TBOPHOBLAST AND SEROSA. 589

Trophoblast and Serosa. A Contribution to theMorphology of the Embryonic Membranes ofInsects.

By

Arthur Willey, D.Sc.Loml., Hon. M.A.Cnntab.,Balfour Student of the University of Cambridge.

THE substance of the following remarks formed the subjectof a paper1 read by me at the last meeting of the BritishAssociation in Bristol.

It is matter of common knowledge that, during the early-stages of development the embryos of insects are protectedby two membranes,—an inner, the amnion, and an outer, theserosa,—which resemble in principle the homonymous foetalmembranes of the higher vertebrates.

Both in the embryos of the Vertebrata Amniota and in thoseof insects, the amnion and serosa are derivatives of the extra-embryonic blastoderm (abstraction being made of the adven-titious mesodermal elements which accompany the membranesin vertebrates), and in both it may be stated in general termsthat the amnion is subsidiary to the serosa. In insects thesecondary character of the amnion, as compared with theserosa, is particularly clearly marked, and it has been recog-nised that the serosa, being a direct derivative of the blas-toderm, is the older structure (Heymons, 4).

The peripheral, extra-embryonic, non-formative epiblast orblastoderm of the mammalian blastodermic vesicle has been

1 Entitled "Considerations bearing upon the Phylogeny of the ArthropodAranion,"

590 ARTHUR WILLBY.

defined as the t rophoblast by Hubrecht (5), since its prin-cipal function is to provide for the nutrition of the embryo.

More recently (6) Hubrecht has published a very remark-able and what I venture to predict will become a classicaltheory of the mammalian trophoblast, in which he seeks todemonstrate a phyletic relationship between the latter and thesuperficial ectoderm ("embryonic epidermis," Balfour; "Deck-schicht," Goette) of the embryos of Amphibia.

Hubrecht points out that the vertebrate amnion is a de-rivative of the trophoblast, which is a structure sui generis.

If the vertebrate amnion, in its capacity of derivative ofthe trophoblast, has a profound phylogenetic significance, onewould be inclined to suppose that an analogous significancewould attach to the embryonic membranes of insects.

Hitherto the prevailing impression seems to have been thatthe latter were of merely cenogenetic importance, and allserious attempts to account for them morphologically havebeen more or less coloured by this assumption.

The embryos of a species of Peripatus which I found inNew Britain last year (1897), of which I have recently pub-lished a full description (14), seem to me to point the way outof this somewhat barren and unsatisfactory position, and toendow the embryonic membranes of insects with a singularinterest. Because, if it could be shown that a common prin-ciple governs the theories applied to the explanation of theembryonic membranes of insects and of those of the highervertebrates, the one theory would constitute an importantcomplement of the other.

On this occasion I am only dealing with the embryonicmembranes of insects, because they are the best known, andmy own observations only bear upon these structures. Therecan be little doubt that the embryonic membranes of scorpionsare capable of being explained in an analogous manner, onlythe data are not sufficient in this case.

My own idea is that three theories are necessary for the ex-planation of the embryonic membranes of scorpions, insects,and vertebrates, and that a common principle underlies the

TBOPHOBLAST AND SEROSA. 591

whole. For the vertebrates, Hubrecht has provided the requi-site theory. The present paper is written for the purpose ofproviding an analogous theory for the insects, while thescorpions must be handed over to posterity.

My chief object is to demonstrate the applicability of theconception of the trophoblast to invertebrate animals; in fact,to show that the serosa of the insect embryo can be tracedback to a primitive trophoblast.

I believe, in short, that the trophoblast, as it is pre-served to us in the embryos of Peripatus novse-brit-annise, arose in adaptation to a viviparous habitacquired by the terrestrial descendant of an aquaticancestor; and that it became transformed, whetherdirectly or by substitution, into the serosa, in corre-lation with the secondary deposition of yolk-laden

In the case of the vertebrates, Hubrecht starts with a pro-tective layer (Deckschicht), which becomes transformed into anutritive layer (trophoblast). For the insects, I commence witha nutritive layer, which becomes changed into a merely pro-tective layer, the serosa. This example will suffice to showthat the two theories are quite distinct in their treatment ofthe respective problems, only they have the principle in commonwhich is expressed in Hubrecht's admirable conception of thetrophoblast.

