Researching Reproduction in Hedgehog Tenrecs (Afrosoricida, Tenrecidae) Carter, Anthony M

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Hans Bluntschli in Berne Researching reproduction in hedgehog tenrecs (Afrosoricida, Tenrecidae) Carter, Anthony M

Published in: Journal of Morphology

DOI: 10.1002/jmor.20988

Publication date: 2019

Document version: Accepted manuscript

Citation for pulished version (APA): Carter, A. M. (2019). Hans Bluntschli in Berne: Researching reproduction in hedgehog tenrecs (Afrosoricida, Tenrecidae). Journal of Morphology, 280(6), 841-848. https://doi.org/10.1002/jmor.20988

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Hans Bluntschli in Berne: researching reproduction in hedgehog tenrecs (Afrosoricida, Tenrecidae)

Anthony M. Carter

Cardiovascular and Renal Research, Institute of Molecular Medicine, University of Southern Denmark, J. B. Winsloews Vej 21, DK-5000 Odense, Denmark

Correspondence

Anthony M. Carter, Cardiovascular and Renal Research, Institute of Molecular Medicine, University of Southern Denmark, J. B. Winsloews Vej 21, DK-5000 Odense, Denmark. Email: [email protected]

Research Highlights

Tenrec reproduction was the main aspect of Bluntschli’s research after was obliged to leave Frankfurt for Berne

His group described unique features that included non-antral follicles, intraovarian fertilization and absence of a morula stage

Abstract

The Swiss anatomist Hans Bluntschli is best known as a primatologist. Yet his focus during his later years in Berne was on reproduction in Malagasy tenrecs. This research was done with two graduate students, Robert Goetz and Fritz Strauss; all three had been obliged to leave Germany after the National Socialists came to power. Unique features of reproduction in tenrecs included non-antral follicles, intrafollicular fertilization, eversion of the corpus luteum and polyovulation. The fertilized egg formed a blastula that developed into a blastocyst; there was no morula stage. A false placental cushion developed in the endometrium opposite the implantation site. Placentation was complex and included development of a prominent haemophagous organ. These findings are discussed in relation to current concepts of mammalian phylogeny that place tenrecs and golden moles in the same order and as close relatives to elephant shrews and the aardvark.

KEYWORDS blastula, history of science, non-antral follicles, placentation, polyovulation

This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/jmor.20988

In 1931, Hans Bluntschli, renowned primatologist and Director of the prestigious Senckenberg Research Institute, embarked on an expedition to Madagascar (Fig. 1). Two years later, and shortly after his return, he was relieved of his duties in Frankfurt by the National Socialist regime. He then was called to the chair of anatomy at Berne. Although he had collected primate material on Madagascar, his first priority was to describe the reproductive biology of tenrecs. To this end, he supervised research by Robert Goetz, who had been denied a licence to practise medicine in Germany, and Fritz Strauss, who had fled to Switzerland because of his Jewish parentage. Together they described some remarkable features of reproduction in tenrecs such as the absence of antral follicles, lack of a morula stage, large litter size and unique placentation. This work occupied Bluntschli during his most productive years at Berne, yet has been overlooked by previous biographers (Cener, 1990; Greif & Schmutz, 1995).

Tenrec biology attracted scant attention until recently, when molecular phylogenetics shook the mammalian tree (Madsen et al., 2001; Murphy, Eizirik, Johnson, et al., 2001). It focussed interest on a superorder of mammals that included tenrecs, placing them near to the root of the eutherian tree (Carter, 2001). All three species studied by Bluntschli, Goetz and Strauss were from the same subfamily of tenrecs (Tenrecinae) for which they used the synonym Centetinae (McKenna & Bell, 1997). Tenrecs were seen by them to be very primitive insectivores as were golden moles (Bluntschli, 1938). Based on molecular phylogenetics, tenrecs and golden moles are now grouped in the order Afrosoricida (Madsen et al., 2001). In contrast to what was known in Bluntschli’s time, they are thought to belong to a different lineage than other insectivores, such as hedgehogs, shrews and moles. Today, the three subfamilies of Malagasy tenrecs and the African otter shrews comprise the suborder Tenrecomorpha (Everson, Soarimalala, Goodman, & Olson, 2016).

This review has a dual purpose. The first is to recapitulate the careers of three scientists and their intersection in the shadow of the Third Reich (Hildebrandt & Redies, 2012). The other is to review the unique aspects of tenrec biology they described in the late 1930’s and 1940’s and, where relevant, update them with recent data. This story is a timely reminder that research does not operate in a vacuum but must be viewed in the context of contemporary politics and societal norms (Hildebrandt & Redies, 2012).

2 THE SCIENTISTS

This article is protected by copyright. All rights reserved. The principal sources for Bluntschli are an obituary (Strauss, 1964), more recent biographies dealing with him as anatomist (Cener, 1990) and morphologist (Greif & Schmutz, 1995) and detailed accounts of his dismissal from Frankfurt under the National Socialist regime (Benzenhöfer, 2014; Benzenhöfer & Hack- Molitor, 2012). The most comprehensive account of Goetz deals principally with his career after leaving Berne, but includes his own thoughts on the time spent there (Konstantinov, 2000). There is a useful obituary of Strauss (Weber, 1995).

