and blastomeres may occur also. numbers to indicate their generation
The inclination of the spindles in spiral (1A-1D etc.). Meanwhile, Kofoid (1894,
cleavage of the quartet type is usually strik- 1895) had devised a new scheme by which
ingly clear at the third cleavage, at which each cell during the spiral period of cleavtime the first quartet of micromeres is age was designated by (1) a lower case letter
formed. During the first and second cleav- (a, b, c or d) indicating the quadrant, (2) a
ages, which may be either equal (Fig. 1) or first exponent indicating the cell generaunequal (Fig. 2), the obliquity of the spin- tion, and (3) a second exponent to desigdles is less apparent, and the chief criteria nate the quartet (or "story"). Kofoid, howare the pre- and post-cleavage rotational ever, numbered the quartets from the vegmovements. These first two cleavages may etal pole toward the animal pole, and desbe spoken of, therefore, as prospectively ignated the lower cell or quartet by an odd
spiral (Conklin, 1897). Except in those exponent and the upper by an even one.
forms showing reversed symmetry, it is the Thus, his second exponents are directionodd-numbered divisions that are dexio- ally reversed as compared with the corretropic, and the even-numbered laeotropic. sponding designations for quartet and cell
In spirally cleaving forms, there is a transi- positions of the other schemes. Kofoid's
tion to bilateral divisions following the early nomenclature was avidly applied in
segmentation of the embryo, and this fact numerous molluscan and annelidan cleavhas considerable significance in relation to age studies, and modified only slightly for
Lillie's ideas about adaptation in cleavage. cleavage in the cirripede egg by Bigelow
(1902). Anyone familiar with invertebrate
We feel that if cleavage patterns are to be cleavage patterns can readily translate any
used as criteria of embryological relation- of these terminologies into any other (see
ships, both the obliquity of the spindle orienta- Fig. 6), but it is essential to keep in mind the
tions and the regular directional alternations of exact meanings of the designations in the
spiral cleavage must be stressed.
different systems.1 This translation is as
TERMINOLOGY OF SPIRAL CLEAVAGE
The origin of the four-quadrant system
of cleavage nomenclature is shrouded in
obscurity and is likely to remain so until a
1
In our estimation, Conklin's adaptation of
Kofoid's scheme for the ascidian egg is a perfect or
near-perfect nomenclature for that group. For the
Molluscs (and Annelida), we favor Robert's system.
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
simple as converting fractions to decimals.
Obviously, all four-letter systems of cell
nomenclature were devised for the type of
spiral cleavage in which there are four
clearly discernible quadrants, marked
(usually) by four large, yolk-filled macromeres, which produce successive quartets
of micromeres. \nNereis, Wilson (1892) observed that the oil droplets (as well as the
yolk spherules) accumulate in the macromeres and gradually fuse to form a single
large oil drop in each of the four large
endodermal cells, to provide a striking visual criterion of the quadrant arrangement.
FOUR-QUADRANT SPIRAL CLEAVAGE
The classical example of molluscan
four-quadrant spiral cleavage is that of Crepidula, as described by Conklin (1897). As
shown in Figure 1, the first two cleavages
are equal and meridional, giving the four
cells A, B, C and D, with a vegetal polar
furrow resulting from the early rotational
protoplasmic movements. It is the third
279
cleavage which is clearly spiral. The spindles in each of the first four blastomeres
become oriented obliquely (and dexiotropically) to produce the first quartet of
micromeres (la-Id) nearer the animal pole
and the four yolk-laden first generation
macromeres (1A-1D) at the vegetal pole. In
subsequent successive cleavage cycles two
additional complete quartets of micromeres (2a-2d and 3a-3d) are separated
from second generation macromeres (2A2D) and third generation macromeres
(3A-3D). These divisions lead to the 12-ceII
and 20-cell stages and are, respectively,
laeotropic and dexiotropic. At the 24-cell
stage a micromere spindle appears in the
macromere of only one quadrant. The ensuing laeotropic division separates 4d (the
mesentoblast) from 4D, identifying the left
posterior macromere. Soon after the formation of 4d it divides dexiotropically into
right and left halves. These cells lie to the
right of the future median plane, which is
marked by the second cleavage furrow.
