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4 Mammalian Embryology and Organogenesis Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2018 4. Mammalian embryology and organogenesis Werneburg, Ingmar ; Spiekman, Stephan N F Abstract: 4.1 Historical introduction : The origin of the human being is one of the major philosophical questions. One way of answering it is through an ontogenetic and evolutionary approach. Theories about the developmental origin in the mother’s womb were first documented by Greek scholars in the 5th century BC (Breidbach 2015). Being dependent on the success of reproduction, fertility has triggered human thinking for a much longer period of human evolution as is documented in the art of the Paleolithic, the Mesolithic, the Neolithic, and later phases of human cultural evolution (Fig. 4.1). Fertility was manifested by the representation of stout mother goddesses with a demonstrative focus on their hips and breasts (Fig. 4.1 C) and by the presentation of erect penises in men (Fig. 4.1 G). In some cases, the process of birth was depicted as a key event of life (Fig. 4.1 D). Birth, pregnancy, and lactation of other vertebrate species were also of interest to ancient cultures and were illustrated, particularly, among species that played an important role in everyday life, such as prey and domesticated, mostly mammalian, animals (Fig. 4.1 A and I). Fertility rites, including hierogamy (Fig. 4.1 H) and sodomy (Fig. 4.1 J), are thought to have played a major role in prehistoric cults and were meant to increase the number of offspring and to guarantee their health (Frazer 1922, Campbell 1960). These attempts to understand and to influence our own development culminated in the artificial representation of homunculi in the Renaissance age,in which a human was “created” by alchemists in a jar. The mental construct of a test-tube baby (Fig. 4.1 K) was a symbol for the development of the human mind itself, which alchemists tried to raise to a higher level of cognition (Gebelein 1996, Wiesing 2004). The historical representation of homunculi also corresponds to the ideas of preformationists in the 17th century that the human being is fully present as a miniature in the male’s sperm and only has to unfold to progress through embryological development to a fully formed human (Fig. 4.1 F; Hartsoeker 1694). With the rise of evolutionary thinking (Bell et al. 2010), a broad scientific discourse about the unique anatomy and development of mammalian species emerged. Mammalian embryology received particular attention in comparative anatomy and physiology because of its relevance in understanding our own biological history (Haeckel 1874,1877, Keibel 1906). Recent scientific approaches try to manipulate the early embryology of mammals, including man,to prevent diseases (Gilbert 2006) or to select for particular forms through domestication (Clutton-Brock 1999). Experimental biological studies mainly focus on model organisms that are easy to breed, have a large number of offspring, and have short reproductive cycles. For placental embryology, the house mouse Mus musculus is most often used (Cook 1965, Green 1968, Theiler 1989, Hedrich 2012). Among marsupials, the opossum Monodelphis domestica and the wallaby Macropus eugenii are two of the most important model organisms (e.g., Smith 2002, Hickford et al. 2009, Keyte and Smith 2009, Rousmaniere et al. 2010). However, recent studies have highlighted the value of nonmodel organisms for testing the taxonomic applicability of experimental studies, and more evolutionary questions are being asked that require extensive knowledge of non-model organisms all over the tree of life (Butler and Juurlink 1987, Jenner and Wills 2007, Milinkovitch and Tzika 2007, Tzika and Milinkovitch 2008), including mammals (Werneburg et al. 2013). The aim of the present chapter is to provide a general overview of the main developmental differences among the three major mammalian groups, to characterize mammals among amniotes, and to present some crucial aspects of the anatomy and physiology of mammalian embryogenesis. We cover different aspects of embryology in a chronological order. We first discuss particular attributes of monotremes, followed by marsupials and lastly placental mammals. We also focus on the developmental peculiaritiesin humans. Finally, we summarize some discussions on the potential relationships between life history parameters and evolutionary patterns. The selection of topics is mainly anatomically oriented and reflects our personal morphological interest. It does not aim to represent an in-depth review of all aspects of mammalian embryology, nor does it aim to be complete. As new data, we present a reconstruction of the ancestral developmental sequence of external organ characters for Placentalia, which is based on a phylogenetic comparison of about 80 tetrapod species. DOI: https://doi.org/10.1515/9783110341553-004 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-165594 Book Section Published Version Originally published at: Werneburg, Ingmar; Spiekman, Stephan N F (2018). 