Just as, throughout the series of the Amniota, the forma-tion of the amnion by no means takes place according to thestereotyped plan with which we are familiar in the chick, so ininsects there is a distinct gradation in the mode andextent of development of the amnion. It attains itscompletest development in the highest order of insects, namelythe Hymenoptera, while its most nascent condition is exhibitedin the most primitive insect in which an amnion has beenfound to occur, namely the Thysanurid, Lepisma saccha-rina, L. (Heymons, 4). The observations of Heymons on thedevelopment of Lepisma are particularly noteworthy. Not

592 ARTHUR WILLBT.

Only is the amniotic cavity of greater relative cnbic capacityin Lepisma than in any other Hexapod, but it never com-pletely closes, remaining permanently open by a minute orifice,the amniotic pore. Thus, in its most primit ive condi-tion, the amniot ic cavity of insects is an open sac.This is in strong contrast with the vertebrate amniotic cavity,as exemplified in the embryo of Erinaceus. Two quotationsfrom Hubrecht's memoir will suffice to call to mind the pointof view adopted by him with regard to the vertebrate amnion.

He says (6, p. 24) : " Ich denke mir das Amnion in seinerallerersten Entstehung gleich als geschlossene Blase;* ichbetrachte somit die Entwickelungsweise durch sich entgegen-wachsende Faltenrander als ein bedeutend cenogenetisch modi-ficirten Entwickelungsprozess."

Again, on p. 25 he says : " Meiner Ansicht nach muss mannicht bei Sauropsiden, sondern bei den Saugern nach Andeu-tungen der primitiveren, der mehr urspriinglichen Amnion-entwickelung suchen."

In Per ipa tus novse-britannise the egg is without yolkand the embryo develops on the surface of a relatively enormousblastodermic vesicle, whose wall consists of an internal layer ofendoderm and an external layer of ectoderm. The ectodermof this trophic vesicle does not consist of flattened and passivecells, as does the serosa of insects, but it is a mucous epithelium,the cells having vacuolar contents and serving for the absorp-tion of nutrient fluids from the uterine wall and their trans-ference to the trophic cavity, whence they are available for thenutrition of the embryo. The trophic ectoderm is there-fore the trophoblast of the embryos of this species ofPer ipa tus . The chorionic membrane always intervenes be-tween the trophoblast and the uterine mucosa.

At first the embryonic tract lies at the posterior ventralextremity of the trophic or blastodermic vesicle, and at thisstage the entire embryo bear? a remarkable resemblance to an

1 The posterior amuiotic canal of Chelonians (Mitsukuri,) and Hatteria(Dendy) requires special explanation.

TROPHOBLAST AND SEROSA. 593

insect egg with the embryonic tract lying upon the yolk (Figs.1, A and B).

At a later stage the trophic vesicle develops a caudal exten-sion, so~[that the embryo attains a more central position,although the cephalic portion of the vesicle is, as a rule, con-siderably larger than the posterior portion (Fig. 2, A).

A B

PIG. 1.—A. Embryo of Peripatus novse-britannise, with embryonictract at posterior ventral extremity of trophic or blastodermic vesicle(original).

B. Egg of Gryllus, with embryonic tract at the posterior ventralsurface of the vitellus. (After Heymons.)

The young embryo rests upon the trophic vesicle as on acushion, and there can be little doubt that in the fresh condi-tion, when the cavity of the vessel is filled to repletion with itsnutrient fluid contents, the embryo lies in a sort of lap or bayor depression, bounded by turgid lips, produced by the inflationof the surrounding thin wall of the vesicle. I cannot statethis as a definite fact as I did not observe the living embryos.Everything, however, points to such a state of things.

594 ARTHUR WILLEY.

As the embryo advances in development; the relative dimen-sions of the trophic organ decrease pari passu with thegrowth of the embryo. The posterior portion of the vesicle isthe first to disappear, being used up in the formation of thedorsal body-wall of the embryo. When there is no longer anycaudal extension of the vesicle there may still be observed a

FIG. 2.—A. Embryo of Peripatus novse-britannise, showing posteriorextension of trophic vesicle and primary ventral flexure of embryonictract. (Original.)

B. Egg of Strongylosoma guerinii, Gerv. (a Diplopod), showingprimary ventral flexure of embryonic, tract. (After Metschnikoff.)

large head-fold, which, in consequence of the cephalic flexuresubsequently undergone by the embryo, is reflected like a capover the ventral surface of the embryo (14, pi. iii, fig. 35).

TROPHQBLAST AND SEBOSA. 595

This head-fold or cephalic portion of the trophicvesicle is attached to the embryo in the nuchal region;in other words, the point at which the final resorption of thetrophic organ of these embryos takes place, lies in the nuchalregion (cf. Fig. 3, A). This fact is of capital importance whentaken in comparison with the remarkable phenomena attendantupon the involution of the serosa of insect embryos.