Hermann Georg Hans Bluntschli was born at Frankfurt on Main on 19 February 1877. His father was a renowned Swiss architect. Bluntschli studied medicine at the University of Zurich but developed symptoms of a hereditary hearing impediment (otosclerosis) that he knew would hinder a clinical career. In consequence, after his final exams, he moved to the Anatomical Institute at Heidelberg. There, under the guidance of Max Fürbringer (1846-1920), a student of Carl Gegenbauer (1826-1903), he wrote a dissertation on the liver of the Queensland lungfish Neoceratodus forsteri (Bluntschli, 1904). He then returned to Zurich with a view to studying the comparative anatomy of primates. His thesis (Habilitation) was about the branches of the femoral artery in catarrhine primates (Bluntschli, 1906). In 1912 he made an expedition to Brazil to collect material from Neotropical primates, following in the footsteps of the eminent Swiss-Brazilian zoologist Emil August Goeldi (1859-1917). On his return, he was recruited by the Senckenberg Research Institute in Frankfurt, becoming a full professor in 1914. Here he did his most important primatological work (Greif & Schmutz, 1995). From 1931 to 1932, he embarked on an expedition to Madagascar, where he collected lemurs and tenrecs with the intent of studying their embryology. Not long after his return, he was relieved of his duties by the National Socialist regime (Benzenhöfer & Hack- Molitor, 2012). He was, however, called to the chair of anatomy in Berne, where he remained until his retirement in 1947. Bluntschli favoured a holistic approach to anatomy (Benzenhöfer & Hack-Molitor, 2012) and in 1938 founded a new journal Bio-Morphosis, with the aim of fostering the exchange of ideas between morphologists and physiologists (Strauss, 1964). A considerable part of the tenrec work was published there. Hans Bluntschli died at Berne on 13 July 1962.

Robert Hans Goetz was born in Frankfurt 17 April 1910. He read medicine at the University of Frankfurt and while still a student invented a finger plethysmograph (Goetz, 1933). In 1934, after completing his finals, he was declared “politically unreliable” and denied a medical license. Meanwhile, Goetz had married Verena Bluntschli and his father-in-law gave him the opportunity to work on the tenrec material in Berne

This article is protected by copyright. All rights reserved. (Konstantinov, 2000). In 1937 he went to South Africa, where he had to retake his medical exams before practising medicine. During the Cape Town years, he conducted innovative field studies on the cardiovascular physiology of the giraffe (Mitchell, 2008). In 1957 Goetz, by then a cardiac surgeon, settled in the United States. While at the Albert Einstein College of Medicine, New York, he performed the first successful coronary bypass operation (Konstantinov, 2000). Throughout his career, Goetz was supported by his wife, who was a physician trained in Geneva and Frankfurt (e.g. (Goetz, Jallah, & Goetz, 1967)). Goetz died 15 December 2000 (Mitchell, 2008).

Fritz Strauss was born in Nuremberg on 14 April 1907. He read medicine at Erlangen, Kiel and Freiburg-im- Breisgau, graduating in 1932. In the following year, he fled Germany with his parents, who were of Jewish descent, and found employment in Switzerland. In 1936 he was recruited by Bluntschli to work on implantation and placentation in tenrecs and he completed his thesis (Habilitation) in 1944 (Strauss, 1944). He collaborated with Kurt Feremutch (1920-2004), another of Bluntschli’s students, who would later make his mark as a neuroanatomist. In 1949-50, Strauss spent a year in Madison, Wisconsin as postdoctoral fellow with Harland W. Mossman (1898-1991). Later he worked on the golden hamster (Mesocricetus auratus) (Strauss, 1956), European hare (Lepus europaeus) (Strauss, 1957), pocket gopher (Geomys sp.) (Mossman & Strauss, 1963) and grey mouse lemur (Microcebus murinus) (Strauss, 1978). He wrote the chapter on the female reproductive tract for the authoritative Handbuch der Zoologie (Strauss, 1963). Strauss was professor of anatomy at Berne from 1953 until his retirement in 1973. He died at Berne on 29 April 1994 (Weber, 1995).

3 TENREC REPRODUCTION

3.1 Ovulation and corpus luteum formation

Bluntschli and Goetz reported on the ovary and early embryology of the lowland streaked tenrec (Hemicentetes semispinosus) with additional remarks on the tailless tenrec (Tenrec ecaudatus) (Bluntschli, 1937a; Goetz, 1938a). Strauss dealt with the greater hedgehog tenrec (Setifer setosus), giving a detailed description that was extensively referenced by Mossman and Duke (Mossman & Duke, 1973; Strauss, 1938a, 1938b).

