Developmental Diversity of Amphibians Richard P
Total Page：16
File Type：pdf, Size：1020Kb
Advanced Review Developmental diversity of amphibians Richard P. Elinson1∗ and Eugenia M. del Pino2 The current model amphibian, Xenopus laevis, develops rapidly in water to a tadpole which metamorphoses into a frog. Many amphibians deviate from the X. laevis developmental pattern. Among other adaptations, their embryos develop in foam nests on land or in pouches on their mother’s back or on a leaf guarded by a parent. The diversity of developmental patterns includes multinucleated oogenesis, lack of RNA localization, huge non-pigmented eggs, and asynchronous, irregular early cleavages. Variations in patterns of gastrulation highlight the modularity of this critical developmental period. Many species have eliminated the larva or tadpole and directly develop to the adult. The wealth of developmental diversity among amphibians coupled with the wealth of mechanistic information from X. laevis permit comparisons that provide deeper insights into developmental processes. © 2011 Wiley Periodicals, Inc. How to cite this article: WIREs Dev Biol 2012, 1:345–369. doi: 10.1002/wdev.23 INTRODUCTION Even among this group of model amphibians, there are fundamental differences in development. Fer- mphibians have long been model organisms for tilization in most anurans, the frogs, is monospermic developmental biology. While Xenopus laevis is A as in mammals, but fertilization in most urode- presently the amphibian model, others had previously 7,8 enjoyed the spotlight.1–3 Various salamanders were les, the newts and salamanders, is polyspermic. used in classic studies by Spemann, Vogt, Harrison, Primordial germ cells form via the germ plasm, a Fankhauser, Holtfreter, and others.4 Pleurodeles cytoplasmic localization in anurans, but via induction 9–12 waltl, the Spanish ribbed newt, was popular in in urodeles. The body form changes completely French laboratories, as was Cynops pyrrhogaster, and abruptly at metamorphosis in anurans, but the the fire bellied newt, in Japanese laboratories. The body form undergoes minimal, gradual changes in Mexican axolotl, Ambystoma mexicanum,emerged urodeles.13 Finally urodeles possess remarkable regen- as the urodele of choice, since it could be easily bred eration abilities, not found in anurans.14 and maintained in laboratory colonies. This permitted We expect to find more variation in embryos of identification of a few mutant genes, largely through amphibians than in embryos of eutherian mammals the pioneering efforts of Humphrey.5,6 Presently, the for two reasons. First, amphibians have had a long axolotl is the urodele targeted for genomic analysis phylogenetic history. Even representatives of model (http://www.ambystoma.org).6 Among frogs, several systems diverged from each other hundreds of mil- species of Rana were exploited by Pasteels, Ancel lions of years ago. Second, all of the amphibians used & Vintemberger, the Barths, and Briggs and King as models are similar in that early development takes among many. Xenopus laevis arose through its use in place in water. There are a large number of amphibian pregnancy testing, and it was established as a model 2 species whose embryos develop either on land or in for development by Nieuwkoop and Fischberg. the body of the adult.15,16 In the evolution of these species, the embryos had to adapt to new environ- ∗Correspondence to: [email protected] ments, quite different from pond water. In contrast, 1Department of Biological Sciences, Duquesne University, Pittsburgh, PA, USA development of eutherian mammals occurs in the con- 2Escuela de Ciencias Biologicas,´ Pontificia Universidad Catolica´ del served environment of the amnion within the uterus. Ecuador, Quito, Ecuador We will review aspects of reproduction and embryonic Volume 1, May/June 2012 © 2011 Wiley Periodicals, Inc. 345 Advanced Review wires.wiley.com/devbio development in amphibians that develop in a variety transitions in a caecilian and a snake implies that evo- of environments. lution of the elongated body plan involved alternative interpretations of the Hox code. With respect to limb- lessness, correlations have been made with changes PHYLOGENY in caecilian Hox gene and cluster structure,22,23 but There are three amphibian orders, the anurans, the causal connections have not emerged. urodeles, and the legless caecilians, which are part of There are several feeding strategies among cae- the monophyletic Lissamphibians. While the urodeles cilian larvae.24 Feeding by suction occurs in larvae of and anurans are considered to be more closely oviparous caecilians in aquatic habitats, and scrap- related to each other than either is to caecilians, ing of the uterine epithelium is the mode of prenatal the last common ancestors were in the Permian, feeding