These soon divide again, cutting off a pair
IB
la 1
2b
la 1
3a
3B
3C
FIG. 1. Cleavage of Crepidula (redrawn from Conklin, spindles for 2nd quartet with 1st quartet cells rotated
1897). Top row, left to right: Two-cell resting stage, polarinto macromere furrows. Bottom row, left to nght: De\ioview, showing dexiotropic position of nuclei and asters tropic spindles for 3rd quartet, with central cells, lurprior to their laeotropic rotation; four-cell stage, with ret cells and 2nd quartet constituting cap; 24-cell stage.
nearly radial spindles, prior to their dexiotropic rota- with spindle for 4d (mesentoblast): side view. 29-cell
tion for the third cleavage; laeotropic fourth cleavage stage, showing relation of 4d to 4D.
280
DONALD P. COSTELLO AND CATHERINE HENLEY
of primary enteroblasts posteriorly. The
first bilateral cleavages thus appear suddenly at the 42-cell stage. It is not until the
68-cell stage that the mesoblasts are completely separated from the enteroblasts.
Spiral cleavage of the quartet type does
not necessarily involve two initial equal divisions (Treadwell, 1899). In Nereis (described initially by Wilson, 1892, and with
slight modifications of terminology by Costello, 1945) the first two cleavages are unequal (Fig. 2). Thus one can identify the
four quadrants as early as the 4-cell-stage.
Aside from this inequality and the fact that
the quartets of micromeres are considerably larger in Nereis than in Crepidula, the
basic patterns of spiral cleavage of these
forms are essentially similar. Transition to
bilateral cleavages begins at the 38-cell
stage in Nereis. At this time the primary
mesoblast has just been segregated.
The parallel fates of the cells after the
segregation of ectoblast, mesoblast and
entoblast, in the production of trochophore
or veliger larvae, have been described by a
number of authors for the various annelidan and molluscan species, and will not be
repeated here. Obviously, there are differences, also, especially in later larval development and during metamorphosis.
THREE DEPARTURES FROM THE FOUR-QUADRANT
SYSTEM OF SPIRAL CLEAVAGE
Acoel turbellarians
A simpler type of spiral cleavage, characteristic of the acoel turbellarians was described by Gardiner in 1895; it involves the
formation of only two large macromeres
and successive pairs of micromeres. A suitable system of nomenclature, involving
halves instead of quadrants, and duets of
micromeres instead of quartets, was devised by Bresslau (1909) and employed by
2d
FIG. 2. Cleavage of Nereis (after Wilson, 1892, as modified by Costello, 1945). Top row, left to right: Two-cell
stage, polar view; 4-cell stage, polar view, with vegetal
polar furrow indicated; 8-cell stage, with 1st quartet of
micromeres in dexiotropic position above macromeres. Bottom row, left to right: 16-cell stage, showing
central cells, trochoblasts, 2nd quartet and macromeres; 16-cell stage, from right side; 22-cell stage,
polar view, with 2d about to divide and formation of
the two posterior 3d micromeres. (re-used with permission of the Wistar Press)
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
281
that author (1933) and by Costello (1937, tion. Subsequent cleavages are not clearly
1961).
spiral or oblique in orientation and, like
those
in four-quadrant spirally cleaving
Essentially, the process involves a meridional first cleavage, producing two blasto- eggs, undergo a transition to bilateral divimeres equal in size. The second division is sions, foreshadowing bilaterality in the
not meridional, as in four-quadrant spiral juvenile.
