Form and Function
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E. S. (Edward Stuart) Russell >> Form and Function
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Tackling his main problem of the unity of plan of the vertebrate skull,
Huxley shows, by a careful discussion of the anatomical relationships of
the chief bones in typical examples of all vertebrate classes, that
there is on the whole unity of plan as regards the osseous skull. This
unity of composition can be established, on the gradation method, by
considering the connections of the bones of the skull with one another,
their relations to the parts of the brain and to the foramina of the
principal cranial nerves. The assistance of the embryological method is,
however, necessary in determining many points with regard to the bones
developed in relation to the visceral arches. But there is a further
step to be taken. "Admitting ... that a general unity of plan pervades
the organisation of the ossified skull, the important fact remains that
many vertebrated animals--all those fishes, in fact, which are known as
_Elasmobranchii_, _Marsipobranchii_, _Pharyngobranchii_ and _Dipnoi_
have no bony skull at all, at least in the sense in which the words have
hitherto been used" (p. 571). The membranous or cartilaginous skull of
these fishes shows a general resemblance in its main features to the
ossified skull of other Vertebrates; the relations of the ear to the
vagus and trigeminal nerves are, for instance, the same in both; the
main regions of the cartilaginous skull can be homologised with definite
bones or groups of bones in the bony skull; but discrepancies occur. It
is again to development that we must turn to discover the true
relationship of the cartilaginous to the ossified skull. "The study of
the development of the ossified vertebrate skull ... satisfactorily
proves that the adult crania of the lower _Vertebrata_ are but special
developments[220] of conditions through which the embryonic crania of
the highest members of the sub-kingdom pass" (p. 573). It is with the
embryonic cranium of higher Vertebrates that the adult skull of the
lower fishes must be compared, and the comparison will show a
substantial though not a complete agreement between them. Thus, speaking
of the development of the frog's skull, Huxley writes:--"If, bearing in
mind the changes which are undergone by the palatosuspensorial
apparatus, ... we now compare the stages of development of the frog's
skull with the persistent conditions of the skull in the _Amphioxus_,
the lamprey, and the shark, we shall discover the model and type of the
latter in the former. The skull of the _Amphioxus_ presents a
modification of that plan which is exhibited by the frog's skull when
its walls are still membranous and the notochord is not yet embedded in
cartilage. The skull of the lamprey is readily reducible to the same
plan of structure as that which is exhibited by the tadpole when its
gills are still external and its blood colourless. And finally, the
skull of the shark is at once intelligible when we have studied the
cranium in further advanced larvae, or its cartilaginous basis in the
adult frog" (p. 577). Development, therefore, proves what comparative
anatomy could only foreshadow--the unity of plan of all vertebrate
skulls, ossified and unossified alike. "We have thus attained to a
theory or general expression of the laws of structure of the skull. All
vertebrate skulls are originally alike; in all (save _Amphioxus_?) the
base of the primitive cranium undergoes the mesocephalic flexure, behind
which the notochord terminates, while immediately in front of it the
pituitary body is developed;[221] in all, the cartilaginous cranium has
primarily the same structure--a basal plate enveloping the end of the
notochord and sending forth three processes, of which one is short and
median, while the other two, the lateral trabeculae, pass on each side of
the space on which the pituitary body rests, and unite in front of it;
in all, the mandibular arch is primarily attached behind the level of
the pituitary space, and the auditory capsules are enveloped by a
cartilaginous mass, continuous with the basal plate between them. The
amount of further development to which the primary skull may attain
varies, and no distinct ossifications at all may take place in it; but
when such ossification does occur, the same bones are developed in
similar relations to the primitive cartilaginous skull" (p. 578).
In a word, there is a general plan or primordial type which is
manifested in the higher forms most clearly in their earliest
development--an embryological archetype therefore.
Huxley now goes on to consider the relation of this general plan or type
of the skull to the structure and development of the vertebral column.