An important finding was the absence of an antrum in the mature follicles of Hemicentetes and Setifer (Figure 2 a). Later this observation was extended to Tenrec (Nicoll & Racey, 1985), the lesser hedgehog

This article is protected by copyright. All rights reserved. tenrec (Echinops telfairi) (Enders, Carter, Kunzle, & Vogel, 2005) and the Nimba otter shrew (Micropotamogale lamottei) (Enders et al., 2005). Non-antral follicles have not been described in other eutherians although the antrum is quite small in several species of shrew. The lack of true Graafian follicles was one feature that led Bluntschli to compare the tenrec ovary to that of reptiles and monotremes (Bluntschli, 1937a).

Much later, when ovaries of Echinops and Micropotamogale were examined by transmission electron microscopy, follicular fluid was found in the intercellular spaces between the more peripheral granulosa cells of mature follicles (Enders et al., 2005). This may be relevant to the supposed mechanism of ovulation in tenrecs. Strauss described the granulosa as oedematous and spongy and supposed that ovulation was not an eruptive process. Rather he considered that rearrangement of the granulosa cells brought the ovum towards the surface of the ovary for fertilization and ovulation (Strauss, 1938a).

The tenrec ovary was enclosed by a bursa within which spermatozoa often were found. Bluntschli had supposed that fertilization might occur in the bursa (Bluntschli, 1937a), but Strauss went further and showed the presence of spermatozoa within the granulosa of ripe follicles (Strauss, 1938a). Furthermore, he documented that extrusion of the first polar body and fertilization of the ovum occurred in the ovary. Particularly convincing is his photograph of an ovum with two pronuclei caught just prior to ovulation. (Figure 2 b). Intrafollicular fertilization may also occur in Tenrec (Nicoll & Racey, 1985).

Following ovulation, granulosa cells protruded above the surface of the ovary. Changes associated with their subsequent luteinisation and vascularization resulted in a partially everted corpus luteum. The outer surface was, however, rapidly covered by connective tissue and associated blood vessels and then by epithelium. This sequence of events was described in detail for Setifer with additional observations on Ericulus and Hemicentetes (Strauss, 1938b). Eversion of the luteinized granulosa was later shown for Tenrec (Nicoll & Racey, 1985) and the formation of cup-shaped corpora lutea described in Micropotamogle (Enders et al., 2005). Everted corpora lutea also occur in Grant’s golden mole (Eremitalpa granti) (Mossman & Duke, 1973), several species of elephant shrew (Macroscelididae) (Horst & Gillman, 1940; Tripp, 1971) and the aardvark (Orycteropus afer) (Horst, 1949).

Bluntschli is often cited (e.g. (Treat et al., 2018)) for his observation that Tenrec can have a litter of up to 32 young and he mentions finding as many as 40 blastocysts in the uterus (Bluntschli, 1937a). This is the upper

This article is protected by copyright. All rights reserved. end of the range as a later study found a mean of 9.7 implantations (Nicoll & Racey, 1985). Hemicentetes gives birth to 6-8 young (maximum 10), yet 20 embryos at cleavage stages could be isolated from the uterus (Bluntschli, 1937a). The release of more ova than can be accommodated by the uterus is known as polyovulation. It is common in marsupials (Harder, Stonerook, & Pondy, 1993; Tyndale-Biscoe & Renfree, 1987), but unusual in eutherians; other examples are some species of elephant shrew (Tripp, 1971) and the plains viscacha (Weir, 1971). An aardvark with a single fetus had a total of 5 corpora lutea (Horst, 1949).

3.2 Early development and implantation

Initial cleavage of the fertilized ovum of Hemicentetes led to formation of a blastula, i.e. a single layer of cells enclosing a fluid cavity (Figure 3). This progressed to a blastocyst without passing through a morula stage (Bluntschli, 1937a; Goetz, 1938a). The absence of a morula stage is known from only one other eutherian, the Eastern rock elephant shrew (Elephantulus myurus) (Horst, 1942).

Implantation of the blastocyst was lateral (orthomesometrial) in Hemicentetes in contrast to most mammals, where it occurs on the mesometrial or antimesometrial wall of the uterus (Bluntschli, 1937a; Goetz, 1937b; Strauss, 1943). Once nidation had commenced, there was rapid development of the endometrium of the opposite wall to form a large cushion of oedematous connective tissue referred to as the false placental pad (Figure 4). As the primary yolk sac of the embryo protruded into the uterine lumen, its surface was protected by this outgrowth. The membranes did not, however, adhere to that side of the uterus (Bluntschli, 1938; Goetz, 1937b). Lateral implantation and development of a false placental pad had previously been documented in the Cape golden mole (Chrysochloris asiatica) (Lange, 1919).

Subsequent development of the fetal membranes and placenta was described in detail for three species of tenrec (Goetz, 1937a, 1937b, 1938b; Strauss, 1943) and has since been explored in Echinops (Carter, Blankenship, Kunzle, & Enders, 2004, 2005), several species of shrew tenrec (Microgale spp.) (Enders, Blankenship, Goodman, Soarimalala, & Carter, 2007), the mole-like rice tenrec (Oryzorictes hova) (Enders et al., 2007) and two otter shrews (Potamogale velox and Micropotamogale lamottei) (Carter, Blankenship, Enders, & Vogel, 2006). As remarked by Bluntschli, tenrec placentation was complex and hardly indicative of primitive conditions (Bluntschli, 1937b). One striking feature was the prominent haemophagous organ found at the centre of the placental disk.

