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Emil Selenka on the embryonic membranes of the mouse and placentation in gibbons and orangutans
Placenta 37 (2016) 65e71
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Emil Selenka on the embryonic membranes of the mouse and placentation in gibbons and orangutans A.M. Carter a, *, R. Pijnenborg b a b
Department of Cardiovascular and Renal Research, University of Southern Denmark, DK-5000 Odense, Denmark Department of Development and Regeneration, Katholieke Universiteit Leuven, B-3000 Leuven, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 October 2015 Received in revised form 13 November 2015 Accepted 16 November 2015
Background: Emil Selenka made important contributions to embryology in marsupials, rodents and primates that deserve wider recognition. Here we review his work on early development of the mouse and placentation in the great apes. Findings: Selenka was intrigued by germ layer theory, which led him to study inversion of the germ layers in the mouse and other rodents. He found it was growth of the ectoplacental cone that caused a downward shift in the position of the underlying ectoderm and endoderm, leading to an inside-outside inversion of these layers. In primates he made the important discovery that the embryos of gibbons and orangutans develop under a decidua capsularis. Thus all great apes, including humans, exhibit interstitial implantation; this is in contrast to other primates where implantation is superficial. Conclusions: Selenka's work was thorough and brilliantly illustrated. It was an important influence on his contemporaries and was well known to scientists of the following generation. Embryologists continue to advance our knowledge of fetal membranes and placentation in the mouse, but Selenka's work on gibbons is unique and our knowledge of orangutan placentation is restricted to his specimens. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Decidua capsularis Germ layers History of science Interstitial implantation
1. Introduction Emil Selenka was the first to show the presence of a decidua capsularis in gibbons and orangutans, a feature they share with the human. As implantation is superficial in New and Old World monkeys [1], these observations are important, because they imply that primary interstitial implantation evolved in the ancestral lineage of great apes. Selenka's work on the early development of gibbons [2] is unsurpassed. His orangutan material, described after his death by Strahl [3], is unique. Largely forgotten is Selenka's work on rodents. Yet he was the first to describe the early development of the germ layers in the mouse and to explain how inversion of the germ layers came about [4]. His work on rodents is rarely cited compared, for example, to Sobotta [5], who built further on Selenka's legacy, and Matthias Duval [6e8], who tended to downplay it. Selenka's work encompassed several other mammals including marsupials (Table 1). Thus he was among the first to detail development of the opossum (Didelphis virginiana) [9] and the first to
* Corresponding author. E-mail address: [email protected] (A.M. Carter). http://dx.doi.org/10.1016/j.placenta.2015.11.005 0143-4004/© 2015 Elsevier Ltd. All rights reserved.
describe yolk sac placentation in the Tasmanian bettong (Bettongia gaimardi), gray cuscus (Phalanger orientalis) and common brushtail possum (Trichosurus vulpecula) [10]. This required him to establish breeding colonies for the Australian species. Our aim is twofold: to draw attention to Selenka's work and encourage consultation of his original papers. To this end we have included a bibliographical note and a key to the mammals he studied in which the nomenclature employed by Selenka is compared to that currently in use.
2. Biographical sketch Emil Selenka (Fig. 1) was born 27 February 1842 in Braunschwieg, capital of the independent Duchy of Brunswick. His father, Johannes Jacob Selenka, was a master bookbinder and prominent citizen who founded an arts and crafts school that was the forerunner to the Braunschwieg University of Art [11]. The forecourt of the present day University is named JohanneseSelenkaePlatz. Emil Selenka studied at the local technical college and the €ttingen. His doctoral thesis [12] dealt with the University of Go systematics of sea cucumbers (Holothuroidea). It led to his appointment, at the age of 26, to the Chair of Zoology at Leiden.
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Table 1 Key to the mammals studied by Selenka and the current nomenclature (Wilson and Reeder [50]). Family
Genus and species names used by Selenka
Current classification
Source
Didelphidae Dasyuridae Phalangeridae
Didelphis virginiana Shaw Dasyurus viverrinus Phalangista vulpine Desmarest P. orientalis Waterhouse Hypsiprymnus cuniculus H. penicillatus Waterhouse Arvicola arvalis Pallasa Mus sylvaticus L. Mus musculus L. Mus decumanus Pallas Cavia cobaya Marcgrav Pteropus edulis Tragulus javanicus Cebus fatuellus [L.]b Mycetes seniculus [L.]b Cercocebus cynomolgus Cuvier Macacus nemestrinus Desmarest Semnopithecus maurus Cuvier S. pruinosus Desmarest S. mitratus Eschsholtz S. nasicus Schreber S. cruciger Thomas S. cephalopterus [Boddaert] S. rubicundus [Müller]b Inuus speciosus [F. Cuvier]c Hylobates concolor Harland H. Mülleri H. agilis Cuvier H. Rafflesi? H. leuciscus Schreber Siamanga syndactylus Raffles Simia satyrus Linne
Didelphis virginiana Kerr Dasyurus viverrinus Shaw Trichosurus vulpecula Kerr Phalanger orientalis Pallas Bettongia gaimardi Desmarest Bettongia penicillata Gray Microtus arvalis Pallas Apodemus sylvaticus L. Mus musculus L. Rattus norvegicus Berkenhout Cavia porcellus L. Pteropus vampyrus L. Tragulus javanicus Osbeck Cebus apella L. Alouatta seniculus L. Macaca fascicularis Raffles M. nemestrina L. Geoffroy Trachypithecus auratus E. T. cristatus Raffles Presbytis melalophos Raffles Nasalis larvatus Wurmb Presbytis chrysomelas Müller Trachypithecus vetulus Erxleben Presbytis rubicunda Müller Macaca fuscata Blyth Hylobates albibaris Lyon H. muelleri Martin H. agilis F. Cuvier H. agilis F. Cuvier H. moloch Audebert Symphalangus syndactylus Raffles Pongo pygmaeus L.