Does the skull in its development show any signs of a composition out of
several vertebrae? The vertebral column develops as a segmented structure
round the notochord; the skull develops first as an unsegmented plate
extending far beyond the notochord. The processes of this basilar plate,
the trabeculae, are quite unlike anything in the vertebral column. It is
true that when the process of ossification begins, separate bones are
differentiated in the basilar plate one in front of the other, giving an
appearance of segmentation. The hindmost of these bones, the
basioccipital, ossifies round the notochord, quite like a vertebral
centrum, and its side parts which form the occipital arch develop in a
"remotely similar" way to the neural arches of the vertebrae. The next
bone, however, the basisphenoid, develops in front of the notochord, and
shows very little analogy with a vertebral body. The analogy is even
more far-fetched when applied to the axial bones in front of the
basisphenoid. The cranium might indeed be divided upon ossification into
a series of segments bearing a more or less remote analogy with
vertebrae. "In the process of ossification there is a certain analogy
between the spinal column and the cranium, but that analogy becomes
weaker and weaker as we proceed towards the anterior end of the skull"
(p. 585). The best way to state the facts is to say that both skull and
vertebral column start in their development from the same point, but
immediately begin to diverge. The clear indications of segmentation
which fully ossified adult skulls undoubtedly show are, therefore,
secondary, and the vertebral theory of the skull, which was originally
based upon the appearance of such fully ossified crania, is on the whole
negatived by embryology.
We have now to turn back a few years in order to follow up another line
of discovery which had an important bearing upon the theory of the
vertebrate skull--the working out of the distinction between membrane
and cartilage bones.
As early as 1731, R. Nesbitt,[222] in two lectures delivered to the Royal
College of Surgeons, demonstrated that in the human foetus some bones
were formed not in cartilage but directly in fibrous tissue, and this
observation was confirmed by other human anatomists, particularly by
Sharpey at a considerably later date. In 1822 Arendt[223] focussed
attention upon the remarkable structure of the skull of the Pike, with
its cartilaginous brain-box studded all over with bony plaques, an
arrangement which had already attracted the interest of Cuvier and
Meckel. K. E. von Baer[224] in 1826 discussed at some length the relation
between the bony and the cartilaginous skull in fishes, with particular
reference to the sturgeon, coming to the following just conclusion:--"If
we consider the fibrous skeleton of _Ammocoetes_ as the first foundation
of the skeleton of Vertebrates, we can form a series among the
cartilaginous fishes, according as a cartilaginous skeleton penetrates
more and more into this fibrous foundation. In the same way the process
of ossification supplants the cartilaginous skeleton. So long as the
ossifications lie in the skin, as in the sturgeon, they form corneous
bones (_Hornknochen_), but when they lie under the skin, they form true
bones, _e.g._, the bones of the skull in the pike" (p. 374).
Embryologists soon become aware that a similar distinction between a
primitive cartilaginous foundation and a secondary overlying
ossification of the skull showed itself in the development of all
Vertebrates. Duges, in his _Recherches sur l'osteologie et la myologie
des Batraciens_ (1834), distinguished between such bones as are formed
by direct ossification of the cartilaginous groundwork of the skull, and
such as are developed in the periosteal fibrous tissue.
Reichert in 1838[225] noted that several of the skull bones in Amphibia
are formed without the intermediary of cartilage, such as the nasals,
the maxillaries and the lacrymals. So, too, the frontals and parietals
of Teleosts developed independently of the cartilaginous skull, and
belonged to the skeletal system of the skin, not to the true vertebral
axial skeleton (pp. 215-6). Even more interesting was his discovery,
afterwards confirmed by Hertwig,[226] that in the newt several bones
connected with the palate were formed in the mucous membrane of the
mouth by the fusion of a number of little conical teeth (p. 97). Certain
of these bones he considered to be the substitutes, not the equivalents,
of the palatine and pterygoid of other Vertebrates, which are formed
from the upper part of the first visceral arch, a part missing in the
newt (p. 100). Owing to the difference of development he would not
homologise these bones in the newt with the palatine and pterygoid of
other Vertebrates. He recognised also that the bone now known as the
parasphenoid was developed in the frog in the mucous membrane of the
mouth, and had originally no connection with the cranial basis (p. 34).
Rathke in 1839 also allowed the distinction between cartilage and
membrane bone, but laid no stress upon it (_Entw. d. Natter._, p. 197).
Jacobson in 1842[227] introduced the useful term, "primordial cranium,"
for the primitive cartilaginous foundation of the skull, and drew a
sharp distinction between cartilage bones and membrane bones.