cleavage, but rather is oblique, cutting off
A clue to the possible role of centrioles in
two micromeres (la and lb) at the animal orienting the alternately laeotropic and
pole; it is laeotropic and unequal (Fig. 3). dexiotropic spindles of spiral cleavage by
The first duet of micromeres likewise di- duets in the acoel Polychoerus was offered by
vides obliquely, in a dexiotropic division, to Costello (196la). In this form the 2n (34)
produce la 1 and la 2 , and lb 1 and lb 2 . chromosomes are arranged in a circle at
About this time the two first generation metaphase around the central spindle of
macromeres cleave, in an orientation which the equal first cleavage. At each pole there
is dexiotropic, but tending toward the bilat- is a remarkably large (4.5-5 /im long) roderal condition, resulting in a pair of second shaped centriole, readily visible by light
duet micromeres (2a and 2b) and a pair of microscopy. The axes of the two centrioles
second generation macromeres (2A and are at right angles to one another, and to
2B). At the 8-cell stage, a third duet of the axis of the spindle. Subsequent to the
micromeres (3a and 3b) is produced by a publication of that paper, further study of
cleavage which, again, is laeotropic, with cleavage spindles by light microscopy resome tendency towards the bilateral condi- vealed that replication of these long cen-
FIG. 3. Cleavage of Polychoerus carmelensis (redrawncells, after division of 1st duet; 8-cell stage, after forfrom Costello, 1961). Top row, left to right- Two-cell mation of 2nd duet.
stage; 4-cell stage, side view. Bottom row, left to right: 6
282
DONALD P. COSTELLO AND CATHERINE HENLEY
trioles occurred at their centers, not near
the ends. If daughter centrioles formed by
such a pattern of replication separated
from their mother centrioles, obliquely and
at right angles in the A blastomere as compared with the B blastomere, the second
cleavage spindles thus generated would be
in the precise laeotropic orientation which
has been observed. A similar pattern of centriole replication in the upper cells at the
third cleavage would result in dexiotropically oblique spindles. Thus, in this
case at least, the regular alternation of laeotropic and dexiotrophic divisions for the
early divisions can be explained by the
mode of replication of the centrioles, so
long as the progression is toward the animal
pole. There is no apparent a priori reason
why the same, or a similar, mechanism
could not be the clue to spiral cleavage of
the quartet and monet types as well.
As a matter of historical interest, Figure 4
shows some sketches of the development of
the acoel Polychoerus caudatus, made at
Woods Hole in 1890 by Thomas Hunt
Morgan. They are probably the earliest
camera lucida sketches ever made of duettype spiral cleavage and were never published. Morgan's hand-written comments
accentuate the excitement attendant on
new discoveries at that time. The accuracy
of his observations can be attested by
studies made in 1968 by Costello (also unpublished) of cleavage stages of living eggs
of the California species of Polychoerus.
Bresslau (1933) established the eventual
fates of the cells in acoel embryos, and
showed that the first duet of micromeres
produce ectodermal structures, including
the nervous system. The second and (probably) third duets of micromeres form
epidermis and peripheral parenchyma,
while the fourth duet of micromeres gives
rise to part of the internal mass of the embryo (which, of course, lacks a defined gut).
The fourth generation macromeres likewise contribute to this internal parenchymal mass. Bresslau's observations have
\r
U. (1 1
FIG. 4. Four of Morgan's 1890 sketches, showing a
sequence of cleavage divisions in a living embryo of
Polychoerus caudatus.
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
been confirmed and extended for a
number of other acoel forms by Apelt
(1969).
In the polydad turbellarians, which have
the typical four-quadrant pattern, the four
quartets of micromeres have fates similar to
those described above for the duets of
acoels: the first quartet produces anterior
dorsal ectoderm, eye pigmentation, and
ganglia of the nervous system; the second
quartet cells likewise contribute to the dorsal epidermis, and in addition their progeny produce mesectoderm, forming muscular and mesenchymal portions of the
pharynx. The fate of third quartet cells and
their descendants is similar to that of the
second quartet. Three of the fourth quartet
micromeres (4a-4c) do not divide further
but are nutritive; the fourth member of this
quartet (4d) eventually gives rise to mesoderm and endoderm and, as Kato (1940,
1957 [trans. 1968]) points out, is thus entirely comparable to the mesentoblast cell
of the molluscan embryo.
It is important to emphasize here that the
acoels have direct development, with no intervening larval stage, and hatch as miniature bilaterally symmetrical adults. The
polyclads, in contrast, often produce larval
forms which have at least a superficial resemblance to the trochophores of annelids
and molluscs (see, also, Henley, 1974).