Brazil and laboratory bred Not known Australia and laboratory bred Australia and laboratory bred Not known Australia and laboratory bred Not stated Erlangen, Germany Laboratory bred Laboratory bred Laboratory bred Not known Java, Borneo (?) Not stated Not stated Java, Borneo, Malacca Borneo Java Borneo Java Borneo Borneo Ceylon Borneo? Japan Borneo Borneo Sumatra Sumatra Java Sumatra Borneo
Hypsiprymnodontinadae Cricetidae Muridae
Caviidae Pteropodidae Tragulidae Cebidae Atelidae Cercopithecidae
Hylobatidae
Hominidae a
This is the common vole, but the German name Feldmaus has been translated by some authors as field mouse. Described by Strahl and Happe [51]. Described as Macacus speciosus by Strahl and Happe [51]. d The species name is now reserved for Nomascus concolor, which does not occur on Borneo [52]. The most important specimen mentioned as Hylobates concolor was collected by Selenka on the left bank of the River Kapuas and therefore can be assigned to H. albibaris [53]. b c
Here he continued to work on marine invertebrates. During this period he founded what is now the Royal Dutch Zoological Society. He also hosted a doctoral student from the University of Utrecht, Ambrosius Hubrecht [13], who was to become a lifelong friend and intellectual sparring partner. In 1874, after 6 years in the Netherlands, Selenka was called to a Chair at Erlangen. It was now that he began to focus his attention on developmental biology. The opening statement of his first important paper, again on sea cucumbers, explains his motivation [14]. He thought it important to determine the origin of echinoderms and the fossil record had failed to provide convincing answers. Therefore it was important to try a new approach based on embryology. He continued along similar lines with a major study of the early development and larval stages of sea urchins (Echinoidea) [15]. His work on marine invertebrates also encompassed saltwater planarians, but around 1882 he switched gears and began his studies of mammalian development, at first in rodents and marsupials. Gradually Selenka developed a desire to link his animal studies to ontogenesis in human beings and for this he needed primate material. To this end he embarked upon two expeditions to the Dutch East Indies, accompanied by his second wife Lenore. They also visited Ceylon and Japan. During the second trip, Selenka fell seriously ill with malaria and went to convalesce in the Himalayas, whilst Lenore spent several more months in Borneo. Both husband and wife were interested in ethnography and their travel book, “Sonnige Welten,” was a bestseller that went into three editions [16]. Margarethe Lenore Selenka was a prominent feminist and is
better remembered than her husband; there is now a MargaretheeSelenkaeStrasse in Munich. Selenka had accumulated an impressive amount of material. One recent estimate is that he and his staff shot around 400 orangutans [17]. Conscious of the toll, he determined to make full use of the animals and embarked on studies of the skeleton and dentition of the great apes. His collection of orangutan skeletons at Munich (Die Zoologische Staatssammlung München, ZSM) is still an important resource [18]. In 1895, better to devote his time to research, Selenka resigned his Chair at Erlangen and moved to Munich, where he had the status of honorary professor. He died there in 1902, just before his 60th birthday, leaving the work unfinished. As we shall see, it was continued by his colleagues, particularly Hubrecht and Hans Strahl [19]. For further details of Selenka's life and early work, including a complete bibliography, reference should be made to Hubrecht's obituary [20]. A briefer but more accessible account is given by Lubosch [21].
3. Rodents 3.1. Germ layer theory In his studies of invertebrates, Selenka had been much concerned with the germ layers; his paper on sea cucumbers had the subtitle, “A contribution to germ layer theory” [14]. The prevalent view was that each germ layer (ectoderm, mesoderm and endoderm), regardless of species, gave rise to a fixed set of organs. This
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towards the uterine lining. In between, however, there remained the yolk sac cavity and the outer wall of the yolk sac comprising parietal endoderm and trophoblast. This state is sometimes referred to as “incomplete inversion.” Disappearance of the outer wall occurs later in development of the mouse; there is then said to be “complete inversion” [24]. An important causal element in the inversion process of the germ layers in the mouse is the proliferation of a group of cells, now known as the ectoplacental cone, referred to as a “Zapfen” (plug) in €ger” Bischoff's study of the guinea-pig [28], but renamed as the “Tra by Selenka [4], a more general term which would fit better with observations in other related rodent species. In Selenka's view it €ger which caused a downward was the inward growth of the Tra shift in the position of the underlying ectoderm and endoderm, leading to an inside-outside inversion of these layers. The term Tr€ ager must be one of the very few German terms which regularly turn up in the older English literature (e.g. Refs. [29,30]). The now ^ ne common term “ectoplacental cone” was introduced by Duval (co ectoplacentaire), who also studied this inversion process in order rifier les to, “confirm the elegant studies of Selenka on this topic” (ve belles recherches de Selenka sur ce sujet) [6]. After expressing his admiration for Selenka's study of early mouse embryos, however, €ger to the he criticized him for not relating the formation of the Tra subsequent development of the placenta, which was rectified by Duval's altered term ‘ectoplacental cone’. Furthermore, Duval noted Selenka's mistaken identification of the (trophoblastic) giant cells surrounding the implanting blastocyst as decidual cells. 3.3. Germ layer inversion in the guinea pig and other rodents
Fig. 1. Emil Selenka (1842e1902): German zoologist and embryologist. Reproduced from Ref. [20].