In his _Recherches sur les Poissons fossiles_,[228] L. Agassiz used Vogt's
work on the development of _Coregonus_ to establish a classification of
the bones of the skull in fish, a classification which had the merit of
drawing a sharp distinction between the cartilaginous groundwork and
the "protective plates" of the fish's skull. He recognised that the
protective plates developed in a different way from the other bones of
the skull. "We must distinguish," he writes, "two kinds of ossification;
one which tends to transform the primitive parts of the embryonic
cranium directly into bone, and another which leads to the deposition of
protective plates round this core, which develop not only upon the upper
surface, as has hitherto been supposed, but also on the lateral walls
and on the lower surface of the cranium" (p. 112). In the skull of all
fish there are three elements--(1) the cartilaginous base, including the
nuchal plate, the trabeculae and the facial plate, together with the
auditory capsules; (2) the cartilaginous cerebral envelope; (3) the bony
protective plates (absent in Elasmobranchs). The bones developed in
relation to these cranial elements can be classified as follows:--(1)
the basioccipital, exoccipitals (paroccipitals?), supraoccipital and
"petrous" (_rocher_), developed from the nuchal plate; the ali- and
orbito-sphenoids developed from the trabeculae; the "cranial ethmoid"[229]
developed from the facial plate; (2) the parietals, frontals and nasals
formed from the "superior" protective plate; the "anterior" and
"posterior" frontals and the temporal, from the "lateral" plates; the
body of the sphenoid and the vomer from the "inferior" plates. The other
element, the cartilaginous brain-box, does not ossify, and tends to
become absorbed (p. 124).
In 1849 Koelliker published a paper[230] dealing with the morphological
significance of the distinction between membrane and cartilage bones,
and in 1850[231] he defended his views against the criticisms of
Reichert[232] in a further note entitled _Die Theorie des
Primordialschaedels festgehalten_. It is convenient to consider these
papers together. Koelliker held that there was (1) a histological and (2)
a morphological difference between the two categories of bones. The
histological development of the two kinds was different, but this
difference was not sufficient to establish a morphological distinction
between them, a distinction in their anatomical _Bedeutung_. The true
morphological distinction between them was their development in
different skeleton-forming layers. Membrane bones were developed in
fibrous tissue lying between the skin and the deep layer which formed
the primordial cranium, and it was this formation in a separate layer
that gave them a different morphological significance from the bones
formed directly in the deep layer. Koelliker's distinction, therefore,
was between the bones formed in the primordial cartilaginous cranium on
the one hand, and the superficial ossifications in fibrous tissue on the
other hand. The cartilaginous cranium in Koelliker's opinion was formed
upon the vertebral type, and the membrane bones were accessory. This, at
least, was his opinion in 1849. In 1850, after Stannius had shown that
membrane bones occurred as integral parts of the vertebrae in certain
fish, he modified his view of the membrane bones, and admitted them, at
least in some cases, as constituents of the cranial vertebrae.
On this morphological distinction of membrane and cartilage bones future
comparative osteology was to be based:--
"My sole aim is to state again the principle upon which comparative
osteology is to be based and extended, and this is that first place
should be assigned to anatomical considerations, and among these to the
manner of origin of the whole bone in relation to the skeleton-forming
layers" (1850, p. 290).
The homologies established by this new principle might run counter to
the homologies indicated by the study of adult structure. "Thus, for
instance, although the lower jaw in position, function, form and shape,
appears to be the same bone throughout, yet it must be admitted that it
shows a difference in the different classes. In Mammals and Man it is an
entirely secondary bone (an extremity according to Reichert), in Birds,
Amphibia and Fishes only partially so, for its articular belongs to
Meckel's cartilage and is accordingly analogous to a rib; indeed, in the
Plagiostomes, etc., the whole lower jaw along with the articular is a
persistent Meckel's cartilage" (p. 290, 1850).
So, too, the supraoccipital in man cannot be fully homologised with the
supraoccipital of many mammals, for its upper half arises at first in
isolation as a secondary bone (p. 290).
Reichert objected to the distinction drawn by Koelliker, and denied that
there was either a histological or a morphological difference between
membrane and cartilage bones. It was shown a few years later by H.
Mueller[233] that there was in truth no essential difference in
histological development between the two categories of bone, that the
cartilage cells were replaced by bone cells identical with those taking
part in the formation of membrane bones. The morphological distinction
continued however to be recognised, particularly by the embryologists.
Rathke in his volume of 1861[234] classified the bones of the skull
according to their origin from the primordial cranium or from the
overlying fibrous layer, distinguishing as membrane bones, the
parietals, frontals, nasals, lachrymals, maxillaries and premaxillaries,
jugals, tympanic, parts of the "temporal," vomer, part of the
supraoccipitals in some mammals, and the mandible (with the exception of
the articular in such as have a quadrate bone). Huxley was also inclined
in 1864[235] to recognise the distinction, but he writes with some
reserve:--"Is there a clear line of demarcation between membrane bones
and cartilage bones? Are certain bones always developed primarily from
cartilage, while certain others as constantly originate in membrane? And
further, if a membrane bone is found in the position ordinarily occupied
by a cartilage bone, is it to be regarded merely as the analogue and not
as the homologue of the latter?" (p. 296).
