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For Peer Review Journal: Journal of Morphology CORE Metadata, citation and similar papers at core.ac.uk Journal of Morphology Provided by Digital.CSIC The Morphology of Pre-hatching Embryos of Caecilia orientalis (Amphibia: Gymnophiona: Caeciliidae) For Peer Review Journal: Journal of Morphology Manuscript ID: draft Wiley - Manuscript type: Research Article Date Submitted by the n/a Author: Complete List of Authors: Perez, Oscar; Pontificia Universidad Catolica del Ecuador, School of Biological Science Lai, Ngan; University of California, Berkeley, Integrative Biology Buckley, David; University of California, Berkeley, Integrative Biology del Pino, Eugenia; Pontificia Universidad Catolica del Ecuador, School of Biological Science Wake, Marvalee; Univ of California, Integrative Biology Keywords: caecilian, direct development, bone mineralization, tooth crowns John Wiley & Sons Page 1 of 36 Journal of Morphology 1 2 3 4 5 6 7 8 9 10 11 The Morphology of Pre-hatching Embryos of Caecilia orientalis (Amphibia: 12 13 Gymnophiona: Caeciliidae) 14 15 16 17 18 For Peer Review 19 20 21 22 23 Oscar D. Pérez 1, Ngan Betty Lai 2, David Buckley 2, Eugenia M. del Pino 1, and Marvalee 24 25 2 26 H. Wake * 27 28 29 30 1 School of Biological Sciences, Pontificia Universidad Católica del Ecuador, Quito, 31 32 33 Ecuador 34 35 2Department of Integrative Biology and Museum of Vertebrate Zoology, University of 36 37 California, Berkeley, CA 94720-3140 38 39 40 41 42 43 44 Running head: Pre-hatching caecilian embryo morphology 45 46 47 48 49 *Correspondence to: 50 Marvalee H. Wake 51 52 Department of Integrative Biology 53 3060 VLSB 54 University of California 55 Berkeley, CA 94720-3140 USA 56 e-mail: [email protected] 57 Phone: 1510 642-4743 58 59 60 1 John Wiley & Sons Journal of Morphology Page 2 of 36 1 2 3 ABSTRACT 4 5 A clutch of advanced embryos of the direct-developing caecilian Caecilia orientalis 6 7 (Caeciliidae: Gymnophiona: Amphibia) was collected in the field in Ecuador. Specimens 8 9 were cleared and stained in order to evaluate skeletal development (each element of the 10 11 12 chondrocranium, dermatocranium, jaws and teeth, hyobranchial apparatus, vertebrae) at 13 14 near-hatching. Because it is established that development is correlated with reproductive 15 16 modes in a number of features, we included comparison with taxa that represent the 17 18 For Peer Review 19 major reproductive modes and all of the modern normal tables and ossification 20 21 sequences. The embryos most closely resembled stage 47/48 Gegeneophis ramaswamii, 22 23 24 an Indian caeciliid, and stage 45-48 Hypogeophis rostratus , a Seychellian caeciliid, both 25 26 direct developers, in details of bone mineralization, chondrocranial degeneration, and 27 28 vertebrogenesis, and stage 42 H. rostratus in external features (gills, pigmentation, etc.). 29 30 31 They were less like pre-hatchlings of Ichthyophis kohtaoensis , an ichthyophiid with free- 32 33 living larvae, and fetuses of the viviparous caeciliid Dermophis mexicanus and the 34 35 viviparous typhlonectid Typhlonectes compressicauda at comparable total lengths. A 36 37 38 correlation of developmental features with mode of life history is implied. A noteworthy 39 40 feature is that the direct-developing C. orientalis has an armature of multiple rows of 41 42 teeth on the lower jaw with tooth crowns that resemble the “fetal” teeth of viviparous 43 44 45 taxa and that are covered with a layer of oral mucosal epithelium until full development 46 47 and eruption, but the upper jaw bears a single row of widely spaced, elongate, slightly 48 49 50 recurved teeth that resemble those of the adult. 51 52 53 54 Key words: caecilian, direct development, bone mineralization, tooth crowns 55 56 57 58 59 60 2 John Wiley & Sons Page 3 of 36 Journal of Morphology 1 2 3 Caecilians (Amphibia: Gymnophiona) are elongate, limbless, tailless or nearly so 4 5 6 animals that inhabit most of the tropical regions of the world. They are not often 7 8 observed because they are fossorial or secondarily aquatic to semi-aquatic. However, 9 10 11 information is accruing about their biology and the nature of their adaptive radiation. In 12 13 particular, their reproductive biology is of interest because it includes several different 14 15 modes. Apparently all caecilians have internal fertilization via the male intromittent 16 17 18 organ inserted intoFor the vent of Peerthe female to transportReview sperm. Eggs may be laid 19 20 terrestrially shortly after fertilization, with the mother guarding the clutch until hatching, 21 22 when larvae wriggle into streams for a relatively lengthy period up to one year before 23 24 25 metamorphosing and returning to