283
which the yolk is still contained. The four
cells were described by Bigelow as becoming "adjusted in a laeotropic arrangement,"
and he points out that even in this early
stage there is a suggestion of coincidence
between this arrangement of the cells and
the future sagittal plane of the embryo. The
third cleavage is "equatorial," and again the
micromeres divide equally and synchronously, while the macromere divides unequally and is slightly retarded, the yolk
again being segregated into the macromere
daughter cell (3D), while the micromere
daughter (3d) contains ectoblast. Bilaterality in cleavage is well established by this
stage. The primary mesoblast cell (4d) is
segregated from the yolk-laden macromere
(4D) at the fourth division, so that at the
16-cell stage the entoblast is completely
separated from the other germ layers.
Bigelow describes the origin of mesoblast as
being dual in nature, part derived from
entoblast at the fourth cleavage and part
from ectoblast at the sixth cleavage. The
four secondary mesoblast cells derived
from the sixth cleavage apparently form "at
least the mesenchyme of the Nauplius."
This includes the musculature of the paired
larval appendages. The blastoderm,
Bigelow emphasizes, is formed from derivatives of three, and only three, micromeres. It is, of course, the first three single
micromeres (Id, 2d and 3d) that give rise to
ectoblast and, later, to the secondary mesoCirripedes
blast. The single fourth micromere of
Bigelow's description is primary mesoblast,
A second major departure from and he refers to the precocious segregation
quartet-quadrant type spiral cleavage was of ectoblast beginning without the previous
found to occur in the cirripede crustacean division of the entoblast into a quartet of
Lepas, as described by Bigelow (1902). The cells. "As a result of this there \s in Lepas one
first cleavage of this egg is unequal and entoblastic macromere instead of four, as in
markedly oblique (Fig. 5), dividing the zy- annelids and molluscs, and single microgote into a smaller anterior cell, mostly meres appear to represent quartets. So far
protoplasmic (the first micromere, Id by as the order of cleavage involved in the
our terminology), and a larger, yolk-laden segregation of the primary germ layers is
posterior cell, the macromere (ID). Next concerned, the first micromere of Lepas apthere is an almost simultaneous "merid- parently corresponds to the first quartet of
ional" division of each of the two blasto- ectoblastic micromeres seen in the eightmeres, which is perpendicular to the first cell stage of such eggs as have four macrocleavage plane; the micromere (Id) divides meres resulting from the [quadrant-formequally, giving rise to two daughters (Id 1 ing] (first and second) cleavages. The
and Id2), while the macromere (ID) has an micromeres of Lepas are, then, according to
unequal division, producing a smaller this view, to be regarded as equivalent to
micromere (2d) and a macromere (2D) in
id
id
FIG. 5. Cleavage of Lepas (redrawn from Bigelow, anaphase, second cleavage, viewed from above animal
1902, but with our designations). Top row, left to right- pole, the oblique line designating the sagittal plane of
Zygote with polar bodies (2nd polar body attached.at the later embryo. Second row, left to right: 8-cell stage
animal pole) and yolk in an eccentric position at the from above animal pole; same, from vegetal pole; 16vegetal pole; first cleavage anaphase in egg under- cell stage from animal pole; same from vegetal pole.
going typical rotation; two cell stage, with clear Third row, left to right: Parasagittal section of late 16-cell
micromere and yolk-containing macromere; late stage; same of later cleavage stage, with primary
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
the quartets of micromeres, while the single
yolk-macromere equals a quartet of
macromeres" (Bigelow, 1902; pp. 124125).
Considering Bigelow's acuity in recognizing the significance of the cell homologies
of Lepas, when compared with those of
many annelids and most molluscs, it is indeed unfortunate that his cleavage terminology was based on Kofoid's four-letter
system. Possibly he was influenced by the
director and/or advisor for his Ph.D. dissertation work. Certainly the Addendum to
Bigelow's 1902 paper, by E. L. Mark and W.
E. Castle (pp. 136-137), containing the remarks about four-quadrant "symmetry"
finding frequent expression in the cleavage
of Lepas, is errant nonsense. In actuality,
Lepas shows unit spiral cleavage instead of
quadrant spiral cleavage, and this involves
monets of micromeres instead of duets or
quartets (Costello, 1948).
