Abstract

BackgroundComparative analyses between amphibians, concentrating on the cellular mechanisms of morphogenesis, reveal a large variability in the early developmental processes that were thought to be conserved during evolution. Increased egg size is one factor that could have a strong effect on early developmental processes such as cleavage pattern and gastrulation. Salamanders of the family Plethodontidae are particularly appropriate for such comparative studies because the species have eggs of varying size, including very large yolky eggs.ResultsIn this paper, we describe for the first time the early development (from fertilization through neurulation) of the plethodontid salamander Ensatina eschscholtzii. This species has one of the largest eggs known for an amphibian, with a mean ± SD diameter of 6 ± 0.43 mm (range 5.3-6.9; n = 17 eggs). Cleavage is meroblastic until approximately the 16-cell stage (fourth or fifth cleavage). At the beginning of gastrulation, the blastocoel roof is one cell thick, and the dorsal lip of the blastopore forms below the equator of the embryo. The ventral lip of the blastopore forms closer to the vegetal pole, and relatively little involution occurs during gastrulation. Cell migration is visible through the transparent blastocoel roof of the gastrula. At the end of gastrulation, a small archenteron spreading dorsally from the blastopore represents the relatively small and superficial area of the egg where early embryonic axis formation occurs. The resulting pattern is similar to the embryonic disk described for one species of anuran.ConclusionsComparisons with the early development of other species of amphibians suggest that an evolutionary increase in egg size can result in predictable changes in the patterns and rate of early development, but mainly within an evolutionary lineage.

Highlights

  • Comparative analyses between amphibians, concentrating on the cellular mechanisms of morphogenesis, reveal a large variability in the early developmental processes that were thought to be conserved during evolution

  • Gravid E. eschscholtzii were collected in various California locations in the springs of 1986 to 1989, and oviposition was induced by intraperitoneal injections of 0.1 ml of luteinizing hormone releasing hormone

  • Because the eggs deposited by non-injected females developed in the same way as those deposited by injected females and because eggs deposited by injected females hatched into apparently normal juveniles, we concluded that the development observed after luteinizing hormone releasing hormone (LHRH)-induced oviposition is normal

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Summary

Introduction

Comparative analyses between amphibians, concentrating on the cellular mechanisms of morphogenesis, reveal a large variability in the early developmental processes that were thought to be conserved during evolution. Salamanders of the family Plethodontidae are appropriate for such comparative studies because the species have eggs of varying size, including very large yolky eggs. The objective of this study was to investigate how egg size and yolk content affects the mechanisms of morphogenesis in early amphibian development, with an analysis of cleavage, gastrulation and neurulation in a caudate amphibian with a large yolky egg, Ensatina eschscholtzii. Studies on the hylid frog, Gastrotheca riobambae, have indicated significant differences in early development from that of Xenopus, such as meroblastic and asynchronous early cleavages, an uncoupling of events of the midblastula transition, and blastopore closure before archenteron and notochord elongation [8,9,10]. All amphibian eggs eventually have holoblastic cleavage (the egg is totally divided by the first and all the following cleavage planes), but in some species ( those with large yolky eggs) the first few cleavage planes fail to pass completely through the egg [11,12,13,14,15]

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