concept was shortly to be refuted by the eminent Swiss embryol€lliker [22] and was eventually demolished by ogist Albert von Ko experimental embryologists (reviewed in Ref. [23]). Their experiments proved there was no fundamental difference between the three layers. However, that was in the future. There is little doubt that germ layer theory strongly influenced the thinking of Selenka and his contemporaries. 3.2. Germ layer inversion in the mouse Inversion of the germ layers is a process by which the endoderm of the embryonic hemisphere is everted toward the uterine lining [24]. Inversion of the germ layers was known to occur in the guinea pig embryo, but there had been no satisfactory explanation of how this was brought about. Selenka's contribution was to show that inversion of germ layers occurred in the mouse and demonstrate the mechanism by which this was achieved [4,25]. He was not alone in working on this problem and his paper appeared in the same year as Fraser's on the rat [26] and Kupffer's on the common vole [27]. In the mouse, Selenka [4] found that the primitive endoderm (hypoblast) was present at implantation and isolated endodermal cells had spread to the inside of the blastocyst cavity (Fig. 2A). Shortly afterward, eversion of the embryonic hemisphere had commenced resulting in inversion of the germ layers (Fig. 2B). The endoderm covering the embryo (visceral endoderm) now faced out
Having identified the events underlying germ layer inversion in the mouse, Selenka [31] attempted to extend this analysis to other rodents. He argued convincingly for a similar process in the rat (Rattus norvegicus) and field mouse (Apodemus sylvaticus) and drew a credible parallel to a cricetid rodent, the common vole (Microtus arvalis). In this he combined his own observations with those of Fraser [26] and Kupffer [27]. His main object of study, however, was the guinea pig (Cavia porcellus), and here he found a somewhat different situation. Perhaps most significant was the precocious €hle), which distanced appearance of the exocoelom (Interamnionho the embryonic ectoderm from the extraembryonic ectoderm of the Tr€ ager (Mossman [24] names this cavity the precoelom). He noted in addition the failure of extraembryonic endoderm to line the trophoblast and form a true yolk sac. The trophoblast itself persists in early stages, a detail that was lost in some later studies but confirmed by the eminent Cambridge embryologist J. T. Wilson [32]. Otherwise, Selenka's [31] account added little to that of Bischoff [28] and is in any case less widely known than the later study by Duval [33]. It is worth consulting mainly for the exquisite detail of the illustrations and the schematic comparison of early development in the rabbit and five species of rodent (Plate XVI in Ref. [31]). 4. Primates Selenka's most important work concerned the early development and placentation of Old World monkeys and great apes and was based on specimens he collected in Indonesia (Table 1). 4.1. Gibbons The first publication concerned the development of gibbons [2]. It is especially important for establishing the presence of a decidua capsularis in gibbons (Fig. 3A) and his recognition that this feature distinguished all the great apes from the Old World primates. Of
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Fig. 2. Inversion of germ layers in the mouse (Mus musculus). A. Implanting blastocyst. The primitive endoderm (or hypoblast) is apparent and one cell has migrated to the inside of the blastocyst wall. Reproduced from Selenka [4]. B. Growth of the ectoplacental cone (extraembryonic ectoderm) has pushed the epiblast down into the yolk sac cavity. As a result the visceral endoderm faces outwards (germ layer inversion). The parietal endoderm provides a partial lining to the yolk sac cavity. Reproduced from Selenka [4]. C. Mouse blastocyst at E4.5. D. Inversion of the germ layers at E5.0-E5.5. Drawings C and D are by Paulo Pereira and reproduced with permission from Downs [54] © 2011 European Molecular Biology Organization.
equal note is his description of very early stages in gibbon development. To our knowledge, there is but one other description of an early ape embryo: the 10.5 day implantation site of a chimpanzee [34,35]. Selenka obtained a pre-somite embryo of a gibbon (Hylobates albibaris) at a slightly later stage; we estimate it to correspond to Carnegie stage 7 or early stage 8 in the human. The secondary yolk sac and exocoelom were fully formed with branching villi arising from the surface of the chorion (Fig. 3A). A section through
the wall of the yolk sac revealed blood vessels with nucleated cells, probably haemocytoblasts (Fig. 3C). The villi had two layers of trophoblast surrounding a mesodermal core, but no blood vessels (Fig. 3B). A second embryo (Hylobates agilis) had three somites corresponding to Carnegie stage 9. Because the uterus had been opened before fixation, the swelling retained its spherical form. The villous trees were sparser on the side beneath the decidua capsularis. Blood vessels were now present in the chorion and stem villi.
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Fig. 3. Presomite embryo of the Bornean white-bearded gibbon (Hylobates albibaris). A. Overview of the implantation site showing the amnion (a), secondary yolk sac (ys) and exocoelom. The chorion gives rise to branching villi. B. Section through a villus showing two layers of trophoblast and the mesodermal core (m). C. Section through the yolk sac wall showing extra-embryonic endoderm and mesoderm, and blood vessels with nucleated red cells. Reproduced from Selenka [2].
The vasculature of the yolk sac was quite extensive. The intervillous space was stated to contain lymph. Given the extent of the endometrial glands at the implantation site, this might have been glandular secretion as shown to be the case early in human pregnancy [36]. A comparative study of the early development of primates appeared posthumously [37]. It included brief descriptions of later stages of development in gibbons, but the planned chapter on placentation was not completed on Selenka's death and the published sketches are difficult to interpret. Subsequently, Strahl [3] described the later stages of gibbon placentation starting with a late secondary villus stage where blood was found in the intervillous space and there was a small yolk sac. The fetalematernal interface or basal plate comprised a mixed layer (eine Mischlage) of cellular trophoblast and decidual cells. The basal decidua contained dilated glands and was infiltrated by lymphocytes. The description of this uterus and five later ones mentions blood vessels opening into the intervillous space, but there is insufficient detail to identify any as spiral arteries.
cross sections can be found in the non-pregnant uterus but lack a connective tissue sheath. We are inclined to see this is evidence of spiral artery transformation in the gravid orangutan. A uterus with a small fetus (crown-rump length 48 mm; Fig. 4) was of interest
4.2. Orangutan It was left to Strahl [3] to describe Selenka's orangutan uteri. The earliest embryo had 10e12 somites corresponding to Carnegie stage 10 in the human. The basal decidua had an extensive system of enlarged glands full of secretion. There was no blood in the intervillous space. Although endothelium-lined veins opened into it, no arterial openings could be discerned, despite the presence of numerous sections through corkscrew-like arteries. The latter were embedded in tracts of connective tissue and surrounded by small cells interpreted as decidual in nature. Strahl mentions that arterial
Fig. 4. Gravid uterus of an orangutan (Pongo pygmaeus), fetal crown-rump length 48 mm, to show the decidua capsularis. Reproduced from Strahl [3].