FIG. 3.—A. Embryo of Peripatus novee-britan niee, in which the posteriorextension of trophic vesicle lias almost entirely disappeared. The ante-rior portion of the vesicle is.present as a large lobe attached to thehead. The figure also illustrates the caudal flexure in addition to theventral flexure of the embryo. (After Willey, 'Zoological Results/Cambridge, 1898.)

B. Egg of Gryllus, at stage after the eversion of the embryo, am.Amnion reflected over dorsum of embryo, ser. Serosa withdrawn toanterior portion of vitellus and attached to head of embryo, like thetrophic vesicle in A. A slight caudal flexure is present, but no ventralflexure. (After Heymons.)

After the amnion of the Insecta Pterygota is formed bythe fusion of tail-fold, lateral folds, and head-folds, the anmiotic

596 ARTHUR WILLEY.

cavity is present as a closed sac, and the amnion itself hascompletely separated from the rest of the blastoderm, whichhas, ipso facto, become converted into the serosa.

At a later stage the amnion enters for a second time, i.e.secondarily, into relations with the serosa, fusing with it nearthe head end of the embryo. The fused area becomes perfo-rated and the embryo undergoes a process of eversioD (revolu-

Micr

.StJ

'Stbl

SUO

F I G . 4..—Egg of F o r f i c u l a after eversion of embryo, with caudal flexure.Micr. Micropjle. am. Amnion reflected over dorsum. ser. Dorsal organ(remains of serosa). St^—St10. Stigmata. Stbl. Stink-gland. (AfterHeymons.)

tion of Wheeler, Umrollung of Heymous and others), evertingitself through the opening thus produced.

The secondary fusion of the amnion with the serosa is theinitial stage in the involution or retrogressive development ofthe serosa. By the eversion of the embryo, the amnion

TR.OPHOBLAST AND SF.ROSA. 597

becomes reflected over the surface of the yolk, while the serosashrinks away towards the anterior end of the egg (Fig. 3, B).Finally the serosa shrivels up until it constitutes the dorsa lorgan of the insec t embryo , which in p r i m i t i v e i n -sects is s i tua ted in the nuchal region, e.g. Lepisma,Gryllus, Forficula (cf. Fig. 4). The dorsal organ is subse-quently withdrawn into the yolk, where it undergoes disinte-gration and absorption.

In the more primitive insects, therefore, the point at whichthe absorption of the serosa into the yolk takes place, lies inthe nuchal region.

The resemblance between the trophic vesicle of the embryoof P e r i p a t u s novse-britanniae shown in Fig. 3, A, with theserosa of the embryo of Gryllus copied from Heymons in Fig.3, Bj is too striking to need further comment. If this were all,I should almost regard the suggested homology between thetfophoblast of my Peripatus embryos and the serosa of insectembryos as a fai t accompl i . But it is not all.

The indusium of the Locustidae described by Wheeler (12),and the dorsal organ (" micropyle," " micropylar organ") ofthe Poduridse have to be taken into consideration. They canonly be accounted for by invoking the aid of hypothesis; butthen every explanation of any structure or phenomenon ismore or less hypothetical.

Since the embryos of P e r i p a t u s novae-bri tanniae haveenabled us for the first time, so far as the Invertebrata areconcerned, to seize upon the most precious conception of thetrophoblast, I think we are not only justified but absolutelycalled upon to face any difficulties which may obscure theapplication of this conception in all its phylogenetic ramifica-tions.

To account for the dorsal organ of the Poduridae and theindusium of the Locustidae, we must call to our aid the prin-ciple of substitution. Without doubt Kleinenberg has left usa noble legacy in his principle of substitution, applicable as itis both to ontogenetic and phylogenetic changes.

I assume that the transformation of the trophoblast into the

598 ARTHUR WILLEY.

serosa took place by substitution, and my meaning can best beillustrated by an observation of my own with regard to theendoderm in the embryos of P. novse-britannise. The tro-phic cavity of the embryo becomes the gastral cavity of theadult, but the exceedingly thin layer of endoderm lining thetrophic cavity does not become the definitive endoderm bysimple continuous growth. On the contrary, the embryonicendoderm undergoes histolytic changes, the cells losing theirmutual contiguity, rounding up and migrating as free t r o -phocytes into the trophic cavity. After this remarkablehistolysis, the endoderm reconstitutes itself, secretes a basalmembrane, and produces the high columnar epithelium of thegut.

Thus, while the gastral endoderm of the adult is derivedfrom the trophic endoderm of the embryo, it is not exactly thesame as the latter since histolytic changes intervene.