This is not idle conjecture. As Bigelow
pointed out, the first cleavage of Lepas is
clearly spiral, involving rotation of spindle
and protoplasmic areas, inclination of the
spindle obliquely with respect to the polar
axis, division into micromere and macromere (with the yolk contained in the latter)
and subsequent shifting of blastomeres. If
one should wish to consider the cleavage of
Lepas a "quadrant" form of spiral cleavage,
there is but one "quadrant," which, by
homology, should be referred to as the "D"
(Fig. 6).
But of far more significance than finding
parallels, as such, between the cleavage patterns of cirripedes, and those of annelids
and molluscs, are the differences, which
demonstrate that the "purpose" inherent in
the cleavage of Lepas is the formation of a
bilaterally symmetrical nauplius larva, and not
285
velopmental mechanics of evolution, and
the role played by adaptation. "Purpose" is
here used in the context employed by Lillie.
The views of Wilson (1895, 1898), Conklin
(1898), Child (1900) and others have been
carefully evaluated also. We shall return to
this point below.
Much later, Anderson (1969) studied the
development of a number of cirripedes
from Australia, and while his observations
confirm the ones made by Bigelow (1902)
on Lepas and by Dels man (1917) on Balanus,
he used a different terminology and came
to far different conclusions. Anderson (p.
221) states: "The cleavage pattern in cirripede crustaceans hatching as planktotrophic nauplii is indisputably . . . a modified total, spiral cleavage. The first two
cleavage divisions segregate four cells as
anterior, posterior, left and right quadrant
cells, of which the former, B and D, retain
transverse contact ventrally while the latter,
A and C, retain median contact dorsally in
the typical spiral cleavage manner. . . . It is
not surprising, therefore, that the spiral
cleavage terminology of Wilson (1892) can
be applied to the cirripede cleavage sequence with very little modification. The
earlier accounts of cell lineage in cirripedes
by Bigelow (1902) and Delsman (1917)
. . . established most of the cleavage sequence described in the present paper, but
both authors obscured the significance of
their results by adopting a terminological
system which rendered comparison with
spiral cleavage almost impossible. .. . The
modifications of spiral cleavage displayed in
the Cirripedia can now be interpreted as
functional changes facilitating cleavage and
gastrulation in a small but densely yolky
of a trochophore or veliger. The similarities
are, perhaps, ancestral reminiscences,
while the differences demonstrate the de-
egg-"
In reality, the obfuscation is equally
complete whether one applies Wilson's
terminology, as Anderson has done, or retains the terminology of Bigelow and of
mesoblasts (ms'bl) divided (bl'po = blastopore); same
of later embryo, with mesoblast band (ms'bl) extending anteriorly along dorsal side at right (en'bl = entoblast); profile of 3-metamere stage, with metameres
separated by transverse furrows (I, 2,), seen from left
side. Fourth row, left to right: Later stage viewed from
left side with third furrow (3) superficially dividing
mandibular metamere; still later, from left side, with
furrow 4 sub-dividing first antennary metamere; dorsal view, same stage, showing longitudinal and transverse furrows which, growing ventrally, fold off the
appendages (at1, at2 = antennary rudiments, md =
mandibular rudiment); napulius, after developing
paired appendages (at1, at2, md) and rudiment of labrum (lbr), seen from left side with ventral surface at
top.
286
DONALD P. COSTELLO AND CATHERINE HENLEY
Zygote
FIG. 6. Table of the cell lineage oiLepas; a translation
of the terminologies of Bigelow (1902) (uppermost of
each of the three designations), Costello and Henley
(this paper) (middle designation) and Anderson
(1969) (lowermost designation), for the blastomeres of
the 2- and 4-cell stages, and for parts of the 8-, 16- and
32-cell stages. Derivation of two of the secondary
mesoblast cells of the 62-cell stage is indicated for
Bigelow's scheme. In parentheses are Bigelow's alternative designations for the three single micromeres,
the single yolk-bearing cells of the several successive
generations, and for the primary and secondary
mesoblast.
Delsman (Kofoid's scheme) since in either
case a four-quadrant terminology is not
applicable to a one-"quadrant" system.
Bigelow, at least, realized the lack of pertinence of the terminology he was employing, while Anderson clearly does not.