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because a small yolk sac was found at the edge of the placenta between the amnion and chorion. The villous trees and intervillous space had increased greatly in volume, but there were still prominent glands in the basal decidua. At a later stage, with a fetal crownrump length of 10 cm, the thickness of the basal decidua was greatly reduced. In this specimen, Strahl observed cell columns extending from anchoring villi into the decidua. The basal plate of the mature placenta he again characterized as a mixed layer of trophoblasts and decidual cells.
that established interstitial implantation in a gibbon (Fig. 5), but this went largely unnoticed. Accounts of implantation in nonhuman primates begin at best with the chimpanzee [43]. It is not uncommon to encounter statements such as, “Implantation in the human is unique” [44]. Awareness of the sequence in which human placentation evolved is indispensable to the correct interpretation of molecular data such as those pertaining to the immunology of pregnancy [45,46]. In this context Selenka's findings are indispensable.
5. Legacy
5.1. Bibliographical note
Emil Selenka [4] wrote the first detailed and accurate description of early development in the mouse. Given the iconic status of the mouse model it is remarkable that his contribution is so seldom cited. Despite changes in terminology his description differs little from current dogma (Figs. 2 CeD). Although Duval [6] has fared a little better, most recent reviews (e.g. Refs. [38,39]) start with Sobotta [5]. One obvious reason is that Sobotta [5] published in a mainstream journal that now is readily accessible online. Selenka's work on the guinea pig was less original; Kaufmann and Davidoff [40] conclude that neither Selenka [31] nor Duval [32] added substantially to the findings of Bischoff [28]. Nevertheless, Selenka had an important influence on his contemporaries [26,27], who likewise were preoccupied with understanding inversion of the germ layers. Finally, many of the pioneering studies in embryology were overshadowed by the commanding presence of Grosser [41] throughout the first half of the 20th century (discussed in Ref. [19]). It is regrettable that Selenka's contribution to primate placentation goes unnoticed. His work on gibbons [2] has not been superseded, nor has Strahl's [3] account of the orangutan placenta, which built on his collection. Hill [42] reprinted two of the figures
It perplexes readers and librarians alike that Selenka published his definitive accounts in a new journal and changed the name halfway through to accommodate accounts of his ape skeletons. The original title was Studien über Entwickelungsgeschichte der Thiere. There were 14 issues in all, but the last nine were published both under the original title (Parts V-XIV) and as Menschenaffen €delbau (Is(Anthropomorphae) Studien über Entwickelung und Scha sues 1e9). The entire series was published in Weisbaden by C. F. Kreidel's Verlag. Most but not all of the text can be found online [47e49]. Conflict of interest statement The authors have no conflict of interest. Acknowledgments We thank Dr. Thomas Greissman, University of Zurich, for clarifying the historical context of Selenka's gibbon nomenclature. References
Fig. 5. Decidua capsularis of agile gibbon (Hylobates agilis). Selenka's figure [2] redrawn by A.K. Maxwell for Hill's review on placentation in primates [42]. (a) Ventral half of uterus opened to show decidual swelling: d.p., decidua parietalis; f, fimbriae; lg, broad ligament; msc, myometrium; ov, right ovary; ut.c., uterine cavity. (b) Section through the uterine wall and decidual swelling showing the chorionic vesicle (ch. ves.) in situ: ar, artery; blv, blood vessel; d.c., decidua capsularis; d.b., decidua basalis; gl, gland; ivs, intervillous space; v, villi.