The three principal phases in the development of the endo-derm in the embryos of P. novse-britannise may be sum-marised as follows:

I. II. III.Trophic endoderm. Trophocytes. Gastral endoderm.

I regard this method of transformation of trophic endo-derm into gastral endoderm as a special case of substitution,and well adapted to elucidate the significance of the assump-tion that the transformation of the trophoblast into the serosahas taken place by substitution.

Many other still clearer cases of epithelial substitution couldbe adduced. In insects, after the eversion of the embryo andconsequent reflection of the amnion over the yolk, the amnionforms the provisional dorsal wall of the embryo. But itbecomes replaced later by true ectoderm which grows out fromthe pleural edges of the embryo, while the amnion itself under-goes disintegration and absorption (Wheeler, 11, 12; Hey-mons, 2). The origin of the definitive hypodermis of holome-tabolous insects from the imaginal discs is another case inpoint.

TROPHOBLAST AND SBROSA. 599

The above are actual instances of ontogenetic substitution.Instances of phylogenetic substitution can, in the nature ofthings, only be hypothetical.

In the embryos of the Poduridse there is no amnion (Uljanin[10] , Wheeler [ 1 2 ] ) , and therefore no serosa. The blastoderm,however, is not entirely employed in forming the dorsal bodywall of the embryo, since there is a dorsal organ which is some-times spoken of under the name micropylar organ (Wheeler)and spherical organ (Uljanin). This dorsal organ is a localthickening of the blastoderm lying in front of the embryonict rac t ; but at a later stage, when the true topographical rela-tions are established, it is found to lie in the nuchal region (cf.Lemoine's figures [8] ) . It is destined to be absorbed like thedorsal organ of higher insects, which is the product of theinvolution of the serosa.

Appearances are in favour of the Poduridae never havinghad an amnion, but the embryos present the remarkable pecu-liarity that the blastoderm outgrows the vitellus tosuch an extent that it is thrown into numerous complicatedfolds at the surface of the egg. "La superficie de la coucheblastodermique," says Uljanin (10, p. xvii), " devient de plusen plus inegale; cette superficie, beaucoup plus agrandie kcause des inegalite's de la couche blastodermique, secrete unemembrane cuticulaire, cut icule blastodermique, que l'onvoit a travers le chorion de l'oeuf fortement plissee et suivanttautes les inegalite's du blastoderrae e"paissi." Lemoine (8)figures eggs with such a folded blastoderm.

The fact t ha t the blastoderm of Poduridae out-grows the vitellus, involuntar i ly suggests an ata-vistic repet i t ion of a state in which the size of theegg bore no re la t ion whatever to the dimensions ofthe blastodermic vesicle.

The indusium of Locustid embryos is a remarkable structurediscovered by Wheeler (12). It arises as a small circularlocal thickening of the serosa immediately in front of the headof the embryo, i.e. in a position corresponding to the nnchal

600 ARTHUR WILLEY.

region of the embryo at a later stage. According to Wheeler'sperfectly clear account (12), the indusial thickening becomesovergrown by the surrounding serosa, sinks below the surface,becoming entirely separated from the serosa of which it is aderivative, and gradually spreads over the entire egg until itsgrowing edges meet on the dorsal side of the vitellus and fusetogether. The indusium then forms a complete envelope roundthe egg below the serosa, and it completely usurps the functionsof the latter. Why this substitution of an indusium for theserosa should take place in Locustid embryos is a question noteasily answered. At present all that can be said is that ithappens so and there's an end.

In the course of its development, Wheeler found that the

PIG. 5.—Median section of egg of Anurida maritima, showing dorsalorgan with vacuolar cell contents, as a thickening of the blastoderm.(After Wheeler.)

indusium was subject to great time variations, growth varia-tions, and even numerical variations. In two young embryos

TROPHOBLA.ST AND SBROSA. 601

he found that each possessed two separate indusial thickeningsof the serosa or blastoderm.

In its first appearance as a local thickening of the serosa,the indusium has essentially the same topographical relationswith regard to the nuchal region as the dorsal organ of thePoduridse.

Wheeler says (12, p. 56) : " Although much simpler in itsstructure, I do not hesitate to homologise this ' micropylar'organ in Anurida and the Poduridse in general with theindusium of Xiphidium."

