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Early Development of the Neural Plate, Neural Crest and Facial Region of Marsupials

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Early Development of the Neural Plate, Neural Crest and Facial Region of Marsupials J. Anat. (2001) 199, pp. 121–131, with 9 figures Printed in the United Kingdom 121 Early development of the neural plate, neural crest and facial region of marsupials KATHLEEN K. SMITH Department of Biology, Duke University, Durham, NC, USA (Accepted 11 April 2001) Marsupial mammals have a distinctive reproductive strategy. The young are born after an exceptionally short period of organogenesis and are consequently extremely altricial. Yet because they must be functionally independent in an essentially embryonic condition, the marsupial neonate exhibits a unique suite of adaptations. In particular, certain bones of the facial region, most cranial musculature and a few additional structures are accelerated in their development. In contrast, central nervous system structures, especially the forebrain, are markedly premature at birth, resembling an embryonic d 11 or 12 mouse. This review examines the developmental processes that are modified to produce these evolutionary changes. The focus is on the early development of the neural plate, neural crest and facial region in the marsupial, Monodelphis domestica, compared with patterns reported for rodents. Neural crest begins differentiation and migration at the neural plate stage, which results in large accumulations of neural crest in the facial region at an early stage of development. The early accumulation of neural crest provides the material for the accelerated development of oral and facial structures. The first arch region is massive in the early embryo, and the development of the olfactory placode and frontonasal region is advanced relative to the forebrain region. The development of the forebrain is delayed in marsupials relative to the hindbrain or facial region. These observations illustrate how development may be modified to produce evolutionary changes that distinguish taxa. Further, they suggest that development is not necessarily highly conserved, but instead may be quite plastic. Key words: Heterochrony; mammal; craniofacial development; Monodelphis. the embryonic state of the neonate, it must be able to independently travel to, identify and attach to the Marsupial and placental mammals are distinguished teat. The oral apparatus must be sufficiently developed by significant differences in reproductive and life to suckle, and the major physiological systems history strategies. Metatherian mammals are born (circulatory, respiratory, digestive and excretatory) after a short gestation and a particularly short period must be functional. This contrasts with eutherian of organogenesis. The organogenic period ranges mammals in which maternal investment is more evenly from 11 d in some kangaroos, to no more than 2n5d divided between intrauterine and lactational periods, in many dasyurids (Tyndale-Biscoe & Renfree, 1987; and most morphogenesis is intrauterine (Renfree, Rose, 1989). All marsupials are highly altricial at 1983). Even the most altricial eutherian is well birth, with an overall stage of development resembling developed at birth relative to the marsupial neonate an 11 or 12 d embryonic mouse, or an approximately (Eisenberg, 1981). The evolutionary consequences, 10 wk human embryo. The major portion of mor- significance, advantages and disadvantages of these 2 phogenesis and of maternal investment in the young patterns of life history strategy have been discussed in occurs during an extended lactation period. Despite an extensive literature (e.g. Tyndale-Biscoe, 1973; Correspondence to Dr Kathleen K. Smith, Box 90338, Department of Biology, Duke University, Durham, NC 27708, USA. Tel.: j1 919 684 3402; fax: j1 919 660 7293; e-mail: kksmith!duke.edu 122 K. K. Smith Lillegraven, 1975, 1979, 1984; Kirsch, 1977a, b; of their development (Fig. 2A). At birth, ear and eye Parker, 1977; Russell, 1982; Renfree, 1983, 1995; primordia are barely visible and the head is virtually Hayssen et al. 1985; Lee & Cockburn, 1985; all nose and mouth. There is an extreme gradient Lillegraven et al. 1987; Thompson, 1987; Tyndale- between the fore- and hindlimbs, so that while the Biscoe & Renfree, 1987; Cockburn, 1989). forelimbs are robust, the hindlimbs are barely beyond In order for the neonate to function at this overall bud stage. Cartilage is poorly differentiated. For embryonic state, the morphological configuration example, in the forelimbs of the newborn Tasmanian must differ from that seen in even the most altricial devil (Sarcophilus harrisii), the metacarpals are pres- placental mammal (Esdaile, 1916; Hartman 1919; ent, but the phalanges have not yet differentiated Hill & Hill, 1955; Mu$ ller, 1967, 1972a, b; Nelson, (Hughes & Hall, 1988). Perhaps most unusual is the 