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challenges concerning the body axis of mammals, Bioessays 31 (2009) 892e902. PMID: 19609969. K.M. Downs, K.E. Inman, D.X. Jin, A.C. Enders, The allantoic core domain: new insights into development of the murine allantois and its relation to the primitive streak, Dev. Dyn. 238 (2009) 532e553. PMID: 19191225. P. Kaufmann, M. Davidoff, The guinea-pig placenta, Adv. Anat. Embryol. Cell Biol. 53 (1977) 5e91. PMID: 331890. O. Grosser, Vergleichende Anatomie und Entwicklungsgeschichte der Eih€ aute und der Placenta, Wilhelm Braumüller, Vienna, 1909. J.P. Hill, The developmental history of the primates, Phil. Trans. R. Soc. Lond B 221 (1932) 45e178. A.C. Enders, S. Schlafke, Implantation in nonhuman primates and the human, in: Comparative Primate Biology. 3: Reproduction and Development, Alan R. Liss, Inc., 1986, pp. 291e310. P. Bischof, A. Campana, Molecular mediators of implantation, Baillieres Best Pract. Res. Clin. Obstet. Gynaecol 14 (2000) 801e814. PMID: 11023801. P. Parham, A. Moffett, Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution, Nat. Rev. Immunol. 13 (2013) 133e144. PMID: 23334245. A.M. Carter, Comparative studies of placentation and immunology in nonhuman primates suggest a scenario for the evolution of deep trophoblast invasion and an explanation for human pregnancy disorders, Reproduction 141 (2011) 391e396. PMID: 21273370. E. Selenka. Menschenaffen (Anthropomorphae): Studien über Entwickelung und Sch€ adelbau (read only). http://www.europeana.eu/portal/record/08706/ EA33B4BCC1965D304473DAB1D37B75777E8A77AE.html downloaded 21 October 2015. E. Selenka. Studien über Entwickelungsgeschichte der Tiere (incomplete). http://archive.org/search.php?query¼creator%3A%22Selenka%2C%20Emil%2C %201842-1902%20Menschenaffen%22 downloaded 21 October 2015. E. Selenka. Studien über Entwickelungsgeschichte der Tiere Heft I-V. University of Utrecht. http://aleph.library.uu.nl/F/?func¼direct&doc_ library¼UBU01&doc_number¼000095007 downloaded 21 October 2015. D.E. Wilson, D.M. Reeder, Mammal Species of the World. A Taxonomic and Geographic Reference, third ed., The Johns Hopkins University Press, Baltimore, 2005, pp. 1e2142. H. Strahl, H. Happe, Über die Placenta der Schwanzaffen, Menschenaffen (Anthropomorphae) Stud. über Entwickelung Sch€ adelbau 13 (1905) 493e552. C.P. Groves, Systematics and phylogeny of gibbons, in: D.M. Rumbaugh (Ed.), Gibbon and Siamang, Evolution, Ecology, Behavior, and Captive Maintenance, Vol. 1, Karger, Basel, 1972, pp. 1e89. V.N. Thinh, A.R. Mootnick, T. Geissmann, M. Li, T. Ziegler, M. Agil, P. Moisson, T. Nadler, L. Walter, C. Roos, Mitochondrial evidence for multiple radiations in the evolutionary history of small apes, BMC Evol. Biol. 10 (2010) 74. PMID: 20226039. K.M. Downs, Lineage commitments: emphasis on embryonic-extraembryonic interfaces, EMBO Rep. 12 (2011) 987e990.
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Emil Selenka on the embryonic membranes of the mouse and placentation in gibbons and orangutans A.M. Carter a, *, R. Pijnenborg b a b
Department of Cardiovascular and Renal Research, University of Southern Denmark, DK-5000 Odense, Denmark Department of Development and Regeneration, Katholieke Universiteit Leuven, B-3000 Leuven, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 October 2015 Received in revised form 13 November 2015 Accepted 16 November 2015
Background: Emil Selenka made important contributions to embryology in marsupials, rodents and primates that deserve wider recognition. Here we review his work on early development of the mouse and placentation in the great apes. Findings: Selenka was intrigued by germ layer theory, which led him to study inversion of the germ layers in the mouse and other rodents. He found it was growth of the ectoplacental cone that caused a downward shift in the position of the underlying ectoderm and endoderm, leading to an inside-outside inversion of these layers. In primates he made the important discovery that the embryos of gibbons and orangutans develop under a decidua capsularis. Thus all great apes, including humans, exhibit interstitial implantation; this is in contrast to other primates where implantation is superficial. Conclusions: Selenka's work was thorough and brilliantly illustrated. It was an important influence on his contemporaries and was well known to scientists of the following generation. Embryologists continue to advance our knowledge of fetal membranes and placentation in the mouse, but Selenka's work on gibbons is unique and our knowledge of orangutan placentation is restricted to his specimens. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Decidua capsularis Germ layers History of science Interstitial implantation
1. Introduction Emil Selenka was the first to show the presence of a decidua capsularis in gibbons and orangutans, a feature they share with the human. As implantation is superficial in New and Old World monkeys [1], these observations are important, because they imply that primary interstitial implantation evolved in the ancestral lineage of great apes. Selenka's work on the early development of gibbons [2] is unsurpassed. His orangutan material, described after his death by Strahl [3], is unique. Largely forgotten is Selenka's work on rodents. Yet he was the first to describe the early development of the germ layers in the mouse and to explain how inversion of the germ layers came about [4]. His work on rodents is rarely cited compared, for example, to Sobotta [5], who built further on Selenka's legacy, and Matthias Duval [6e8], who tended to downplay it. Selenka's work encompassed several other mammals including marsupials (Table 1). Thus he was among the first to detail development of the opossum (Didelphis virginiana) [9] and the first to
* Corresponding author. E-mail address: [email protected] (A.M. Carter). http://dx.doi.org/10.1016/j.placenta.2015.11.005 0143-4004/© 2015 Elsevier Ltd. All rights reserved.
describe yolk sac placentation in the Tasmanian bettong (Bettongia gaimardi), gray cuscus (Phalanger orientalis) and common brushtail possum (Trichosurus vulpecula) [10]. This required him to establish breeding colonies for the Australian species. Our aim is twofold: to draw attention to Selenka's work and encourage consultation of his original papers. To this end we have included a bibliographical note and a key to the mammals he studied in which the nomenclature employed by Selenka is compared to that currently in use.
2. Biographical sketch Emil Selenka (Fig. 1) was born 27 February 1842 in Braunschwieg, capital of the independent Duchy of Brunswick. His father, Johannes Jacob Selenka, was a master bookbinder and prominent citizen who founded an arts and crafts school that was the forerunner to the Braunschwieg University of Art [11]. The forecourt of the present day University is named JohanneseSelenkaePlatz. Emil Selenka studied at the local technical college and the €ttingen. His doctoral thesis [12] dealt with the University of Go systematics of sea cucumbers (Holothuroidea). It led to his appointment, at the age of 26, to the Chair of Zoology at Leiden.
