ReviewThere's more than one frog in the pond: A survey of the Amphibia and their contributions to developmental biology
Introduction
The award of the 1935 Nobel Prize in Physiology or Medicine to Hans Spemann for his research on the Organizer marked the emergence of the amphibian as an important model system for the study of development. The fundamental significance of Spemann's findings galvanised the burgeoning field of experimental embryology. The continued relevance of his contributions is evident in practical laboratories across the world today, where Einsteck transplantation is as much a rite of passage for current students as was the dissection of frog leg muscles by their predecessors in Spemann's time.
For most biologists of the molecular era, amphibian embryology is synonymous with the study of the African Clawed Frog, Xenopus. This anuran has served as a treasure-trove for biologists to plunder in search of novel developmental regulators. The elucidation of the role of TGF-β proteins in mesoderm induction as well as the isolation of patterning genes such as noggin, chordin, goosecoid and cerberus attest to the success of this approach. At the time when Spemann was performing his seminal organizer experiments, however, Xenopus was still languishing in relative obscurity in South African swamps. In this review, I will examine the reasons underlying the rise of Xenopus as the predominant amphibian model, and I will pay homage to some of the other amphibian species, who along with their insightful experimenters, have made contributions to our understanding of development. I will consider cases where examination of different amphibian species has challenged prior models of development, and I will discuss some examples of amphibian developmental diversity. I shall begin by considering the roots of this diversity, with a summary of the nature and origins of the Amphibia.
Section snippets
Amphibian phylogeny
What is an amphibian? The name of this vertebrate class conveys the impression of an animal that has a dual existence, split between water and land. While many European and North-American species, including those most commonly used for experimentation, follow such a biphasic life-history, consisting of an aquatic larval phase followed by metamorphosis into a terrestrial adult, this is by no means true of all amphibians. Many species have become either completely aquatic or entirely terrestrial,
How Xenopus became the top frog in the pond
The rise of Xenopus as the dominant amphibian developmental model is a relatively recent phenomenon. The species is known as Xenopus laevis (Daudin) in honour of the French naturalist who discovered it in 1803 (reviewed in [10]). One of the early embryologists to study Xenopus was Boris Balinsky of the University of the Witwatersrand in South Africa, who utilised his local frog species. Elsewhere, the prevalence of Xenopus can be traced to its use in pregnancy testing. Xenopus hit the hallowed
Developmental contributions of other amphibians
Indubitably, the experimental advantages afforded by Xenopus have contributed greatly towards our understanding of development. However, it is important to note that reliance on one model can result in experimental limitations and can even distort our view of development. While many of the seminal discoveries made in Triturus, Rana and Ambystoma may reflect universal amphibian attributes; it was only through judicious use of available experimental species that the early amphibian embryologists
Comparative developmental biology of the Amphibia
Many of the examples in the previous section have demonstrated that while different amphibians have specific attributes that make them particularly good models for certain aspects of development, care must be chosen in extrapolating information from one species to another. In this section, I will consider amphibian ontogeny within an explicitly comparative context, focussing on the morphological differences between amphibians, and the developmental mechanisms responsible for the generation of
Future research
It has long been known that amphibians exhibit an amazing amount of reproductive diversity, and this is reflected in their varied ontogenies. More recently, the application of molecular techniques to non-model amphibians has allowed us to begin examining the molecular basis underlying these evolutionary innovations in development. Many of these recent comparative studies have correlated altered gene expression patterns with changes in embryogenesis. The next challenge is to acquire experimental
Acknowledgements
I thank Rick Elinson for suggestions, Jim Smith for support and Joana Ramis for bibliographic assistance. This work was supported by a Human Frontier Science Program Long Term Fellowship and by Wellcome Trust funding to Jim Smith. I am grateful to Steve Manning for inspiring me to become a biologist.
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2015, Developmental BiologyCitation Excerpt :Indeed, classical experiments on frog and salamander embryos profoundly influenced our current understanding of fundamental events in vertebrate development (Spemann and Mangold, 1924). In the twentieth century, the frog Xenopus laevis ascended as the amphibian of choice for modern embryologists, largely because of its responsiveness to year-round, hormone-induced ovulation in the laboratory (Callery, 2006). Xenopus explant assays transformed our conception of multi-potency and the cell behaviors that drive morphogenesis (Logan and Mohun, 1993; Saint-Jeannet et al., 1994; Sater and Jacobson, 1989; Wilson et al., 1989), while the capacity to microinject single blastomeres with molecular reagents continues to serve as a powerful system for tissue-specific analyses of gene function and the elucidation of regulatory networks (Amaya et al., 1991; Hopwood and Gurdon, 1990; Moody, 1987a; Moody, 1987b; Smith et al., 1993; Tandon et al., 2012; Woodland and Jones, 1987).