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      A review of the reproductive biology of the only known matrotrophic viviparous anuran, the West African Nimba toad, Nimbaphrynoides occidentalis

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      Zoosystematics and Evolution

      Pensoft Publishers

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          Abstract

          Amphibians, and anurans in particular, show the highest diversity of reproductive modes among tetrapods. Nevertheless, viviparity is scarce in anurans and its occurrence is even more often assumed rather than confirmed. Probably the best studied viviparous amphibian is the Nimba toad, Nimbaphrynoides occidentalis. During more than 40 years of research, the Nimba toad’s reproductive morphology, endocrine activity of the ovary as well as the pituitary gland, and to some extent the ecological impact (seasonality, humidity, food availability) on reproduction was examined. Due to the Nimba toad’s unique reproductive mode, summaries are usually included in reviews discussing amphibian reproduction and articles on reproductive biology often discuss the exceptional reproductive system of Nimba toads. However, to our knowledge a detailed synthesis, summarising all the different original studies on the toad’s reproduction, is so far missing. In this paper we review and summarise all available initial publications, which often have been published in French and/or are difficult to access. A short overview is given of the climatic and environmental conditions experienced by Nimba toads and the key findings supporting a “true” viviparous reproduction with matrotrophy (maternal provision of nutrition during the gestation) and pueriparity (birth of juveniles). Then foetal development (morphological, gonad and pituitary development), and the female (ovary, oviduct, pituitary and their endocrine interactions) and the male reproductive system (testes and pituitary) are reviewed. Finally, the reproductive cycle and its link to the Nimba mountains’ seasonality and ecological/ conservation implications are discussed.

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          Most cited references 62

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          Early origin of viviparity and multiple reversions to oviparity in squamate reptiles.

          Viviparity has putatively evolved 115 times in squamates (lizards and snakes), out of only ~ 140 origins in vertebrates, and is apparently related to colder climates and other factors such as body size. Viviparity apparently evolves from oviparity via egg-retention, and such taxa may thus still have the machinery to produce thick-shelled eggs. Parity mode is also associated with variable diversification rates in some groups. We reconstruct ancestral parity modes accounting for state-dependent diversification in a large-scale phylogenetic analysis, and find strong support for an early origin of viviparity at the base of Squamata, and a complex pattern of subsequent transitions. Viviparous lineages have higher rates of speciation and extinction, and greater species turnover through time. Viviparity is associated with lower environmental and body temperatures in lizards and amphisbaenians, but not female mass. These results suggest that parity mode is a labile trait that shifts frequently in response to ecological conditions. © 2013 John Wiley & Sons Ltd/CNRS.
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            Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis.

            Phylogenetic analyses indicate that viviparity (live-bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid-Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co-opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition.
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              A New Hypothesis for the Evolution of Viviparity in Reptiles

               Richard Shine (1995)
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                Author and article information

                Journal
                Zoosystematics and Evolution
                ZSE
                Pensoft Publishers
                1860-0743
                1435-1935
                February 03 2017
                February 03 2017
                : 93
                : 1
                : 105-133
                Article
                10.3897/zse.93.10489
                © 2017

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