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Table 1 Key to the mammals studied by Selenka and the current nomenclature (Wilson and Reeder [50]). Family
Genus and species names used by Selenka
Current classification
Source
Didelphidae Dasyuridae Phalangeridae
Didelphis virginiana Shaw Dasyurus viverrinus Phalangista vulpine Desmarest P. orientalis Waterhouse Hypsiprymnus cuniculus H. penicillatus Waterhouse Arvicola arvalis Pallasa Mus sylvaticus L. Mus musculus L. Mus decumanus Pallas Cavia cobaya Marcgrav Pteropus edulis Tragulus javanicus Cebus fatuellus [L.]b Mycetes seniculus [L.]b Cercocebus cynomolgus Cuvier Macacus nemestrinus Desmarest Semnopithecus maurus Cuvier S. pruinosus Desmarest S. mitratus Eschsholtz S. nasicus Schreber S. cruciger Thomas S. cephalopterus [Boddaert] S. rubicundus [Müller]b Inuus speciosus [F. Cuvier]c Hylobates concolor Harland H. Mülleri H. agilis Cuvier H. Rafflesi? H. leuciscus Schreber Siamanga syndactylus Raffles Simia satyrus Linne
Didelphis virginiana Kerr Dasyurus viverrinus Shaw Trichosurus vulpecula Kerr Phalanger orientalis Pallas Bettongia gaimardi Desmarest Bettongia penicillata Gray Microtus arvalis Pallas Apodemus sylvaticus L. Mus musculus L. Rattus norvegicus Berkenhout Cavia porcellus L. Pteropus vampyrus L. Tragulus javanicus Osbeck Cebus apella L. Alouatta seniculus L. Macaca fascicularis Raffles M. nemestrina L. Geoffroy Trachypithecus auratus E. T. cristatus Raffles Presbytis melalophos Raffles Nasalis larvatus Wurmb Presbytis chrysomelas Müller Trachypithecus vetulus Erxleben Presbytis rubicunda Müller Macaca fuscata Blyth Hylobates albibaris Lyon H. muelleri Martin H. agilis F. Cuvier H. agilis F. Cuvier H. moloch Audebert Symphalangus syndactylus Raffles Pongo pygmaeus L.
Brazil and laboratory bred Not known Australia and laboratory bred Australia and laboratory bred Not known Australia and laboratory bred Not stated Erlangen, Germany Laboratory bred Laboratory bred Laboratory bred Not known Java, Borneo (?) Not stated Not stated Java, Borneo, Malacca Borneo Java Borneo Java Borneo Borneo Ceylon Borneo? Japan Borneo Borneo Sumatra Sumatra Java Sumatra Borneo
Hypsiprymnodontinadae Cricetidae Muridae
Caviidae Pteropodidae Tragulidae Cebidae Atelidae Cercopithecidae
Hylobatidae
Hominidae a
This is the common vole, but the German name Feldmaus has been translated by some authors as field mouse. Described by Strahl and Happe [51]. Described as Macacus speciosus by Strahl and Happe [51]. d The species name is now reserved for Nomascus concolor, which does not occur on Borneo [52]. The most important specimen mentioned as Hylobates concolor was collected by Selenka on the left bank of the River Kapuas and therefore can be assigned to H. albibaris [53]. b c
Here he continued to work on marine invertebrates. During this period he founded what is now the Royal Dutch Zoological Society. He also hosted a doctoral student from the University of Utrecht, Ambrosius Hubrecht [13], who was to become a lifelong friend and intellectual sparring partner. In 1874, after 6 years in the Netherlands, Selenka was called to a Chair at Erlangen. It was now that he began to focus his attention on developmental biology. The opening statement of his first important paper, again on sea cucumbers, explains his motivation [14]. He thought it important to determine the origin of echinoderms and the fossil record had failed to provide convincing answers. Therefore it was important to try a new approach based on embryology. He continued along similar lines with a major study of the early development and larval stages of sea urchins (Echinoidea) [15]. His work on marine invertebrates also encompassed saltwater planarians, but around 1882 he switched gears and began his studies of mammalian development, at first in rodents and marsupials. Gradually Selenka developed a desire to link his animal studies to ontogenesis in human beings and for this he needed primate material. To this end he embarked upon two expeditions to the Dutch East Indies, accompanied by his second wife Lenore. They also visited Ceylon and Japan. During the second trip, Selenka fell seriously ill with malaria and went to convalesce in the Himalayas, whilst Lenore spent several more months in Borneo. Both husband and wife were interested in ethnography and their travel book, “Sonnige Welten,” was a bestseller that went into three editions [16]. Margarethe Lenore Selenka was a prominent feminist and is
better remembered than her husband; there is now a MargaretheeSelenkaeStrasse in Munich. Selenka had accumulated an impressive amount of material. One recent estimate is that he and his staff shot around 400 orangutans [17]. Conscious of the toll, he determined to make full use of the animals and embarked on studies of the skeleton and dentition of the great apes. His collection of orangutan skeletons at Munich (Die Zoologische Staatssammlung München, ZSM) is still an important resource [18]. In 1895, better to devote his time to research, Selenka resigned his Chair at Erlangen and moved to Munich, where he had the status of honorary professor. He died there in 1902, just before his 60th birthday, leaving the work unfinished. As we shall see, it was continued by his colleagues, particularly Hubrecht and Hans Strahl [19]. For further details of Selenka's life and early work, including a complete bibliography, reference should be made to Hubrecht's obituary [20]. A briefer but more accessible account is given by Lubosch [21].