4 DISCUSSION

This article is protected by copyright. All rights reserved. Three interlaced themes prompt further thought. First, what were the circumstances that brought this group of researchers together in Berne? Second, what prompted Bluntschli to focus on the tenrecs? His reputation had been built on his contributions to primatology and he had gathered a unique material on Madagascar, including a developmental series of the grey mouse lemur (Microcebus murinus) collected in the semiarid Androy region of Madagascar (Anonymous & Bluntschli, 1951). Much of the material was sectioned but no major publication appeared in Bluntschli’s lifetime. Finally, how well do the findings of Bluntschli’s group fit with current thinking on the phylogenetic position of tenrecs?

4.1 Political context

Both Bluntschli and Goetz had strong political views. Bluntschli was a declared pacifist (Benzenhöfer & Hack-Molitor, 2012). He had long been worried about the future of Germany and was opposed to any form of dictatorship. Kreft relates an anecdote told by Bluntschli’s student, Dietrich Starck (1907-2001), to show how Bluntschli openly voiced his disdain for Adolf Hitler (Kreft, 2008). It is, therefore, unsurprising that he fell victim to the civil service law (Gesetz zur Wiederherstellung des Berufsbeamtentums) introduced by the National Socialists in 1933 and designed to remove Jews and political opponents from office. His departure from Frankfurt was precipitated by his removal from teaching responsibilities. There followed a lengthy process with the Dean, Franz Volhard (1872-1950), attempting mediation. The situation was largely resolved when Bluntschli was called to the chair in Berne and resigned on grounds of health, seeking to retain his pension and his research material (Benzenhöfer, 2014; Benzenhöfer & Hack-Molitor, 2012; Kreft, 2008). Goetz had also made clear his political views. Forced to join the National Socialist Student Organization, as a prerequisite for sitting the exams, he resigned after passing his finals. As punishment, he was denied both his diploma and a medical license (Konstantinov, 2000). Volhard had otherwise singled him out for an internship in the Department of Medicine (Konstantinov, 2000). In one sense the pair were fortunate. Bluntschli had a high reputation as a scientist, was from a good Swiss family, and soon found a position in Berne. Most established scholars dismissed under the civil service law struggled to find work (Hildebrandt, 2012). Goetz may have benefited from his marriage to Bluntschli’s daughter. The situation was rather different for Strauss. He is not known to have been politically active, but his career was interrupted when he fled Germany because of his Jewish background (Hildebrandt, 2012).

Among Bluntschli’s students was another Jewish refugee, Conrad Rosenstein, whose autobiography gives a good picture of Bluntschli at this time (Rosenstein, 1958). He was an academic of the old school and could

This article is protected by copyright. All rights reserved. be demanding of his graduate students. Misunderstandings often arose due to his deafness, although afterwards he felt embarrassed and tried to patch things over (Rosenstein, 1958). Mossman visited the lab early in 1939 and found it impossible to talk to Bluntschli whose deafness exacerbated the language barrier (Mossman, 1990).

4.2 Why tenrecs rather than lemurs?

Bluntschli was without doubt fascinated by tenrec biology. He presented the salient points in a few brief papers (Bluntschli, 1937a, 1937b, 1938) and closely monitored Goetz’s work on Hemicentetes and Tenrec. Goetz may well have welcomed the supervision. Later he recalled, “While I was very grateful to Professor Bluntschli for giving me a job when I desperately needed one, my heart was not really in anatomy” (Konstantinov, 2000). His strengths lay in experimental work such as the plethysmograph of his student days and subsequent cardiovascular research in Cape Town and New York.

Bluntschli’s pioneering work on tenrec reproduction has been overlooked by recent biographers. They have instead focussed on his reputation as a primatologist. Indeed, Bluntschli had made substantial contributions to that field before setting foot on Madagascar. A doctoral thesis on Bluntschli the anatomist (Cener 1990) makes little mention of his tenrec work nor does a paper that explores Bluntschli’s views on evolutionary biology (Greif & Schmutz 1995). That is quite surprising given Bluntschli’s remarks on Hemicentetes as the most primitive of the insectivores with features reminiscent of reptiles (Bluntschli 1937a).

It is, indeed, remarkable that Bluntschli paid little attention to the developmental series of the grey mouse lemur (Microcebus murinus) that is an important part of his Madagascar collection. The main reason for the expedition had been to get further material for a planned work on Der Mensch als Primat (man as a primate) (Greif & Schmutz, 1995). Did this project founder against the background of National Socialist abuse of evolutionary theory? Bluntschli did supervise several doctoral students, mostly from the dental faculty, who wrote dissertations on the development of the head, jaw muscles and teeth in Microcebus (Strauss, 1964). However, in contrast to the tenrec work, this did not lead to published papers.