Again, with reference to the indusium Wheeler says (p. 58) :" That the organ is rudiraental is shown by its tendency tovary, especially during the earlier stages of its development;that it still performs some function is indicated by its some-what complicated later development, and by its survival in butvery few forms [Locustidse] out of the vast group of Pterygo-tous insects. This seeming paradox may be explained if wesuppose that the indusium was on the verge of disappearing,being the last rud iment of some very ancient s t ruc -tu re . As such a rudiment it no longer fell under the influenceof natural selection, and for this reason began to vary consider-ably like other rudimental organs. Some of these fortuitousvariations may have come to be advantageous to the embryo,and were perhaps again seized upon by natural selection, thenearly extinct organ being thus resuscitated and again forcedto take an active part in the processes of development."

Eventually the indusium undergoes retrogressive develop-ment like the serosa of other forms, and produces an indusialdorsal organ, which, however, is not absorbed but shed(Wheeler [12]).

Accepting Wheeler's view of the homology between thedorsal organ of Poduridse and the indusium of Locustidse, andadmitting that these structures are not the same as the serosaldorsal organ of other insects, we are now in a position todiscuss the bearing of these various observations. A certainamount of repetition is unavoidable if there is to be any

602 ARTHUR WILLEY.

approach to clearness. In the following considerations, factsand hypotheses are given indifferently.

1. The trophoblast of the embryos of Per ipa tus novae-britanniae is a raucous membrane in virtue of its closeproximity to the uterine mucosa; the chorionic membrane,however, always intervening between the trophoblast and themucosa. This is a special case of Driesch's principle of thedependence of function on position—" Die Zelle ist Funktionder Lage."

2. The eggs of P. novse-britannise have retained theprimitive alecithality which must have characterised the eggsof the aquatic ancestor of Peripatus, which presumably spawnedin the water. In connection with the neotropical species ofPeripatus, Kennel was also of the opinion that their lack ofyolk was a primary deficiency, and not a secondary loss.

If this postulate as to the primary character of the aleci-thality of the eggs of my Peripatus be not conceded, my theorywould be thereby practically rendered nugatory.

3. The viviparity of Peripatus is to be regarded as a directresult of the transition from an aquatic to a terrestrial life.This was also Kennel's opinion.

4. In adaptation to the requirements of the intra-uterinenutrition of the embryo, various provisional embryonic trophicorgans were evolved, e.g. dorsal (ectodermal) hump of P.capensis (Sedgwick), trophic vesicle of P. novse-britanniae,trophic sac of P. edwardsii , yolk of P. novse-zealandise.It is neither easy nor necessary to decide which of these camefirst, or whether they were evolved more or less independently.Future investigation of the development of other species, suchas P . tholloni , Bouvier, from the Gaboon district, may throwlight on this matter.1

1 Por facts indicating the relatively primitive character of P. novse-britannise the reader may be referred to my paper (14). According to thedescriptions of Kennel and Sclater, the trophic organ of the embryos of the neo-tropical Peripatus has the form of a spheroidal vesicle, into which the embryois inverted and to the wall of which it is united by an at Brst solid stalk. Thevitelline membrane undergoes early resorption (Kennel), so that the wall ofthe sac comes into direct contiguity with the uterine mucosa. This inversion

TUOPflOBLAST AND SEROSA. 603

5. We may, however, be quite certain that yolk is not themost primitive kind of trophic organ for the intra-uterinenutrition of the embryo, for the simple reason that the accumu-lation of yolk, such as occurs in the eggs of the Australianand New Zealand species of Peripatus, is a step towardssecondary oviposition on terra firma, a condition which isactually realised in the case of the Victorian species, P.oviparus Dendy.

6. The lecithality and deposition of the eggs of insects areboth secondary.

7. With oviparity the trophoblast necessarily ceased to actas an absorbent mucous membrane.

8. The trophoblast therefore became transformed into theblastoderm and its derivative the serosa, by substitution, thisbeing apparently the prevailing method by which an epithelialtransformation or metamorphosis is effected.

9. The serosal dorsal organ of insects is the product of theOntogenetic involution of the serosa.

10. The phylogenetic involution of the trophoblast has alsoto be accounted for, it being understood that the serosa wasnot directly derived from a primitive trophoblast, but by sub-stitution. Although phyletically related, the trophoblast andserosa are therefore not identical structures. Accordingly wemay well expect to find some vestiges of the true primitivetrophoblast cropping up here and there.

11. I see in the dorsal organ of the Poduridse and in theindusium of the Locustidse, vestiges of the true trophoblast,both of these structures presenting, in the earlier stages oftheir development, many of the characters of a mucous mem-brane. This interpretation of facts at least accounts for theotherwise meaningless dorsal organ of the Poduridse (Fig. 5).