4. Mammalian embryology and organogenesis. In: Zachos, Frank; Asher, Robert. Mammalian Evolution, Diversity and Systematics. Berlin: Walter de Gruyter, 59-116. DOI: https://doi.org/10.1515/9783110341553-004 2 Ingmar Werneburg, Stephan N. F. Spiekman 4 Mammalian embryology and organogenesis 4.1 Historical introduction anatomy and physiology because of its relevance in understanding our own biological history (Haeckel 1874, The origin of the human being is one of the major philo- 1877, Keibel 1906). sophical questions. One way of answering it is through an Recent scientific approaches try to manipulate the ontogenetic and evolutionary approach. Theories about early embryology of mammals, including man, to prevent the developmental origin in the mother’s womb were diseases (Gilbert 2006) or to select for particular forms first documented by Greek scholars in the 5th century through domestication (Clutton-Brock 1999). Experimen- BC (Breidbach 2015). Being dependent on the success of tal biological studies mainly focus on model organisms reproduction, fertility has triggered human thinking for a that are easy to breed, have a large number of offspring, much longer period of human evolution as is documented and have short reproductive cycles. For placental embry- in the art of the Paleolithic, the Mesolithic, the Neolithic, ology, the house mouse Mus musculus is most often used and later phases of human cultural evolution (Fig. 4.1). (Cook 1965, Green 1968, Theiler 1989, Hedrich 2012). Fertility was manifested by the representation of stout Among marsupials, the opossum Monodelphis domestica mother goddesses with a demonstrative focus on their hips and the wallaby Macropus eugenii are two of the most and breasts (Fig. 4.1 C) and by the presentation of erect important model organisms (e.g., Smith 2002, Hickford et penises in men (Fig. 4.1 G). In some cases, the process of al. 2009, Keyte and Smith 2009, Rousmaniere et al. 2010). birth was depicted as a key event of life (Fig. 4.1 D). Birth, However, recent studies have highlighted the value of non- pregnancy, and lactation of other vertebrate species were model organisms for testing the taxonomic applicability also of interest to ancient cultures and were illustrated, of experimental studies, and more evolutionary ques- particularly, among species that played an important role tions are being asked that require extensive knowledge in everyday life, such as prey and domesticated, mostly of non-model organisms all over the tree of life (Butler mammalian, animals (Fig. 4.1 A and I). Fertility rites, and Juurlink 1987, Jenner and Wills 2007, Milinkovitch including hierogamy (Fig. 4.1 H) and sodomy (Fig. 4.1 J), and Tzika 2007, Tzika and Milinkovitch 2008), including are thought to have played a major role in prehistoric cults mammals (Werneburg et al. 2013). and were meant to increase the number of offspring and to The aim of the present chapter is to provide a general guarantee their health (Frazer 1922, Campbell 1960). overview of the main developmental differences among the These attempts to understand and to influence our three major mammalian groups, to characterize mammals own development culminated in the artificial representa- among amniotes, and to present some crucial aspects of tion of homunculi in the Renaissance age, in which a the anatomy and physiology of mammalian embryogene- human was “created” by alchemists in a jar. The mental sis. We cover different aspects of embryology in a chron- construct of a test-tube baby (Fig. 4.1 K) was a symbol for ological order. We first discuss particular attributes of the development of the human mind itself, which alche- monotremes, followed by marsupials and lastly placental mists tried to raise to a higher level of cognition (Gebe- mammals. We also focus on the developmental peculiar- lein 1996, Wiesing 2004). The historical representation ities in humans. Finally, we summarize some discussions of homunculi also corresponds to the ideas of preforma- on the potential relationships between life history param- tionists in the 17th century that the human being is fully eters and evolutionary patterns. The selection of topics is present as a miniature in the male’s sperm and only has mainly anatomically oriented and reflects our personal to unfold to progress through embryological development morphological interest. It does not aim to represent an to a fully formed human
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