In 1951 Bluntschli sold his Madagascar collection. Adult specimens went to the American Museum of Natural History in New York, where they remain. The developmental series of tenrecs and lemurs were acquired by the Carnegie Institute of Washington (Anonymous & Bluntschli, 1951). Later the Carnegie

This article is protected by copyright. All rights reserved. Collection was curated by Ronan O’Rahilly (1921-2018) at the University of California at Davis. Strauss would eventually turn his attention to implantation in the mouse lemur, but first when the specimens were in Davis (Strauss, 1978). Bluntschli’s collection was also studied by Reng and both authors supplemented it with new material collected by Robert D. Martin (Reng, 1977; Strauss, 1978).

4.3 Tenrec biology and mammalian systematics

Although insectivores had been considered a heterogenous group, it was not until the advent of molecular phylogenetics that tenrecs and golden moles were placed in the same order and found to belong to an entirely different superorder (Afrotheria) than shrews, moles and hedgehogs. Phylogenomics reinforced the concept of a basal position for tenrecs. There is general agreement that eutherians fall into four major clades and that Afrotheria and Xenarthra (comprising sloths, anteaters and armadillos) are close to the root of the tree (Foley, Springer, & Teeling, 2016).

The current consensus is that Afrotheria comprises two major lineages, one leading to elephants, manatees and hyraxes (collectively Paenungulata) and the other to tenrecs and golden moles (Afrosoricida), elephant shrews (Macroscelidea) and the aardvark (Tubulidentata) (Figure 5) (Foley et al., 2016). It is, therefore, interesting that several of the unusual reproductive features of tenrecs also occur in elephant shrews (Table 1). Less is known about the ovaries and early development in golden moles and the aardvark, although both present everted corpora lutea. Mossman studied ovarian sections from Grant’s golden mole (Eremitalpa granti), but was unable to identify ripe follicles that might have an antrum (Mossman & Duke, 1973). Tenrecs and elephant shrews are unique among eutherians in having a blastula stage. A small cavity was observed in the 8-cell morula of Eremitalpa (Gabie, 1959), but nothing resembling a blastula. It should be noted that the blastula of marsupials is a different structure, It develops from a morula stage and is so called because of the absence of an inner cell mass (Lillegraven, 1985). Lateral implantation is unusual but shared by some tenrecs and golden moles. However, Strauss described implantation as antimesometrial in Setifer and Mossman questioned whether there was lateral implantation in Hemicentetes (Mossman, 1987; Strauss, 1943). Tenrecs and golden moles do, however, share the development of a false placental pad opposite the site of implantation.

To what extent are these features plesiomorphic? Starting with Hubrecht, embryologists focussed on insectivores because they were perceived to be primitive and could cast light on the basic mammalian

This article is protected by copyright. All rights reserved. condition (Hubrecht, 1889). Tenrecs continue to be viewed in this light (Treat et al., 2018). They have a low encephalisation index (Mack et al., 2018; Stankowich & Stensrud, 2019), a cloaca (Riedelsheimer, Unterburger, Kuenzle, & Welsch, 2007) and highly variable body temperature (Treat et al., 2018). Internal testes comprise another plesiomorphic feature, and this character is shared with other members of the Afrotheria clade (Kleisner, Ivell, & Flegr, 2010). Several of these features occur in the hypothetical eutherian ancestor as reconstructed by O’Leary and colleagues (O'Leary et al., 2013).

5 CONCLUSIONS

Bluntschli’s work at Berne, in the years following his expulsion from Frankfurt, focussed mainly on tenrec reproduction and revealed some unusual features. These remain of interest especially in the light of recent taxonomic revisions. He was assisted by Goetz and Strauss who likewise had fled from the National Socialist regime. The Madagascar expedition of 1931 was undertaken with the explicit purpose of collecting primate material, but Bluntschli’s developmental series of Microcebus was not published in his lifetime. Thus, although Bluntschli’s reputation was established by his work as a primatologist, no description of his life’s work is complete without reference to his fascinating findings on tenrecs.

ACKNOWLEDGEMENT

Dr. Paula Holahan, Curator of Birds and Mammals at the University of Wisconsin Zoological Museum kindly provided access to photomicrographs by Fritz Strauss from the Harland W. Mossman Embryological Collection. Two anonymous reviewers are thanked for perceptive comments on an earlier version of the manuscript.

CONFLICT OF INTEREST

The author declares no conflict of interest.

FIGURE LEGENDS

Figure 1. Hans Bluntschli in Madagascar with a hedgehog tenrec (probably Setifer setosus). Postcard in the collection of the National Museum of Health and Medicine, Washington D.C.

Figure 2. Ovary of the greater hedgehog tenrec (Setifer setosus). (a) Ripe follicle. There is no antrum. (b) Egg with two pronuclei about to be shed from the follicle. This is evidence of intrafollicular fertilization.

This article is protected by copyright. All rights reserved. Photomicrographs by Dr. Fritz Strauss from the Harland W. Mossman Embryological Collection at the University of Wisconsin Zoological Museum.

Figure 3. Blastula of the lowland streaked tenrec (Hemicentetes semispinosus). Instead of a morula, cleavage resulted in formation of a hollow blastula that later formed the blastocyst. As evidence, Bluntschli published these serial sections of a blastula loosely attached to the uterine mucosa. Reprinted with permission from (Bluntschli, 1937a) © Swiss Zoological Society.

