Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles.

Stefano Tiozzo,Fabien Lombard,Casey W Dunn,Rebecca R Helm,Martin K S Lilley

doi:10.1186/s13227-015-0005-7

Abstract

BackgroundSimple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? To address this question, we examined the development in several species of pelagiid jellyfish. Most members of Pelagiidae have a complex life cycle with a sessile polyp that gives rise to ephyrae (juvenile medusae); but one species within Pelagiidae, Pelagia noctiluca, spends its whole life in the water column, developing from a larva directly into an ephyra. In many complex life cycles, adult features develop from cell populations that remain quiescent in larvae, and this is known as life cycle compartmentalization and may facilitate the evolution of direct life cycles. A second type of metamorphic processes, known as remodeling, occurs when adult features are formed through modification of already differentiated larval structures. We examined muscle morphology to determine which of these alternatives may be present in Pelagiidae.ResultsWe first examined the structure and development of polyp and ephyra musculature in Chrysaora quinquecirrha, a close relative of P. noctiluca with a complex life cycle. Using phallotoxin staining and confocal microscopy, we verified that polyps have four to six cord muscles that persist in strobilae and discovered that cord muscles is physically separated from ephyra muscle. When cord muscle is removed from ephyra segments, normal ephyra muscle still develops. This suggests that polyp cord muscle is not necessary for ephyra muscle formation. We also found no evidence of polyp-like muscle in P. noctiluca. In both species, we discovered that ephyra muscle arises de novo in a similar manner, regardless of the life cycle.ConclusionsThe separate origins of polyp and ephyra muscle in C. quinquecirrha and the absence of polyp-like muscle in P. noctiluca suggest that polyp muscle is not remodeled to form ephyra muscle in Pelagiidae. Life cycle stages in Scyphozoa may instead be compartmentalized. Because polyp muscle is not directly remodeled, this may have facilitated the loss of the polyp stage in the evolution of P. noctiluca.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0005-7) contains supplementary material, which is available to authorized users.

Highlights

Simple life cycles arise from complex life cycles when one or more developmental stages are lost
We examined polyp muscle morphology in C. quinquecirrha, to determine if polyp muscle is remodeled during strobilation and tested whether polyp muscle is necessary for ephyra muscle formation through experimental isolation of developing ephyra structures
In C. quinquecirrha, we examined the oral ectoderm of developing ephyrae at multiple stages and found no evidence that cord muscle contributes to ephyra muscle formation

Summary

Introduction

Simple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? The ciliated larva of P. noctiluca transforms into a single small ephyra (Figure 1B), bypassing a benthic stage. This species spends its entire life in the water column. As the only species within Pelagiidae to have a simple life cycle (Figure 1C), P. noctiluca provides a unique opportunity to study the evolutionary simplification of a life cycle and its developmental implications

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