We may note here that many comparative anatomists of the period were
quite ready to decide Huxley's last question in a sense favourable to
the older, purely anatomical, view of homology. Owen, for instance, held
that difference of development did not disturb homologies established by
form and connections. "Parts are homologous," he writes, "in the sense
in which the term is used in this work, which are not always similarly
developed: thus the 'pars occipitalis stricte dicta,' etc., of
Soemmering is the special homologue of the supraoccipital bone of the
cod, although it is developed out of pre-existing cartilage in the fish
and out of aponeurotic membrane in the human subject."[236] Similarly he
pointed to the diversities of development of the vertebral centrum in
the different vertebrate classes as proof that development could not
always be relied upon in deciding homologies (p. 89). But he could not
deny that the archetype was better shown in the embryo than in the adult
(_supra_, p. 108).
J. V. Carus[237] likewise stood firm for the older method of determining
homologies by comparison of adult structure. "We can regard as
homologous," he writes, "only those parts which in the fully formed
animal possess a like position and show the same topographical relations
to the neighbouring parts" (p. 389). Parts homologous in this sense
might develop in different ways, but no great importance was to be
attached to such a circumstance. Membrane and cartilage bones developed
in practically the same way, from the same skeleton-forming layer, and
no morphological significance attached to their distinction (pp. 227,
457). Embryology was of considerable value in helping to determine
homologies, but the evidence that it supplied was contributory, not
conclusive. Perhaps the greatest service which the study of development
rendered was to disentangle, by a comparison of the earliest embryos,
the generalised type (p. 389).
We have now traced, by our historical study of the theory of the skull,
the gradual evolution of the tendency to find in development the surest
guide to determining homologies. We have seen how the embryological
"type" came to be substituted, in whole or in part, for the anatomical
"type" derived from the study of adult structure. But we have had to do
only with a modification, not with a transformation, of the criterion of
homology recognised by the anatomists. Homology is still determined by
position, by connections, in the embryo as in the adult. "Similarity of
development" has become the criterion of homology in the eyes of the
embryologist, but "similarity of development" means, not identity of
histological differentiation, but similarity of connections throughout
the course of development. For the purposes of morphology, development
has to be considered as an orderly sequence of successive forms, not in
its real nature as a process essentially continuous. Morphology has to
replace the living continuity by a kinematographic succession of stages.
Since it is the earliest of these stages that manifest the simplest and
most generalised structural relations of the parts, it is in the earlier
stages that homologies can be most easily determined. But these
homologies are still determined solely by the relative positions and
connections of the parts, just as homologies are determined in the last
of all the stages of development, the adult state. And since the
generalised type is shown most clearly in the earliest stages and tends
to become obscured by later differentiation, homologies observed in
embryonic life are to be upheld even if the relations in adult life seem
to indicate different interpretations.
[183] See review by Cuvier, _Mem. Mus. Hist, nat._, iii.,
pp. 82-97, 1817.
[184] _Mem. Savans etrangers_, vi. Extract in _Ann. Sci.
nat._ (2) i. (_Zool._), pp. 366-72, 1834.
[185] _Recherches sur la generation des Mammiferes_, 1834.
_Embryogenie comparee_, 1837.
[186] "Kiemen bey Saeugthieren," _Isis_, pp. 747-9, 1825.
[187] "Kiemen bey Voegeln," _Isis_, pp. 1100-1, 1825.
[188] "Ueber die Kiemenbogen und Kiemengefaesse beym
bebrueteten Huehnchen," _Isis_, xx., pp. 401-3, 1827.
(Read in Sept. 1826 to the _Versammlung der deutschen
Naturforscher und Aerzte_, then recently founded by
Oken).
[189] _Isis_, pp. 160-4, Pl. II., 1828.
[190] "Ueber die Kiemen und Kiemengefaesse in den Embryonen
der Wirbelthiere," Meckel's _Archiv_ for 1827, pp.
556-68. Also in _Ann. Sci. nat._, xv., pp. 266-80,
280-4, 1828.
[191] Meckel's _Archiv_, vi., pp. 1-47, 1832.
[192] _Untersuchungen ueber die Bildung und Entwickelung
der Fluss-Krebses_, Leipzig, folio, 1829. Preliminary
notice in _Isis_, pp. 1093-1100, 1825.
[193] "Untersuchungen ueber die Bildung und Entwickelung
der Wasser-Assel.," _Abh. z. Bild. u. Entwick.-Gesch._,
i., pp. 1-20, 1832. Translated in _Ann. Sci. nat._ (2),
ii., (_Zool._), pp. 139-57, 1834.