3. Rodents 3.1. Germ layer theory In his studies of invertebrates, Selenka had been much concerned with the germ layers; his paper on sea cucumbers had the subtitle, “A contribution to germ layer theory” [14]. The prevalent view was that each germ layer (ectoderm, mesoderm and endoderm), regardless of species, gave rise to a fixed set of organs. This
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towards the uterine lining. In between, however, there remained the yolk sac cavity and the outer wall of the yolk sac comprising parietal endoderm and trophoblast. This state is sometimes referred to as “incomplete inversion.” Disappearance of the outer wall occurs later in development of the mouse; there is then said to be “complete inversion” [24]. An important causal element in the inversion process of the germ layers in the mouse is the proliferation of a group of cells, now known as the ectoplacental cone, referred to as a “Zapfen” (plug) in €ger” Bischoff's study of the guinea-pig [28], but renamed as the “Tra by Selenka [4], a more general term which would fit better with observations in other related rodent species. In Selenka's view it €ger which caused a downward was the inward growth of the Tra shift in the position of the underlying ectoderm and endoderm, leading to an inside-outside inversion of these layers. The term Tr€ ager must be one of the very few German terms which regularly turn up in the older English literature (e.g. Refs. [29,30]). The now ^ ne common term “ectoplacental cone” was introduced by Duval (co ectoplacentaire), who also studied this inversion process in order rifier les to, “confirm the elegant studies of Selenka on this topic” (ve belles recherches de Selenka sur ce sujet) [6]. After expressing his admiration for Selenka's study of early mouse embryos, however, €ger to the he criticized him for not relating the formation of the Tra subsequent development of the placenta, which was rectified by Duval's altered term ‘ectoplacental cone’. Furthermore, Duval noted Selenka's mistaken identification of the (trophoblastic) giant cells surrounding the implanting blastocyst as decidual cells. 3.3. Germ layer inversion in the guinea pig and other rodents
Fig. 1. Emil Selenka (1842e1902): German zoologist and embryologist. Reproduced from Ref. [20].
concept was shortly to be refuted by the eminent Swiss embryol€lliker [22] and was eventually demolished by ogist Albert von Ko experimental embryologists (reviewed in Ref. [23]). Their experiments proved there was no fundamental difference between the three layers. However, that was in the future. There is little doubt that germ layer theory strongly influenced the thinking of Selenka and his contemporaries. 3.2. Germ layer inversion in the mouse Inversion of the germ layers is a process by which the endoderm of the embryonic hemisphere is everted toward the uterine lining [24]. Inversion of the germ layers was known to occur in the guinea pig embryo, but there had been no satisfactory explanation of how this was brought about. Selenka's contribution was to show that inversion of germ layers occurred in the mouse and demonstrate the mechanism by which this was achieved [4,25]. He was not alone in working on this problem and his paper appeared in the same year as Fraser's on the rat [26] and Kupffer's on the common vole [27]. In the mouse, Selenka [4] found that the primitive endoderm (hypoblast) was present at implantation and isolated endodermal cells had spread to the inside of the blastocyst cavity (Fig. 2A). Shortly afterward, eversion of the embryonic hemisphere had commenced resulting in inversion of the germ layers (Fig. 2B). The endoderm covering the embryo (visceral endoderm) now faced out
Having identified the events underlying germ layer inversion in the mouse, Selenka [31] attempted to extend this analysis to other rodents. He argued convincingly for a similar process in the rat (Rattus norvegicus) and field mouse (Apodemus sylvaticus) and drew a credible parallel to a cricetid rodent, the common vole (Microtus arvalis). In this he combined his own observations with those of Fraser [26] and Kupffer [27]. His main object of study, however, was the guinea pig (Cavia porcellus), and here he found a somewhat different situation. Perhaps most significant was the precocious €hle), which distanced appearance of the exocoelom (Interamnionho the embryonic ectoderm from the extraembryonic ectoderm of the Tr€ ager (Mossman [24] names this cavity the precoelom). He noted in addition the failure of extraembryonic endoderm to line the trophoblast and form a true yolk sac. The trophoblast itself persists in early stages, a detail that was lost in some later studies but confirmed by the eminent Cambridge embryologist J. T. Wilson [32]. Otherwise, Selenka's [31] account added little to that of Bischoff [28] and is in any case less widely known than the later study by Duval [33]. It is worth consulting mainly for the exquisite detail of the illustrations and the schematic comparison of early development in the rabbit and five species of rodent (Plate XVI in Ref. [31]). 4. Primates Selenka's most important work concerned the early development and placentation of Old World monkeys and great apes and was based on specimens he collected in Indonesia (Table 1). 4.1. Gibbons The first publication concerned the development of gibbons [2]. It is especially important for establishing the presence of a decidua capsularis in gibbons (Fig. 3A) and his recognition that this feature distinguished all the great apes from the Old World primates. Of
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Fig. 2. Inversion of germ layers in the mouse (Mus musculus). A. Implanting blastocyst. The primitive endoderm (or hypoblast) is apparent and one cell has migrated to the inside of the blastocyst wall. Reproduced from Selenka [4]. B. Growth of the ectoplacental cone (extraembryonic ectoderm) has pushed the epiblast down into the yolk sac cavity. As a result the visceral endoderm faces outwards (germ layer inversion). The parietal endoderm provides a partial lining to the yolk sac cavity. Reproduced from Selenka [4]. C. Mouse blastocyst at E4.5. D. Inversion of the germ layers at E5.0-E5.5. Drawings C and D are by Paulo Pereira and reproduced with permission from Downs [54] © 2011 European Molecular Biology Organization.
equal note is his description of very early stages in gibbon development. To our knowledge, there is but one other description of an early ape embryo: the 10.5 day implantation site of a chimpanzee [34,35]. Selenka obtained a pre-somite embryo of a gibbon (Hylobates albibaris) at a slightly later stage; we estimate it to correspond to Carnegie stage 7 or early stage 8 in the human. The secondary yolk sac and exocoelom were fully formed with branching villi arising from the surface of the chorion (Fig. 3A). A section through
the wall of the yolk sac revealed blood vessels with nucleated cells, probably haemocytoblasts (Fig. 3C). The villi had two layers of trophoblast surrounding a mesodermal core, but no blood vessels (Fig. 3B). A second embryo (Hylobates agilis) had three somites corresponding to Carnegie stage 9. Because the uterus had been opened before fixation, the swelling retained its spherical form. The villous trees were sparser on the side beneath the decidua capsularis. Blood vessels were now present in the chorion and stem villi.