Figure 4. Section through the uterus of the lowland streaked tenrec (Hemicentetes semispinosus) showing the false placental cushion (f. Pl. K.) opposite the implantation site. The embryo is shown with its yolk sac (D.S.). The trophoblast (Tr. Z.) has penetrated the uterine glands and the glandular epithelium has formed a symplasma (Sy.). Other symbols: k. Ep., cubical epithelium; h. Ep., hypertrophied epithelium near the implantation site. Reprinted from (Goetz, 1938b) with permission from Springer/Nature © 1938.

Figure 5. Molecular phylogeny of the superordinal clade Afrotheria. Tenrecs and golden moles (collectively Afrosoricida) are on the same major branch as elephant shrews and aardvark, with which they share some affinities. The second major branch comprises manatees, hyraxes and elephants in Paenungulata. Branch order derived from (Murphy, Eizirik, O'Brien, et al., 2001). Branch lengths are arbitrary and do not refer to a time scale.

TABLE

Table 1. Unusual features of tenrec reproduction and comparison with the closely related golden moles, elephant shrews and aardvark

Tenrecs Golden moles Elephant shrews Aardvark Absence of antral No data Antrum small No data follicles Intra-ovarian No data Not observed No data fertilization Everted corpus luteum Present Present Present Polyovulation (Tenrec Not observed Present in some species Probable and Hemicentetes)

This article is protected by copyright. All rights reserved. Blastula Not present (see text) Present No data Lateral implantation Present Implantation Implantation (Tenrec and mesometrial mesometrial Hemicentetes) False placental pad Present Absent Absent

Anonymous, & Bluntschli, H. (1951). The Bluntschli collection of primate and insectivore embryos. Gift of Albert F. Zahm Yearbook of the Carnegie Institution of Washington, 50, 160-165. Benzenhöfer, U. (2014). Die Universitätsmedizin in Frankfurt am Main von 1914 bis 2014. Münster: Kontur- Verlag. Benzenhöfer, U., & Hack-Molitor, G. (2012). Zur Frankfurter Zeit des Anatomen und Pazifisten Hans Bluntschli. In U. Benzenhöfer (Ed.), Ehrlich, Edinger, Goldstein et al.: Erinnerungswürdige Frankfurter Universitätsmediziner (pp. 83-108). Münster/Ulm: Klemm & Oelschläger. Bluntschli, H. (1904). Der feinere Bau der Leber von Ceratodus forsteri, zugleich ein Beitrag zur vergleichenden Histologie der Fischleber. Jena. Bluntschli, H. (1906). Die Arteria femoralis und ihre Äste bei den niederen catarrhinen Affen. Morph Jb, 36, 276-461. Bluntschli, H. (1937a). Die Frühentwicklung eines Centetinen (Hemicentetes semispinosus Cuv.). Rev Suisse Zool, 44, 271-282. Bluntschli, H. (1937b). Le développement primaire et la formation d'un placenta perforé très compliqué et du type labyrinthe chez Hemicentetes. Bull Acad Malgache, 20, 73-75. Bluntschli, H. (1938). Le developpement primaire et l'implantation chez un Centetine (Hemicentetes). C R Assoc Anat, 33, 39-46. Carter, A. M. (2001). Evolution of the placenta and fetal membranes seen in the light of molecular phylogenetics. Placenta, 22(10), 800-807. doi:10.1053/plac.2001.0739 Carter, A. M., Blankenship, T. N., Enders, A. C., & Vogel, P. (2006). The fetal membranes of the otter shrews and a synapomorphy for afrotheria. Placenta, 27(2-3), 258-268. doi:10.1016/j.placenta.2005.02.019 Carter, A. M., Blankenship, T. N., Kunzle, H., & Enders, A. C. (2004). Structure of the definitive placenta of the tenrec, Echinops telfairi. Placenta, 25(2-3), 218-232. doi:10.1016/j.placenta.2003.08.009 Carter, A. M., Blankenship, T. N., Kunzle, H., & Enders, A. C. (2005). Development of the haemophagous region and labyrinth of the placenta of the tenrec, Echinops telfairi. Placenta, 26(2-3), 251-261. doi:10.1016/j.placenta.2004.06.001 Cener, F. (1990). Der Anatom Hans Bluntschli, 1877-1962. Zurich: Juris. Enders, A. C., Blankenship, T. N., Goodman, S. M., Soarimalala, V., & Carter, A. M. (2007). Placental diversity in malagasy tenrecs: placentation in shrew tenrecs (Microgale spp.), the mole-like rice tenrec (Oryzorictes hova) and the web-footed tenrec (Limnogale mergulus). Placenta, 28(7), 748-759. doi:10.1016/j.placenta.2006.10.003 Enders, A. C., Carter, A. M., Kunzle, H., & Vogel, P. (2005). Structure of the ovaries of the Nimba otter shrew, Micropotamogale lamottei, and the Madagascar hedgehog tenrec, Echinops telfairi. Cells Tissues Organs, 179(4), 179-191. doi:10.1159/000085953 Everson, K. M., Soarimalala, V., Goodman, S. M., & Olson, L. E. (2016). Multiple loci and complete taxonomic sampling resolve the phylogeny and biogeographic history of tenrecs (Mammalia: Tenrecidae) and reveal higher speciation rates in Madagascar's humid forests. Syst Biol, 65(5), 890- 909. doi:10.1093/sysbio/syw034 Foley, N. M., Springer, M. S., & Teeling, E. C. (2016). Mammal madness: is the mammal tree of life not yet resolved? Philos Trans R Soc Lond B Biol Sci, 371(1699). doi:10.1098/rstb.2015.0140 Gabie, V. (1959). The early embryology of Eremitalpa granti (Broom). J Morphol, 104, 181-203.