Anderson (1969, 1973) describes the
presumptive mesoderm of cirripedes as
arising from only three "stem-cells" (his 3B,
3A, and 3C) of the 33-cell stage, and the
yolk-cell (his 4D) is the presumptive midgut, with all remaining superficial cells the
presumptive ectoderm. The mesoderm
later forms the musculature of the three
paired appendages and leaves a "residual
posterior mass" which gives rise to all postnaupliar mesoderm, mainly through the
activities of teloblasts (p. 231, 1969).
Bigelow, for Lepas, had described at the
62-cell stage as "secondary mesoblast" four
cells of the upper three "stories" (his a75,
b 75 ,b 77 ,c 7 - 5 )and,as primary mesoblast, the
d 52 cell. Anderson (1969, p. 224) is incorrect in stating that Bigelow (and Delsman)
"placed much greater emphasis on 4d,
posterior to the presumptive midgut, as the
main source of mesoderm in cirripede embryos." Bigelow's "primary mesoblast" was,
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
as noted above, his d 52 cell which, by our
translation, would correspond to 2d in Anderson's scheme of nomenclature, not to his
4d. It becomes 4d only in single-"quadrant," monet-type spiral cleavage (our
nomenclature, Fig. 6). Anderson's 4d
would not appear on the scene until two cell
generations later.
In the bilaterally symmetrical cirripede
nauplius, the paired appendages are developed, beginning anteriorly, at what corresponds to three successive levels or
"stories" of the embryo. Since it is essential
that both larval mesoderm and ectoderm be
provided for each pair of appendages,
which are in serial order, it seems logical to
expect that these materials would originate
from derivatives of the single micromeres
of the three generations (i.e., Id, 2d and
3d), located in these positions. There is less
logic to deriving the three pairs of appendages from the anterior, right and left
quadrant cells (B, C and A derivatives, respectively) of Anderson's terminological
scheme. In other words, a terminology
fitting the situation should be employed.
A crustacean embryo has anteroposterior polarity, and ectodermal and
mesectodermal cells covering a single internal endodermal cell, as Bigelow showed.
There is not a great architectural gulf between such an embryo and one developing
from the centrolecithal egg (of a higher
arthropod), with its superficial covering
(derived through cortical nuclear divisions)
enclosing a central undivided yolk mass.
Different methods of arriving at cellulation
and diverse arrangements for the manipulation of yolk are presumably part of the
adaptation-variation saga. And when one
considers the enormous and varied metamorphic changes that occur between
arthropod larval and adult stages in different forms, one might expect correspondingly great variations in the early developmental stages within this diverse group.
287
Cleavage through the 4-cell stage is
definitely spiral, but the following and later
cleavages appear to have lost this characteristic. At the 4-cell stage there is a single
large yolk-bearing cell from which all the
endoderm is later derived (after six more
generations of small cells are given off).
Jennings used a four-quadrant nomenclature (that devised by Kofoid, 1894, for
Limax), which, of course, would not be
applicable in this situation, and describes
this single large cell (from his "quadrant
D") as "passing within the egg" (p. 54). The
ectoderm, derived from the entire "A, B
and C quadrants" plus some small cells (23
in number by the eighth generation) from
the "D quadrant" covers the endodermal
cell. The origin of the mesoblast in rotifers
remained uncertain.
So here, again, is a case of spiral cleavage
seemingly referable to a single "quadrant"
but much less clear than for Lepas.
There is at least one other group, in addition to the cirripedes and rotifers, in which
all the endoderm is derived from a single
cell of the 4-cell stage. This is the Gastrotricha, as described for Lepidodermella by
Sacks (1955). The cleavage of this form
bears many resemblances to that of Lepas.
We do not agree with Ivanova-Kasas (1959)
that this is a duet form of spiral cleavage.
Marked inclination of the spindles in spiral
cleavage by quartets begins at the third
cleavage; by duets at the second cleavage;
and by monets at the first cleavage, as in
Lepas and Lepidodermella.
Now it is clear that spiral cleavage by
quartets leads to the development of a
trochophore (or corresponding type) larva.
The ideal trochophore, such as that ofHydroides (Fig. 7), has the appearance of a spinning top, with apical tuft and incorporated
bilateral features. It is the ciliated prototroch that characterizes the trochophore.
