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The Embryoid Development of Strigamia Maritima and Its Bearing on Post-Embryonic Segmentation of Geophilomorph Centipedes Carlo Brena

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The Embryoid Development of Strigamia Maritima and Its Bearing on Post-Embryonic Segmentation of Geophilomorph Centipedes Carlo Brena Brena Frontiers in Zoology 2014, 11:58 http://www.frontiersinzoology.com/content/11/1/58 RESEARCH Open Access The embryoid development of Strigamia maritima and its bearing on post-embryonic segmentation of geophilomorph centipedes Carlo Brena Abstract Background: Many arthropods add body segments post-embryonically, including most of the myriapods. However, geophilomorph and scolopendromorph centipedes are epimorphic, i.e. they form all their segments during embryonic time, although this has never been demonstrated directly. Understanding the similarity between embryonic and post-embryonic segmentation is pivotal to understand the possible evolution from anamorphosis to epimorphosis. We have previously demonstrated that in the geophilomorph centipede Strigamia maritima most segments are produced by an oscillatory mechanism operating through waves of expression at double segment periodicity, but that the last-forming (posteriormost) segments are patterned with a different system which might be more similar to post-embryonic segmentation. Results: With a careful analysis of a large number of specimens, I show that the first (“embryoid”) phase of post-embryonic development is clearly distinct from the following ones. It is characterized by more moults than previously reported, allowing me to define and name new stages. I describe these embryoid stages and the first free-leaving stage in detail, providing data on their duration and useful identification characters. At hatching, the prospective last leg-bearing segment is limbless and the genital segments are added in the following stages, indicating a residual anamorphosis in Strigamia segmentation. I demonstrate directly for the first time that at least the leg-bearing segments are in general produced during embryonic life, although in some individuals the external delineation of the last leg-bearing segment may be delayed to post-embryonic time, a possible further residual of anamorphic development. Additionally, I show that the development of the poison claws during this post-embryonic phase may have some element of recapitulation. Conclusions: The data presented in this paper show that the embryoid phase of post-embryonic development of geophilomorph centipedes may represent an extension of embryonic development, possibly in correlation with the evolution of epimorphic development from an anamorphic ancestor, accomplished without completely losing post-embryonic segmentation activity. This continuity in the segmentation process across the embryonic/ postembryonic divide may concur to the evolvability of this developmental process. Keywords: Myriapods, Chilopod, Staging, Post-embryonic, Epimorphosis, Anamorphosis, Arthropod evolution, Forcipule, Recapitulation Correspondence: [email protected] Laboratory for Development and Evolution, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK © 2014 Brena; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Brena Frontiers in Zoology 2014, 11:58 Page 2 of 16 http://www.frontiersinzoology.com/content/11/1/58 Introduction change in the molecular process. Here single segmental Metamerism is a key morphological character of arthro- molecular patterning appears periodically at the anter- pods. To understand its evolution, it is fundamental to ior margin of the still active growth zone, where condi- understand how this reiteration of modules along the an- tions are definitely more static and patterning of the teroposterior (AP) axis is laid down during development. localized undifferentiated tissue appears to be associ- In the great majority of arthropods with a high number of ated more with cell proliferation [4]. These conditions segments, these are mostly formed post-embryonically, might be more similar to the ones which characterise differentiating from a mass of posterior undifferentiated postembryonic segmentation. tissue, with the process not being visible externally from In fact, the embryonic/post-embryonic divide is a prob- the morphology of the exoskeleton. On the contrary, the lematic issue per se. Indeed, it is clear that at hatching, a first segments of those arthropods - and all segments in geophilomorph centipede is little more than an embryo arthropods like the insects - are laid down embryonically without an egg shell, still brooded by the mother for an through a molecular patterning process that can precede additional long period. In