in viviparous species. Juveniles of two direct 300–250 million years ago (MYA).17 By comparison, developing oviparous species feed on the skin of their the last common ancestor of mouse and human lived mothers.25,26 Feeding switches to prey capture by bit- about 100 MYA (http://timetree.org). ing in adult caecilians. The various feeding modes Within anurans, commonly used frogs of of oviparous and viviparous caecilians are in turn the genera Gastrotheca, Eleutherodactylus, Bufo, correlated with differences in jaw development.24 Fur- and Rana are part of the monophyletic clade ther investigations of caecilian early development will Neobatrachia.18 Species of Gastrotheca, Eleuthero- undoubtedly reveal more unexpected characters. dactylus,andBufo shared common ancestors about 55 MYA, and the last common ancestor between this group and Rana was present 160 MYA. Xenopus, DEVELOPMENTAL ADAPTATIONS which belongs to a different clade, shared a common IN URODELES ancestor with the Neobatrachia about 230 MYA. Development of aquatic larvae and metamorphosis The long evolutionary times between amphibian to terrestrial adults is typical of urodeles in the gen- clades is coupled with the diversity of environments era Triturus, Taricha, Notophthalmus, Pleurodeles, for development of amphibian embryos. These two Cynops, and Ambystoma. This reproductive mode is features require us to examine amphibians other than not predominant however among urodeles, as 68% of the model ones in order to understand alternative all urodele species are lungless salamanders of the fam- developmental paths. ily Plethodontidae and have direct development.13,27 DEVELOPMENTAL ADAPTATIONS Aquatic Development in Urodeles IN CAECILIANS and Paedomorphosis Caecilians include 188 species (http://amphibiaweb. In contrast to caecilians, urodeles are classical organ- org, 2011), distributed in tropical regions of the isms for developmental investigations. In fact, research world.15 These elongate and limbless amphibians have on early amphibian embryos was concentrated on secluded life habits, a feature that limits study of their urodele species with a shift toward anurans, partic- embryos, and consequently embryonic development ularly X. laevis, only in the last half century.28 Eggs is little known in this group.19 Their reproductive of urodeles are larger than those of X. laevis,and modes include oviparity with free-living larvae, direct the embryos develop slower, features which facilitate development, and viviparity. Developmental tables for experimental manipulations such as grafting. Anyone a few caecilians are available.19,20 studying neural development in X. laevis would look The independent origin of the elongated, limb- enviously at the prominent neural folds in a urodele less body plan in caecilians and reptiles provides embryo. opportunities to examine the developmental evolution The most widely used urodele, A. mexicanum, of this morphology. Woltering et al.21 recently used exhibits the unusual life history of paedomorphosis, in embryos of the caecilian Icthyophis to compare their which the aquatic larval form persists, and the axolotl elongated morphology to that of snakes. Of the 126 becomes reproductive without metamorphosing. The vertebrae, 120 are rib-bearing thoracic types. Within failure to metamorphose is a derived condition of the somites that give rise to these thoracic vertebrae insufficient thyroid hormone; addition of thyroid however, there are transitions in Hox gene expression hormone causes transformation to the terrestrial which in other animals are associated with transitions adult.29–31 Natural populations of some Ambystomid in vertebral type. The contrast between the pres- species exhibit facultative paedomorphosis, and the ence of Hox transitions and the absence of vertebral frequency of paedomorphosis versus metamorphosis 346 © 2011 Wiley Periodicals, Inc. Volume 1, May/June 2012 WIREs Developmental Biology Developmental diversity of amphibians is influenced by environmental factors.32,33 It is possi- modes.15 The most familiar reproductive mode ble to cross paedomorphic and metamorphic species. includes the aquatic larval tadpole, which eats and These crosses indicate that metamorphosis is domi- grows until it metamorphoses into a terrestrial adult nant to paedomorphosis and that there are several frog. Not all tadpoles live in water, however. Some genetic bases for paedomorphosis.34 Given the plas- begin development on land in foam nests; others are ticity in the genus, it is of interest that metamorphosis carried by a parent or incubated in the parent’s body. was apparently more frequent in the original axolotls, Some do not feed and live off the yolk in the egg. brought to Europe in the nineteenth century.35 This In the extreme cases, tadpoles have been deleted from