In Nereis (Fig. 8) a somewhat simpler
trochophore is produced, but with the same
general characteristics. During the metamorphosis of the Nereis trochophore larva
into
the juvenile, the Nectochaeta larva
Rotifer
(Fig. 9) has accentuated bilateral features,
A cleavage pattern somewhat similar to which are characteristic of the adult. This
that of Lepas is found in the rotifer brings us again to Lillie and his theory of
Asplanchna, as studied by Jennings (1896). adaptation in cleavage.
288
DONALD P. COSTELLO AND CATHERINE HENLEY
F. R. LILLIE AND THE THEORY OF ADAPTATION IN
CLEAVAGE: A NEW APPLICATION
E. B. Wilson (1892, p. 455) once remarked that "The fundamental forms of
cleavage are primarily due to mechanical
conditions, but are only significant morphologically insofar as they have been secondarily remodeled by processes of precocious segregation." F. R. Lillie agreed
(1895; p. 38) and added that "It is parallel
precocious segregation in different cases
that conditions cell homologies." These observations led him to enunciate his theory
of adaptation in cleavage, which stated (p.
39): "These peculiarities of cleavage are all
due to the precocious segregation of organs
or tissues in separate blastomeres. The
order and character of the segregation
again are ruled by the needs of the embryo.
.. . The peculiarities of the cleavage of
Unio are but a reflection of the structure of
the glochidium, the organization of which
controls and moulds the nascent material."
To many embryologists familiar with
invertebrate materials, Lillie's principle of
adaptation in cleavage is a self-evident
truth, yet there are those who consider it to
be retroactive reasoning. But from a neoDarwinian viewpoint, with infinite possible
variation, selectivity pressure, and relative
survival values, it seems clear that production of highly adapted and easily disseminated larval forms could readily contribute
to main evolutionary trends. 2 Garstang
(1922, p. 82) emphasized, "The real
Phylogeny of Metazoa has never been a direct succession of adult forms but a succession of ontogenetic life cycles. Ontogeny
does not recapitulate phylogeny, it creates
it." And, as has been pointed out (Costello,
1961ft, 1970), only in species with direct
development could ontogeny be closely
parallel to the phylogeny of adult form.
If a biological architect indulging in a
flight of imagination envisioned the
trochophore (Figs. 7 and 8) as one of the
near-ideal ways to disseminate a species,
what better means to create this little spinning top could have been devised than on a
potter's wheel of cleavage with spiral
flourishes? And if, after becoming widely
distributed, the trochophores were destined to settle down and become bilaterally
symmetrical organisms, would it not be essential that provision for this transition be
built in? One may bring this too-simple
analogy closer to reality by pointing out that
the cleavages are not truly spiral, but oblique, and that the "wheel" merely "rocks"
back and forth, alternately dexiotropic and
laeotropic. Furthermore, this regular
alternation could easily lead to bilaterality
in later cleavages by stopping at the halfway
point, like a pendulum coming to rest.
Lillie (1895, footnote, p. 38) excepts from
the principle of adaptation the oblique
character of spiral cleavage and its general
form. But for what reasons do cleavage patterns
vary unless it is to adapt them to the needs of the
embryo} Radial cleavage can lead directly to
the radially symmetrical ciliated blastula of
the echinoderm embryo; spiral cleavage
to the trochophore or veliger; and bilateral
cleavage to various tadpole-like or other
bilaterally symmetrical larvae. If development is telescoped, larval stages are omit2
FIG. 7. Six-day trochophore of Hydroides (after
Hatschek, 1886).
An essentially similar conclusion was reached by
the students of cell lineage of the 1890s (see especially
Conklin, 1897, pp. 198-201). But the great significance
of adaptation in cleavage appears to have been largely
ignored by the more recent generations of embryologists.