this animal, the rupture of the any morphological differentiation. This process extends to egg chorion does not represent a clear-cut change from an several segments (sequentially segmenting arthropods) or embryonic to a post-embryonic state [5,6]. These non- even to all segments (long germ arthropods like Drosoph- feeding post-embryonic stages reside with the mother, ila). It is not clear whether this embryonic process is in who stays coiled around them in the brood chamber, a continuity with the post-embryonic phase of segmenta- small cavity in the soil matrix. All these brood stages have tion, and if so to what extent, although understanding this been termed ‘larval stages’ by several authors [7-9] (in par- would be pivotal to understanding the evolutionary transi- ticular Lewis in his review book [10]) to distinguish them tion from anamorphosis to epimorphosis. from the later juvenile instars (‘post-larval stages,’ in Lewis’ Geophilomorph centipedes are the only arthropods with terms). (In this paper I will use the term ‘juvenile’ as a gen- a high and, in most cases, intraspecifically variable number eric term to indicate all post-embryonic immature stages). of segments (up to 191 leg-bearing segments, LBS) known The use of the term ‘larva’ to describe these brooded to form all of their segments embryonically [1] (but see stages is highly debatable, and I agree with Minelli and below). Geophilomorphs are epimorphic as are their sister Fusco [11] in suggesting that we should be cautious using group, the scolopendromorphs, although the latter have this word. I refer to them for a comparative discussion on an intraspecifically-invariant and smaller number of seg- this topic throughout the arthropods. Consequently, I will ments (21–23 LBS) (with two exceptions [2,3]). This is in call these early post-embryonic stages (proembryoid I to contrast with the other centipedes, or Chilopoda (Crateros- III, peripatoid, foetus; see below) ‘embryoid’,aterm tigmomorpha, Lithobiomorpha and Scutigeromorpha) and already used for similar instars in several arthropods all other myriapods (Symphyla, Pauropoda and Diplopoda, (see e.g. [11]), because of their similarity with actual em- or millipedes) all of which have anamorphic development, bryos. Post-embryoid stages start with the first free- with some, or, in the case of the majority of millipedes, living and feeding stage, the adolescens I, which leaves most of the segments formed post-embryonically. The epi- the mother some time after the moult and has most of morphic nature of development has been always considered the adult characters. a well defined trait of Geophilomorpha and Scolopendro- Besides earlier accounts [12-15], the first proper descrip- morpha and has been recognised as a major apomorphy, tion of these embryoid stages was provided by Verhoeff to the extent that their clade is called Epimorpha. Under- [16], describing two stages: a peripatoid and a foetus, and standing how this character has evolved and fixed repre- those terms have been used in subsequent studies on dif- sents a major step towards understanding the evolution of ferent species (e.g. [7-9,17,18]). As far as development is the clade. concerned, Strigamia maritima is by far the best described I have been studying Strigamia maritima as a represen- geophilomorph species. Yet, while we have a reasonably tative of the geophilomorph centipedes. In these centi- good description of the postembryoid stages and their tim- pedes the many segments laid down along the whole germ ing [18-20], previous attempts to describe in part [20] or band are fully available for molecular and developmental specifically [21] these early post-embryonic stages have analysis as a whole. Recent studies [4] have confirmed that somehow failed to recognise the number and timing of the great majority of these segments are originally pro- moults precisely, leading to some confusion and inconsist- duced as morphogenetic units by a sort of segmentation ency in recognising, describing, or naming the stages, an clock, through a cycling activity of segmentation genes op- issue which is common to the whole of Geophilomorpha. erating by waves of expression acting at a double segment To try to better understand and define it, I carried out a periodicity. In contrast, the last part of the segmentation detailed analysis of this phase of post-embryonic develop- process, although in continuity with the main one and in- ment, based on the improved techniques of culturing eggs volving most of the same genes, is associated with a and juveniles in mineral oil [22]. This analysis follows up Brena Frontiers in Zoology 2014, 11:58 Page 3 of 16 http://www.frontiersinzoology.com/content/11/1/58
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