12. The dorsal organs of Crustacean embryos and the primi-tive cumulus of Arachnids must require special explanation,

of the embryo shows that this is a special case, and not one from whichphylogenetic conclusions may safely be drawn. An inverted developmentmust necessarily be secondary, as compared with a development which is notinverted.

VOL. 41 , PART 4.—NEW SERIES. X T

604 ARTHUR WILLBY.

my theory assuming the diphyletic origin of the Tracheataand the monophyletic origin of the Hexapoda.1

1 I am aware that the assumption as to the monophyletic origin of theHexapoda is a very grave one to make, and I only make it in the most generalway. It would take one much too far afield to attempt to justify and explainsuch an assumption in detail. At least two authors, Pocock and Kingsley,have made an onslaught against the group of the Myriapoda; and Pocock(R. I. Pocock, "On the Classification of Tracheate Arthropoda," ' Zool.Anz.,1 xvi, 1893, p. 271) has gone so far as to suggest a scheme of classifica-tion, in which the group of the Myriapoda finds no place. Taking the positionof the generative apertures as his criterion, he divides the Tracheata (apartfrom Arachuida) into two large groups, the Progoueata (Diplopoda andPauropoda) and Opisthogoneata (Ohilopoda, Symphyla, Hexapoda). Tbegroup of the Symphyla (Scolopendrella) is one of the utmost importance inphylogeuetic speculations, and there seems to have been some misunderstandingabout it, which however was subsequently corrected (see ' Nature,' vol. xlix,p. liii). Grassi discovered iu 1886 that the unpaired genital pore ofBeolopeudrella lies on the fourth body-segment, and the same statementis contained iu an important memoir by Kenyon (F. C. Kenyon, " The Mor-phology and Classification of the Pauropoda, with Notes on the Morphologyof the Diplopoda," 'Tuft's College Studies,' No. iv, 1895, see p. 136).The Symphyla would seem to be related to the Chilopoda in an analogousmanner to that in which the Pauropoda are related to the Diplopoda. Itwould, in fact, appear that the Symphyla are distinctly intermediate betweenthe Chilopoda and Diplopoda (Cbilognatha), having Chilopod affinities inrespect of their ambulatory appendages, and Diplopod affinities in respect oftheir manducatory appendages and generative organs (consult table at end ofKenyou's memoir). Even if the two principal sub-divisions of the Myriapodawere sharply divergent, I think the loss of the name Myriapoda would out-weigh the profit ol a classification which omitted all mention of the name.As a matter of fact, although well-marked, the Chilopoda and Diplopoda arenot irretrievably divergent.

Nevertheless, it seems not impossible that the Hexapoda have differentialor heterogeneous relations to the Myriapoda. The Insecta Apterygota aredivisible into two well-defined sub-orders, as shown by Stummer-Traunfels,namely the Apte rygo ta en togna tha (Campodeidse, Japygidse, and Col-lembola) aud the Apterygota ectognatha (Machilidse, Lepismidse).(.Rudolf Hitter v. Stummer-Trauufels, " Vergleichende Untersuchungen iiberdie Mundwerkzeuge der Thysanuren und Collembolen," ' S. B. Ak. Wien,'JJd. c, Abth. 1, April, 1891.)

The Apterygota en togna tha (e.g. Campodea) show strong externalresemblance to Scolopendrella, and the embryonic development (Collembola)

TBOPHOBLAST AND SEROSA. 605

Such are the considerations by which I seek to establish aphyletic relationship between the trophoblast, as it is presentedto us in the embryos of P e r i p a t u s novse-britanniae, and theserosa of insect embryos, and for my part I am disposed to becontent with this demonstration. Nevertheless a few wordson the origin of the insect atnnion may not be out of place.In accounting for the serosa we have not, eo ipso, accountedfor the amnion, notwithstanding that they are both derivatives,and inseparable derivatives, of the blastoderm. The amnioticcavity requires special treatment.

Until Heymons discovered the amnion and serosa ofLepisma, he supposed that the embryonic membranes wereto be regarded as a new acquisition of the Insecta Ptery-gota, and that there was no basis upon which to frame anyhypothesis as to their phylogenetic history (2).

For statements of their own views and references to theviews of others, the reader would find it well worth while toconsult the well-known memoirs of Wheeler and Heymons.Suffice it to say here that Heymons (3) has conclusively shownthat the superficial or ectoblastic type of embryonic tractas exemplified in Orthoptera is more primitive than theimmersed or entoblastic type as exemplified in Libellulidseand Ephemeridse.

So far as I have been able to form an opinion from the datawhich are to hand, I t h i n k t h a t t he a m n i o t i c cavi ty ofinsect embryos was originally a product of invagina-tion, and that this invaginat ion was primitively de-rived from and associated with a ventral flexure ofthe embryo.