[194] Koelliker, _Entwickelungsgeschichte_, 2nd ed., p. 17,
Leipzig, 1879.
[195] _Handbuch der Entwickelungsgeschichte des Menschen
und ... der Saeugethiere und Voegel_, Berlin, 1835.
[196] _Embryogenie comparee_, 1837; _Histoire generale du
developpement des corps organises_, 1847-49.
[197] _Entwickelungsgeschichte des Kaninchen-Eies_,
Braunschweig, 1842; _Entwickelungsgeschichte des
Hunde-Eies_, Braunschweig, 1845;
_Entwickelungsgeschichte des Meerschweinchens_, Giessen,
1852; _Entwickelungsgeschichte des Rehes_, Giessen,
1854.
[198] "It is the role of embryology, as my great teacher
says, to form the court of appeal for comparative
anatomy, and it is from embryology particularly, which
has in the last decades provided such signal instances
of the unravelling of obscure problems, that we have to
expect a definite clearing up of the problems relating
to the development of the head."--Mueller's _Archiv_, p.
121, 1837.
[199] _Anat.-phil. Unters. ue. d. Kiemenapparat u. d. Zungenbein_, Riga
and Dorpat, 1832.
[200] "Bildungs- und Entwickelungs-geschichte des Blennius viviparus,"
_Abhandl. z. Bild. u. Entwick.-Gesch. des Menschen u. der Thiere_,
ii., pp. 1-68, Leipzig, 1833.
[201] _Von den Ur-Theilen des Knochen und
Schalen-Gerustes_, Leipzig, 1828.
[202] _Kiemenapparat_, pp. 107-118.
[203] _Vergleichende Anatomie der Myxinoiden_. Part I.
(Osteology and Myology). (_Abh. koenigl. Akad. Wiss.
Berlin_, for 1834, pp. 65-340, 9 pls., 1836.) Also
separately.
[204] "Ueber die Visceralbogen der Wirbelthiere in
Allgemeinen und deren Metamorphosen bei den Voegeln und
Saeugethiere," Mueller's _Archiv_, pp. 120-222, 1837.
[205] _Handbuch d. menschl. Anatomie_, iv., p. 47.
[206] This was shown by Serres (_Ann. Sci. nat._, xi., p.
54 f.n., 1827), who found in a human embryo a long
cartilaginous piece extending from the ear-ossicles to
the inside of the lower jaw, and suggested that it was
the foundation of the permanent mandible.
[207] _Abhandl._, i., p. 102, 1832; ii., p. 25, 1833. (_Blennius_
paper).
[208] _Vergleichende Entwickelungsgeschichte des Kopfes der nackten
Amphibien_, Koenigsberg, quarto, 276 pp., 1838.
[209] Mueller's _Archiv_ for 1838.
[210] _Entwickelungsgeschichte der Natter_, Koenigsberg,
1839.
[211] _Bemerkungen ueber die Entwickelung des Schaedels der
Wirbelthiere_, Koenigsberg, 1839.
[212] _Handbuch der Physiologie des Menschen_, Koblenz,
1835; Eng. trans. by W. Baly, ii., p. 1615, 1838.
[213] For a full statement of Rathke's conclusions, see
the translation given by Huxley in _Lectures on the
Elements of Comparative Anatomy_, London, 1864.
[214] _Entwickelungsgeschichte der Wirbelthiere_, p. 142,
1861.
[215] _Embryologie des Salmones_. A separate volume of L.
Agassiz's _Histoire naturelle des Poissons d'Eau douce
de l'Europe centrale_, Neuchatel, 1842.
[216] _Untersuchungen ueber die Entwickelungsgeschichte der
Gebuertshelferkroete_, Solothurn, 1842.
[217] Mueller's _Archiv_ for 1843, p. ccxlviii.
[218] _Untersuchtingen ueber die Entwickelung der
Wirbelthiere_, Berlin, 1850-55.
[219] Delivered 17th June 1858. Reprinted in _The
Scientific Memoirs of T. H. Huxley_, edited by M. Foster
and E. Ray Lankester, vol. i., pp. 538-606 (1898).
[220] _Cf._ Reichert, _supra_, p. 149.
[221] The origin of the pituitary body from the roof of
the mouth was first described by Rathke (1839).
[222] _Human Osteogeny explained in two Lectures_, London,
1736.
[223] _De capitis ossei Esocis lucii structura singulari.
Dissert. inaug._ Regiomonti, 1822.
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