SPIRALIAN DEVELOPMENT: A PERSPECTIVE
289
turnings and discardings, to achieve the
adult stage, so long as each adaptation
along the way has had survival value for the
species.This appears to be the case for
-od
fh
forms with complex life cycles. Or there can
be a minimum of deviousness, with no
impedimenta, along the path to the adult,
as in the cases of direct development we
have discussed. Direct development is itself
an adaptation, achieving, as one of its purposes, the conservation of biological materials and energies.
st
In short, we suggest that somewhere in
sd
the evolution of development, for whatever
reason, some zygote followed a modified
mb
spiral cleavage pattern which produced,
FIG. 8. Twenty-hour trochophore of Nereis (after Wil- with minimum expenditure of material and
effort, a successful and viable larva and/or
son, 1892).
juvenile. For the most efficient production
ted, with differentiation to juveniles pre- of a bilaterally symmetrical juvenile, one
ceding the growth transition to adults. As
an example of such direct development, we
can consider that of the squid. Here the
cleavage is not spiral as in other molluscs,
but bilateral; and there is no larva but
rather, direct development to the adult
form. Thus it may readily be seen that here
the "need" of the embryo is to develop the
bilaterally symmetrical condition of the
adult as rapidly as possible. There should
be no wasting of developmental energies on
unnecessary morphogenetic activities.
Thinking in terms of the normal transition from spiral to bilateral, about the only
way one could homologize cephalopod
development with spiral cleavage would be
by assuming that when the transition occurs
sufficiently precociously, there is no spiral
period at all. Bilaterality is, in fact, already
present in the unsegmented squid egg. Arnold (1965) reported no evidence of spiral
cleavage, even during the first two cleavages.3
So we have come to view the evolution of
development as the exploitation of adaptation.
Possibilities for variation are nearly infinite.
There can be a maximum of twistings and
ai.
3
After this account was prepared, a further discussion with Dr. John Arnold revealed that there may,
indeed, be some traces of spiral cleavage in the very
early development ofLoligo. He will perhaps consider
this point in his contribution to the present Symposium.
FIG. 9. Nectochaeta larva of Nereis.
290
DONALD P. COSTELLO AND CATHERINE HENLEY
such "adaptive adoption" of a cleavage pat- Conklin, E. G. 1898. Cleavage and differentiation.
Biol. Lects., MBL, Woods Holl, 1896 and 1897:
tern is spiral cleavage by duets, another by
Ginn, Boston.
monets, a third by purely bilateral cleavage, Costello, D. P. 1937. The early cleavage of Polychoerus
which has lost all vestiges of its spiral nacarmelensis. Anat. Rec. 70:108-109.
ture. These patterns have persisted and Costello, D. P. 1945. Experimental studies on germinal
localization in Nereis. I. The development of isolated
survived because they produced a viable
blastomeres. J. Exp. Zool. 100:19-66.
product, for an existing life-style and Costello,
D. P. 1948. Spiral cleavage. Biol. Bull. 95:265
environment. If, anywhere along the line,
(see, also, Erratum, Biol. Bull. 95:361).
they had taken a wrong turn, so that the Costello, D. P. 1955. Cleavage, blastulation and
gatstrulation. /» B. H. Willier, P. A. Weiss and V.
resulting larva/juvenile was not successful,
Hamburger (eds.), Analysis of development. Saunders,
such cleavage patterns would have been
Philadelphia.
lost.
Costello, D. P. 1961a. On the orientation of centrioles
Admittedly the viewpoints of emin dividing cells and its significance: A new contribution to spindle mechanics. Biol. Bull. 120:285-312.
bryologists are reflections of their personal
philosophies. Much depends on whether Costello, D. P. 1961A.Larva, invertebrate. In P. Gray
(eA.),Encyclopedia of the biological sciences, edit. 1, pp.
they are "splitters" or "lumpers," more con544-549. Reinhold, New York.
cerned with differences or with similarities, Costello, D. P. 1970. Larva, invertebrate. In P. Gray
and upon how they view broad generaliza(ed.), Encyclopedia of the biological sciences, edit. 2, pp.
481-486. Van Nostrand-Reinhold, New York.
tions. But we feel that conjecture can be
useful, as well as entertaining, regardless of Delsman, H. C. 1917. Die Embryonalentwicklung von
Balanus balanoides Linn. Tijdschr. Ned. Dierk. Ver.
whether final solutions to these problems
(2) 15: 419-520.
are forthcoming. This is our perspective. Fol, H. 1875. Etudes sur le developpement des Mollusques. l er Memoire: Sur le developpement des
Pteropodes. Arch. Zool. Exp. Gen. 4:1-214.
Gardiner, E. G. 1895. Early development of Polychoerus caudatus Mark. J. Morph. 11:155-176.
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