As already mentioned, Heymons has in fact found that theamniotic cavity of Lepisma is formed by invagination, which isbrought about by the ventral flexure of the embryo, the orifice

strikingly calls to mind that of the Chilopoda, in that a dorsal flexure of theembryo precedes the ventral flexure.

The Apterygota ectognatha, as exemplified in Lepisma, recall in theirembryonic development that of the Diplopoda in respect of the primaryventral flexure of the embryo.

606 ARTHUR WILLEY.

of invagination narrowing down to a small pore which persistsas the amniotic pore. My views, however, differ from those ofHeymons, in that I regard the ventral flexure as primary,while Heymons regards the dorsal flexure of young embryos ofChilopoda and Poduridse as primary, and he thinks that thisdorsal flexure has been lost by the embryo of Lepisma.Knowing what takes place in the embryos of P. novae-bri-tannise, I am quite satisfied that the early ventral flexureof the Chilognatha (Diplopoda) is primitive, and that theprovisional dorsal flexure of the embryos of Chilopoda andPoduridre is a transitory, cenogenetic, intercalated phase ofdevelopment.

The ventral flexure of the embryo of Lepisma is therefore tobe regarded as comparable with the primitive ventral flexurewhich occurs in Chilognatha and in Peripatus (see below).

Heymons says (4, p. 620) :—" Sucht man bei hoherenInsecten nach einem Anklang an die ausgesprochen ventraleKrummung von Lepisma, so ist dieser wohl zweifellos in dervon mir Caudalkriimmung genannten Umbiegung des hinteren

'PF I G . 6.—Sagittal section through embryo of L e p i s m a s n c c h a r i n a , to

show ventral flexure, amniotic cavity, and amniotic pore. Mesoderm andyolk omitted, a. Amnion. c. Amniotic cavity, h. Head end of embryo.p. Amniotic pore. s. Serosa. t. Tail end of embryo. (Simplified afterHeymons.)

Korperendes vieler Insectenembryonen gegeben. Dieselbezeigt sich bei den Orthopteren, den Odonaten, Ephemeriden

TEOPHOBLAST AND SEROSA. 607

fast in alien bisher bekannt gewordenen Fallen, und sie ge-langt selbst dann zum Ausdruck, wenn der Keimstreifen imtTbrigen vollkommen dorsal gekriimmt ist."

I cannot follow Heymons in the above comparison betweenthe ventral flexure of his Lepisma embryos and the caudalflexure of other insect embryos.1

The embryos of P. no vse-britannise undergo threeabsolutely distinct ventral flexures, namely, (1) the primitiveventral flexure, (2) the caudal flexure, and (3) the cephalicflexure; the last-named flexure not being constant. I t is veryimportant to note that t h e r e is no connec t ion whateverbetween the primitive ventral flexure and the caudalflexure (see Fig. 3, A).

The primitive ventral flexure serves the immediate purposeof releasing the primitive streak, i. e. the principal growingpoint of the embryo, from the rest of the embryonic tract, so asto enable it to continue its growth independently of thetrophic vesicle; and it also serves the essential purpose of keep-ing the growing embryo, during its early stages, in as small aspace as possible, in order to admit of the trophoblast cominginto contact with the uterine mucosa (the chorion intervening)over as large an area as possible. The flexure of the embryois sufficiently accounted for on such physiological grounds asthese.

The occurrence of th ree ventral flexures in theembryos of P. novse-britannise cannot be too stronglyemphasised.

In the Myriapods the ventral flexure of the embryo is anessential and characteristic feature of the development, and isto be considered in connection with the absence of an amnion.It takes place at a very early stage in the Chilognatha(Fig. 2, B), while in the Chilopoda it is preceded by a dorsalflexure. The ventral flexure of the Myriapods (with specialreference to the Chilognatha) is quite obviously to be iden-

1 It is, however, quite possible that, in certaiu oases, the caudal flexureand the primary ventral flexure might coincide.

608 ARTHUR WILLEY.

tified with the primitive ventral flexure of the embryo of myPeripatus (cf. Fig. 2, A and u), with the difference that in theMyriapods the Hexure goes much deeper and is much morepronounced than in Peripatus (cf. Metschnikoff [9], andKorschelt and Heider [7]).1

Thus in the Myriapods (as in Peripatus) the ventral flexureof the embryo may be said to be a product of in vagi nation, butthe orifice of invagination does not narrow down at all, remain-ing freely open on all sides.

