Pecularities of bony skeleton development in Asian clawed salamanders (Onychodactylus, Hynobiidae) related to embryonization

Abstract

We studied skull, vertebral column, and limb skeleton development in Japanese clawed sala mander Onychodactylus japonicus (Hynobiidae). The study is based on the ontogenetic series of embryos and larvae obtained from wild captured adults by artificial induction of breeding using hormonal stimulation. The first stages of the skeleton formation in O. japonicus are shifted to the late embryonic period and hatching lar vae already possess a well ossified vertebral column, large number of skull ossifications and show signs of ossi fication in the forelimb skeleton. Compared to the primitive pattern of the skeleton development typical for other hynobiid salamanders, O. japonicus shows a number of heterochronies related to embryonization. In particular, this species is characterized by an earlier ossification of the vertebral column compared to that of the skull and by the delayed development and early reduction of the coronoid. Our results, along with the pre viously reported data on the skeleton development in the Fischer's clawed salamander O. fischeri (Smirnov and Vassilieva, 2002), indicate that the genus Onychodactylus is characterized by the loss or reduction of sev eral skeletal features typically found at early larval stages in other Hynobiidae species. In particular, provi sional bones (especially the coronoid) and their dentition are underdeveloped. In addition, it is corroborated that the first tooth generation is absent in Onychodactylus, whereas such monocuspid nonpedicellate tooth generation normally develops at the early larval stages of other caudate amphibians. Since similar patterns of skeleton ontogeny are observed in other caudate groups with different extent of embryonization, it is pro posed that, in different lineages of Urodela, the evolution of ontogeny followed similar pathways and was accompanied by the same changes in skeletogenesis.

A new hynobiid-like salamander (Amphibia, Urodela) from Inner Mongolia, China, provides a rare case study of developmental features in an Early Cretaceous fossil urodele

“…The premaxillary teeth in the latter specimen are apparently pedicellate, indicating that in this fossil form the pedicellate condition was achieved earlier than bicuspid crown pattern before metamorphosis. Such a developmental pattern has been documented for extant salamanders, including the hynobiids Hynobius nebulosus and Salamandrella keyserlingii ( Greven & Clemen, 1985 ), Hynobius formosanus ( Vassilieva et al, 2015 ), Onychodactylus fischeri ( Smirnov & Vassilieva, 2002a ), Onychodactylus japonicus ( Vassilieva, Poyarkov & Iizuka, 2013 ), and Ranodon sibiricus ( Vassilieva & Smirnov, 2001 ).…”

“…5 ). The septomaxilla ontogenetically ossifies immediately before or during metamorphosis in the extant hynobiids Onychodactylus ( Vassilieva, Poyarkov & Iizuka, 2013 ), Ranodon ( Schmalhausen, 1968 ; Lebedkina, 2004 ), Salamandrella ( Schmalhausen, 1958 ; Lebedkina, 1964 ; Regel, 1970 ), and Hynobius ( Vassilieva et al, 2015 ).…”

“…The posterolateral process of the parietal is boot-like, in articulation with the prootic, the opisthotic-exoccipital complex posteroventrally, and with the squamosal laterally. A parietal-squamosal contact is plesiomorphically present in cryptobranchids, most hynobiids except Onychodactylus ( Smirnov & Vassilieva, 2002a ; Fei et al, 2006 ; Vassilieva, Poyarkov & Iizuka, 2013 ) and a few species of Hynobius ( Sato, 1943 ; Nambu, 1991 ; Fei et al, 2006 ).…”

“…The exoccipital and opisthotic were reported as unfused in the stem caudate Kokartus ( Skutschas & Martin, 2011 ). In extant salamanders, the fused opisthotic-exoccipital complex with a free prootic is found in all cryptobranchoids ( Carroll & Holmes, 1980 ; Gao & Shubin, 2012 ), except in Onychodactylus , in which the prootic also is fused with the opisthotic-exoccipital complex ( Smirnov & Vassilieva, 2002a ; AmphibiaTree, 2007a ; Vassilieva, Poyarkov & Iizuka, 2013 ).…”

“…The articular is a tiny bone ossified posterodorsally at the end of the lower jaw as observed in adult specimens. The absence of the bone in larval (PKUP V0417–V0420) and postmetamorphic juvenile (PKUP V0416) specimens indicates its delayed ossification after metamorphosis as occurs in extant hynobiids ( Smirnov & Vassilieva, 2002a ; Smirnov & Vassilieva, 2002b ; Lebedkina, 2004 ; Vassilieva, Poyarkov & Iizuka, 2013 ; Vassilieva et al, 2015 ). Among extant cryptobranchoids, the articular is absent by fusion with the prearticular in Cryptobranchidae but is present in Hynobiidae ( Zhang, 1985 ; Rose, 2003 ; Clemen & Greven, 2009 ; Zhang, Liu & Zhao, 2009 ; Vassilieva et al, 2015 ).…”