This article is protected by copyright. All rights reserved. Goetz, R. H. (1933). Zur Analyse der Blutfülle peripherer Gefässgebiete des Menschen. Klin Wochenschr, 12(44), 1717-1719. Goetz, R. H. (1937a). Studien zur Placentation der Centitiden. I. Eine Neu-Untersuchung der Centetesplacenta. Z. Anat. Entwickl., 106, 315-342. Goetz, R. H. (1937b). Studien zur Placentation der Centitiden. II. Die Implantation und Frühentwicklung von Hemicentetes semispinosus (Cuvier). Z Anat Entwickl, 107, 274-318. Goetz, R. H. (1938a). On the early development of the Tenrecoidea (Hemicentetes semispinosus). Biomorphosis, 1, 67-79. Goetz, R. H. (1938b). Studien zur Placentation der Centetiden. III. Die Entwicklung der Fruchthüllen und der Placenta bei Hemicentetes semispinosus (Cuvier). Z Anat Entwickl, 108, 161-200. Goetz, R. H., Jallah, E. M., & Goetz, V. M. (1967). Circulatory dynamics of paired pacing in hypovolemic and cardiogenic shock. Am Heart J, 73(4), 506-515. Greif, R., & Schmutz, H. K. (1995). Hans Bluntschli als Morphologe. Gesnerus, 52, 133-157. Harder, J. D., Stonerook, M. J., & Pondy, J. (1993). Gestation and placentation in two New World opossums: Didelphis virginiana and Monodelphis domestica. J Exp Zool, 266(5), 463-479. doi:10.1002/jez.1402660511 Hildebrandt, S. (2012). Anatomy in the Third Reich: Careers disrupted by National Socialist Policies. Ann Anat, 194(3), 251-266. doi:10.1016/j.aanat.2011.08.009 Hildebrandt, S., & Redies, C. (2012). Anatomy in the Third Reich. Ann Anat, 194(3), 225-227. doi:10.1016/j.aanat.2011.08.006 Horst, C. J. v. d. (1942). Early stages in the embryonic development of Elephantulus. S. Afr. J. Med. Sci. Biol. Suppl., 7, 55-65. Horst, C. J. v. d. (1949). An early stage of placentation in the aard vark, Orycteropus. Proc. Zool. Soc. Lond., 119, 1-18. Horst, C. J. v. d., & Gillman, J. (1940). Mechanism of ovulation and corpus luteum formation in Elephantulus. Nature, 145, 974. Hubrecht, A. A. W. (1889). Studies in Mammalian Embryology, I. The Placentation of Erinaceus europaeus, with remarks on the phylogeny of the placenta. Q J Microsc Sci, 30, 283-404. Kleisner, K., Ivell, R., & Flegr, J. (2010). The evolutionary history of testicular externalization and the origin of the scrotum. J Biosci, 35(1), 27-37. Konstantinov, I. E. (2000). Robert H. Goetz: the surgeon who performed the first successful clinical coronary artery bypass operation. Ann Thorac Surg, 69(6), 1966-1972. Kreft, G. (2008). "...nunmehr judenfrei..." Das Neurologische Institut 1933 bis 1945. In J. Kobes & J. O. Hesse (Eds.), Frankfurter Wissenschaftler zwischen 1933 und 1945 (pp. 125-156). Göttingen: Wallstein Verlag. Lange, D. d. (1919). Contribution to the knowledge of the placentation of the Cape goldmole (Chrysochloris). Bijd Dierkunde Amsterdam, 21, 161-173. Lillegraven, J. A. (1985). Use of the term 'trophoblast' for tissues in therian mammals. J Morphol, 183(3), 293-299. Mack, A. F., Kunzle, H., Lange, M., Mages, B., Reichenbach, A., & Hartig, W. (2018). Radial glial elements in the cerebral cortex of the lesser hedgehog tenrec. Brain Struct Funct, 223(9), 3909-3917. doi:10.1007/s00429-018-1730-1