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Fig. 3. Presomite embryo of the Bornean white-bearded gibbon (Hylobates albibaris). A. Overview of the implantation site showing the amnion (a), secondary yolk sac (ys) and exocoelom. The chorion gives rise to branching villi. B. Section through a villus showing two layers of trophoblast and the mesodermal core (m). C. Section through the yolk sac wall showing extra-embryonic endoderm and mesoderm, and blood vessels with nucleated red cells. Reproduced from Selenka [2].
The vasculature of the yolk sac was quite extensive. The intervillous space was stated to contain lymph. Given the extent of the endometrial glands at the implantation site, this might have been glandular secretion as shown to be the case early in human pregnancy [36]. A comparative study of the early development of primates appeared posthumously [37]. It included brief descriptions of later stages of development in gibbons, but the planned chapter on placentation was not completed on Selenka's death and the published sketches are difficult to interpret. Subsequently, Strahl [3] described the later stages of gibbon placentation starting with a late secondary villus stage where blood was found in the intervillous space and there was a small yolk sac. The fetalematernal interface or basal plate comprised a mixed layer (eine Mischlage) of cellular trophoblast and decidual cells. The basal decidua contained dilated glands and was infiltrated by lymphocytes. The description of this uterus and five later ones mentions blood vessels opening into the intervillous space, but there is insufficient detail to identify any as spiral arteries.
cross sections can be found in the non-pregnant uterus but lack a connective tissue sheath. We are inclined to see this is evidence of spiral artery transformation in the gravid orangutan. A uterus with a small fetus (crown-rump length 48 mm; Fig. 4) was of interest
4.2. Orangutan It was left to Strahl [3] to describe Selenka's orangutan uteri. The earliest embryo had 10e12 somites corresponding to Carnegie stage 10 in the human. The basal decidua had an extensive system of enlarged glands full of secretion. There was no blood in the intervillous space. Although endothelium-lined veins opened into it, no arterial openings could be discerned, despite the presence of numerous sections through corkscrew-like arteries. The latter were embedded in tracts of connective tissue and surrounded by small cells interpreted as decidual in nature. Strahl mentions that arterial
Fig. 4. Gravid uterus of an orangutan (Pongo pygmaeus), fetal crown-rump length 48 mm, to show the decidua capsularis. Reproduced from Strahl [3].
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because a small yolk sac was found at the edge of the placenta between the amnion and chorion. The villous trees and intervillous space had increased greatly in volume, but there were still prominent glands in the basal decidua. At a later stage, with a fetal crownrump length of 10 cm, the thickness of the basal decidua was greatly reduced. In this specimen, Strahl observed cell columns extending from anchoring villi into the decidua. The basal plate of the mature placenta he again characterized as a mixed layer of trophoblasts and decidual cells.
that established interstitial implantation in a gibbon (Fig. 5), but this went largely unnoticed. Accounts of implantation in nonhuman primates begin at best with the chimpanzee [43]. It is not uncommon to encounter statements such as, “Implantation in the human is unique” [44]. Awareness of the sequence in which human placentation evolved is indispensable to the correct interpretation of molecular data such as those pertaining to the immunology of pregnancy [45,46]. In this context Selenka's findings are indispensable.
5. Legacy
5.1. Bibliographical note
Emil Selenka [4] wrote the first detailed and accurate description of early development in the mouse. Given the iconic status of the mouse model it is remarkable that his contribution is so seldom cited. Despite changes in terminology his description differs little from current dogma (Figs. 2 CeD). Although Duval [6] has fared a little better, most recent reviews (e.g. Refs. [38,39]) start with Sobotta [5]. One obvious reason is that Sobotta [5] published in a mainstream journal that now is readily accessible online. Selenka's work on the guinea pig was less original; Kaufmann and Davidoff [40] conclude that neither Selenka [31] nor Duval [32] added substantially to the findings of Bischoff [28]. Nevertheless, Selenka had an important influence on his contemporaries [26,27], who likewise were preoccupied with understanding inversion of the germ layers. Finally, many of the pioneering studies in embryology were overshadowed by the commanding presence of Grosser [41] throughout the first half of the 20th century (discussed in Ref. [19]). It is regrettable that Selenka's contribution to primate placentation goes unnoticed. His work on gibbons [2] has not been superseded, nor has Strahl's [3] account of the orangutan placenta, which built on his collection. Hill [42] reprinted two of the figures
It perplexes readers and librarians alike that Selenka published his definitive accounts in a new journal and changed the name halfway through to accommodate accounts of his ape skeletons. The original title was Studien über Entwickelungsgeschichte der Thiere. There were 14 issues in all, but the last nine were published both under the original title (Parts V-XIV) and as Menschenaffen €delbau (Is(Anthropomorphae) Studien über Entwickelung und Scha sues 1e9). The entire series was published in Weisbaden by C. F. Kreidel's Verlag. Most but not all of the text can be found online [47e49]. Conflict of interest statement The authors have no conflict of interest. Acknowledgments We thank Dr. Thomas Greissman, University of Zurich, for clarifying the historical context of Selenka's gibbon nomenclature. References
Fig. 5. Decidua capsularis of agile gibbon (Hylobates agilis). Selenka's figure [2] redrawn by A.K. Maxwell for Hill's review on placentation in primates [42]. (a) Ventral half of uterus opened to show decidual swelling: d.p., decidua parietalis; f, fimbriae; lg, broad ligament; msc, myometrium; ov, right ovary; ut.c., uterine cavity. (b) Section through the uterine wall and decidual swelling showing the chorionic vesicle (ch. ves.) in situ: ar, artery; blv, blood vessel; d.c., decidua capsularis; d.b., decidua basalis; gl, gland; ivs, intervillous space; v, villi.
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