1981, 1987; Maier, 1984, 1987, 1993, 1999; Hall & large mass of undifferentiated mesenchyme that Hughes, 1987; Klima, 1987; Gemmell & Nelson, occupies the throat and chest region (Fig. 2A). This 1988a, b, 1992; Hughes & Hall, 1988; Filan, 1991; mass is transient and serves to support passively the Clark & Smith, 1993; Gemmell and Selwood, 1994; head and neck of the highly altricial neonate (Hill & Smith, 1994; Frigo & Woolley, 1996). There is an Hill, 1955). overall rostral–caudal gradient in development so that The development of the craniofacial region in the cranial, cervical and upper thoracic regions are marsupials is of particular interest. This region is well developed with little development of posterior exceedingly complex functionally, morphologically regions. The forelimb is particularly large, as are the and developmentally. Many systems, such as the vertebrae in the cervical region. In the head, the central nervous system, the cranial sense organs, and chondrocranium is massive, particularly in the nasal the skeletal and muscular systems are thought to region, and the bones around the oral apparatus are develop in a highly coordinated manner. Further, in developed precociously. Most craniofacial muscles marsupials a number of elements of the craniofacial are well developed and the tongue is particularly region must be functional at a time when much of this large. In contrast, the brain is at an embryonic state of region is just beginning morphogenesis. It has long development, and the bones around the calvaria have been recognised that these functional requirements not yet developed (Fig. 1). Furthermore, the jaw joint have contributed to specific heterochronies and that is uniquely configured. While it superficially resembles some components of the face and oral region develop the primitive condition, with the joint being formed early and rapidly in marsupials relative to eutherians. by the cartilaginous anlagen of the malleus and incus, The patterns of craniofacial development in mar- it also possesses a number of derived features (Filan, supial and placental mammals have been reported in 1991; Maier, 1993). a series of papers (Smith, 1996, 1997, 2000; Nunn & Within marsupials, the variation in degree of Smith, 1998). These studies investigated craniofacial development at birth is narrow, and does not match development during the late organogenic period, from the altricial-precocial spectrum seen in eutherians. approximately the evagination of the telencephalon, However, there is variation between the most and to the last ossification of all bones in the cranium. The least developed marsupial (Hall & Hughes, 1987; analyses included 4 marsupial species (Monodelphis Hughes & Hall, 1988). In phalangers and kangaroos domestica, Macropus eugenii, Perameles nasuta, (Diprotodontia), there is generally a single young that Dasyurus viverrinus), and 6 placental species (Felis weighs between 200 and 800 mg at birth (adult weight domestica, Manis javanica, Mus musculus, Sus scrofa, between 500 g and 27 kg). In these taxa, young are Tarsius spectrum, Tupaia javanica). A major con- relatively well developed with prominent external ear clusion was that, in addition to the patterns discussed and eye primordia, retinal pigmentation, significant above, marsupials were characterised by a delay in the differentiation (e.g. digits present) in the hindlimb, development of major structures in the central nervous and pronounced differentiation of the mandible. The system and an advancement of the development of head and neck are morphologically distinct, and elements in the oral and facial regions. mature cartilaginous elements in the head and Specifically, the initial ossification of the dentary, forelimb (e.g. phalanges) are distinguishable (Hughes maxillary, premaxillary and exoccipital bones, and the & Hall, 1988; Fig. 2B). In contrast, the dasyurid closure of the secondary palate, occurred early in neonate is ultra-altricial. In these taxa, the newborn marsupials relative to placentals. Events that were late weighs between 5 and 20 mg (adult weight between 8 g in marsupials relative to placentals included the and 12 kg), and litter sizes are often as large as 12. evagination of the telencephalon, contact between the These young are remarkable in the rudimentary nature olfactory bulb and the olfactory epithelium, layering Development of neural crest in marsupials 123 Fig. 2. Embryos of newborn (A) Dasyurus viverrinus (redrawn from Hill & Hill, 1955), and (B) Trichosurus vulpecula (redrawn from Klima & Bangma, 1987). These drawings are not to scale. The D. viverrinus neonate is 6 mm in length and generally weighs 12n5 mg. The T.vulpecula neonate is 15 mm in length and generally weighs 200 mg. Note the extreme difference between fore- and hindlimb development, the existence of a large undifferentiated mass in the thorax and cervical region,
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