This article is protected by copyright. All rights reserved. Madsen, O., Scally, M., Douady, C. J., Kao, D. J., DeBry, R. W., Adkins, R., . . . Springer, M. S. (2001). Parallel adaptive radiations in two major clades of placental mammals. Nature, 409(6820), 610-614. doi:10.1038/35054544 McKenna, M. C., & Bell, S. K. (1997). Classification of mammals above the species level. New York, & Chichester, West Sussex: Columbia University Press. Mitchell, G. (2008). Robert Goetz: A pioneer of the study of the physiology of animals in the wild. Trans R Soc South Africa, 63(2), 182-185. Mossman, H. W. (1987). Vertebrate fetal membranes : comparative ontogeny and morphology; evolution; phylogenetic significance; basic functions; research opportunities. Basingstoke: Macmillan : Rutgers University Press. Mossman, H. W. (1990). My Life (unpublished manuscript). University of Wisconsin. Madison, Wisconsin. Mossman, H. W., & Duke, K. L. (1973). Comparative Morphology of the Mammalian Ovary. Madison University of Wisconsin Press. Mossman, H. W., & Strauss, F. (1963). The fetal membranes of the pocket gopher illustrating an intermediate type of rodent membrane formation. II. From the beginning of the allantois to term. Am J Anat, 113, 447-477. doi:10.1002/aja.1001130307 Murphy, W. J., Eizirik, E., Johnson, W. E., Zhang, Y. P., Ryder, O. A., & O'Brien, S. J. (2001). Molecular phylogenetics and the origins of placental mammals. Nature, 409(6820), 614-618. doi:10.1038/35054550 Murphy, W. J., Eizirik, E., O'Brien, S. J., Madsen, O., Scally, M., Douady, C. J., . . . Springer, M. S. (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science, 294(5550), 2348-2351. doi:10.1126/science.1067179 Nicoll, M. E., & Racey, P. A. (1985). Follicular development, ovulation, fertilization and fetal development in tenrecs (Tenrec ecaudatus). J Reprod Fertil, 74(1), 47-55. O'Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., . . . Cirranello, A. L. (2013). The placental mammal ancestor and the post-K-Pg radiation of placentals. Science, 339(6120), 662-667. doi:10.1126/science.1229237 Reng, R. (1977). Die Placenta von Microcebus murinus Miller. Z Saugetierk, 42(4), 201-214. Riedelsheimer, B., Unterburger, P., Kuenzle, H., & Welsch, U. (2007). Histological study of the cloacal region and associated structures in the hedgehog tenrec Echinops telfairi. Mammal Biol, 72(6), 340-341. Rosenstein, C. (1958). Der Brunnen. Eine Familienchronik (manuscript). Stankowich, T., & Stensrud, C. (2019). Small but spiny: the evolution of antipredator defenses in Madagascar tenrecs. Journal of Mammalogy, 100(1), 13-20. doi:10.1093/jmammal/gyz003 Strauss, F. (1938a). Die Befruchtung und der Vorgang der Ovulation bei Ericulus aus der Familie der Centetiden. Biomorphosis, 1, 281-312. Strauss, F. (1938b). Die Bildung des Corpus luteum bei Centetiden. Biomorphosis, 1, 489-544. Strauss, F. (1943). Die Placentation von Ericulus setosus. Rev Suisse Zool, 50, pp. 17-87. Strauss, F. (1944). Die Implantation des Keimes, die Frühphase der Placentation und die Menstruation im Licht vergleichend-embryologischer Erfahrungen. Bern: Paul Haupt. Strauss, F. (1956). The time and place of fertilization of the golden hamster egg. J Embryol Exp Morphol, 4, 42-56. Strauss, F. (1957). Die Placenta des Feldhasen. Acta Anatomica, 30, 815-826. Strauss, F. (1963). Weibliche Geschlechtsorgane. In J. G. L. Helmcke, H.; Starck, D.; Wermuth, H. (Ed.), Handbuch der Zoologie (Vol. 9 (3), pp. 1-96, 97-202). Berlin: Walter de Gruyter.

This article is protected by copyright. All rights reserved. Strauss, F. (1964). Zum Andenken an Hans Bluntschli, 1877-1962. Acta Anat (Basel), 58, 1-25. Strauss, F. (1978). Eine Neuuntersuchung der Implantation und Placentation bei Microcebus murinus. Mitt Naturforsch Ges Bern, 35, 107-119. Treat, M. D., Scholer, L., Barrett, B., Khachatryan, A., McKenna, A. J., Reyes, T., . . . van Breukelen, F. (2018). Extreme physiological plasticity in a hibernating basoendothermic mammal, Tenrec ecaudatus. J Exp Biol, 221(Pt 20). doi:10.1242/jeb.185900 Tripp, H. R. (1971). Reproduction in elephant-shrews (Macroselididae) with special reference to ovulation and implantation. J Reprod Fertil, 26(2), 149-159. Tyndale-Biscoe, C. H., & Renfree, M. (1987). Reproductive Physiology of Marsupials. Cambridge: CUP. Weber, W. (1995). Dem Andenken an Prof. Dr. med. Fritz Strauss. Ann Anat, 177, 395-396. Weir, B. J. (1971). The reproductive organs of the female plains viscacha, Lagostomus maximus. J Reprod Fertil, 25(3), 365-373.