land. Alternatively, development through 26 27 metamorphosis ensues before hatching and a juvenile emerges, obviating the aquatic, 28 29 free-living larval stage. In addition, a number of species are viviparous, retaining the 30 31 32 developing embryos in the maternal oviducts through metamorphosis, so that juveniles 33 34 are born. Yolk is resorbed early during the gestation period, which may be 7-11 months 35 36 37 depending on the species, and nutrient secretions from the mother’s oviductal mucosa 38 39 nourish the fetuses, which actively “forage” in the oviducts (see Wake, 1977ab; 40 41 Himstedt, 1996; Exbrayat, 2000, 2006 for summaries). Recently, it has been observed 42 43 44 that two distantly related direct-developing caeciliid species, the east African 45 46 Boulengerula taitanus and the South American Siphonops annulatus, have precocial 47 48 hatching and the young eat the skin and its secretions of the mother (Kupfer, et al. 2006; 49 50 51 Wilkinson et al., 2008). 52 53 Caecilia orientalis (Taylor, 1968) occurs in the eastern lowlands of 54 55 Ecuador, and its reproductive mode was unknown until the discovery of an egg clutch at 56 57 58 59 60 3 John Wiley & Sons Journal of Morphology Page 4 of 36 1 2 3 the Yanayacu Biological Station in January 2001 (Funk et al., 2004). The rare availability 4 5 6 of a clutch of living embryos of the direct-developing C. orientalis allowed examination 7 8 of several aspects of their biology. For example, an observation derived from the single 9 10 11 clutch of C. orientalis has yielded information about caecilian evolution. The lamina- 12 13 associated polypeptide 2 (LAP2) is an integral protein of the inner nuclear membrane in 14 15 mammals, fish and frogs (reviewed by Dechat et al., 2000; Prüfert et al., 2004). LAP2 16 17 18 expression in somaticFor cells of C.Peer orientalis and Review C. guntheri is strikingly different from 19 20 that of anuran and urodele amphibians (del Pino et al., 2002). Caecilian somatic cells 21 22 include three LAP2 isoforms with electrophoretic motilities comparable to those of the 23 24 25 LAP2 α, β, and γ of mammals (del Pino et al., 2002). Mammalian cells express mainly 26 27 LAP2 α, β, and γ whereas in somatic cells of the frog Xenopus laevis only LAP2 β 28 29 30 isoforms have been detected (Lang et al., 1999). Consequently, LAP2 α is considered a 31 32 mammalian character, and has not been detected in cells of frogs, fish and the chick (del 33 34 35 Pino et al., 2002; Lang et al., 1999; Prüfert et al., 2004). Further analysis of the LAP2 36 37 isoforms found in somatic tissues of caeciliids and other caecilians is required to 38 39 determine whether the caeciliid LAP2 pattern of somatic cells is molecularly similar to 40 41 42 that of mammals. We mention this example to support the necessity of fieldwork for 43 44 molecular studies and the multidisciplinary approach to research on rare taxa. 45 46 We present information on the developmental morphology of the embryos of C. 47 48 49 orientalis based on examination of living and preserved members of that one clutch 50 51 known to science. Caecilian development is known from only a few normal tables and 52 53 54 descriptions of various stages of embryos and larvae for very few species. Because so 55 56 57 58 59 60 4 John Wiley & Sons Page 5 of 36 Journal of Morphology 1 2 3 little is known, this report on a clutch at a particular stage of development presents new 4 5 6 information to contribute to the comparative developmental morphology of caecilians. 7 8 MATERIALS AND METHODS 9 10 11 Specimens 12 13 Three adults (two males and a female), an uncharacterized individual, and an egg 14 15 16 clutch were found under a large decomposing log at the Yanayacu Biological Station, 17 18 Napo Province, EcuadorFor at 00°35’S Peer 77°53’ W.Review The station is located in a region of cloud 19 20 forest at an altitude of approximately 2100 m on the east side of the Cordillera Oriental of 21 22 23 the Andes. The adults and two embryos were preserved and deposited in the Museum of 24 25 Zoology of the Pontificia Universidad Católica del Ecuador (QCAZ). The remaining five 26 27 embryos were maintained for further study. The simultaneous occurrence of adults and 28 29 30 the egg clutch under a log allowed identification of the specimens as Caecilia orientalis 31 32 (see Funk et al., 2004) . 33 34 35 Culture medium and fixation 36 37 The embryos of C. orientalis were cultured by two methods: (1) the egg clutch 38 39 was maintained in a humid chamber that consisted of a 10 cm Petri dish with a bottom 40 41 42 covered by wet filter paper. The egg clutch was placed over a small piece of plastic foil to 43 44 prevent the egg jelly from sticking to the filter paper.
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