In Lepisma, as shown by the observations of Heymons, wehave a primary ventral flexure of the embryo, strictly com-parable with the ventral flexure of the Myriapod embryo, andthe invagination which produces the ventral flexure is accom-panied by a narrowing of the orifice of invagination, thusgiving rise to an ainniotic cavity opening by an amniotic pore.

The preceding remarks may be resumed in tabular form asfollows :

P . NOVJE-BBITANNI.E. MVRIAPODA. LEPISMA.

Shallow ventral flexure.2 Deep ventral flexure. Amniotic cavity andAmniotic pore.

Thus although the arunion itself first appears within thegroup of the Hexapoda, it does not owe its origin to purelymechanical causes, as has been so often supposed, but can betraced back, through the link supplied by Lepisma, to theprimitive ventral flexure of ancestral forms.

I think I have now said enough to explain my theory of theembryonic membranes of insects, and I give it for what it isworth. I have endeavoured to trace the serosa back to aprimitive trophoblast, and the amniotic cavity back to a primi-tive ventral flexure.

NEW MUSEUMS, CAMBRIDGE ;

September 22nd, 1898.1 In the embryos oF P. novne-britannise the primary ventral flexure

does not involve the trophic vesicle; whereas in Mjriapods it does involvethe vitellus.

5 That is to say, shallow in its primary relations to the trophic vesicle.

TfiOPHOBLAST AND SEROSA. 609

LITERATURE.

1. HEIDEH, K.—'Die Embryoualentwickelung von Hydrophilus piceus,L.,' Jena (Gustav Fischer), 1889.

2. HEYMONS, R.—' Die Embryonalentwickelung von Dermapteren undOrthopteren,' Jena (Gnstav Fischer), 1895.

3. HEYMONS, It.—" Grundziige der Entwickelung und des Kbrperbanes vonOdonaten und Epliemeriden," ' Abh. k. Akad. wiss.,' Berlin, 1896.

4. HEYMONS, B..—" Entwickelungsgeschichtliclie Untersuchuugen an Le-pisma saccharina,' L., 'Zeifc. f. wiss. Zool.,' Bd. lxii, p. 583,1897.

5. HUBRECHT, A. A. W.—"Keimbliitterbildung und Placeutation des Igels,"' Anat. Anz.,' iii, p. 510, 1888.

6. HUBKECHT, A. A. W.—" Die Phylogenese des Amnious und die Bedeut-ung des Tioplioblastes," ' Ver. Kou. Akad. Wetenschappen/ Amster-dam, 1895.

7. KORSCHELT, E., uud HEIDEH, K.—' Lehrbuch der vergleichenden Eut-wickelungsgeschichte der wirbellosen Thiere,' Jena, 1890-3.

8. LEMOINE, N.—" Recherclies sur le developpement des Podurelles," re-printed from ' Association franpaise pour l'avancement des Sciences,Congres de la Rochelle, 1882,' Paris, Imprimerie Cliaix, 1883.

9. METSCHNIKOFF, E.—" Embryologie der doppeltfiissigen Myriapoden(Cliilognatha)," ' Zeit. f. wiss. Zool.,' Bd. xxiv, p. 253,1874.

10. ULJANIN, W. N.—" Developpement des Podurelles," ' Arch, de Zool.exper.,' t. v, p. xvii, 1876.

11. WHEELER, W, M.—"The Embryology of Blat ta germanica andDoryphora decemlineata," ' Journ. Morph.,' iii, p. 291,1889.

12. WHEELER, W. M.—"A Contribution to Insect Embryology," 'Journ.Morph.,' viii, p. 1, 1893.

13. WILL, L.—" Entwickelungsgeschichte der viviparen Aphiden," ' Zool.Jahrb.' (' Abth. f. Anat. u. Ont.'), iii, p. 201,1889.

Will thought that the immersed or entoblastic (Wheeler) type ofembryonic tract is the more primitive (opinion shared by Heider andWheeler), and "dass das Amnion als ein riickgebildeter oder meta-morphosirter Theil des Keimstreifens aufzufassen ist."

14. WILLEY, A.—"The Anatomy and Development of Peripatus nov£e-britannise," 'Zoological Results, &c.,' part i, p. 1, 1898, CambridgeUniversity Press.

AGESDA.

SCHMIDT, P.—" Beitrage zur Kenntniss der niederen Myriapoden," ' Zeit. f.

wiss. Zool.,' Bd. lix, 1895, p. 436.

CLAYPOLE, A. M.—"The Embryology and Oogeiiesis of Anurida mari-tima (Gu6r.)," 'Journ. Morph.,' xiv, p. 219, 1898.