The embryoid development of Strigamia maritimaand its bearing on post-embryonic segmentation of geophilomorph centipedes

This is the final version. It was first published by BioMed Central at http://www.frontiersinzoology.com/content/11/1/58.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

Six3 demarcates the anterior-most developing brain region in bilaterian animals.

BACKGROUND: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the 'new phylogeny' placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla. RESULTS: We find that in the marine annelid Platynereis dumerilii, expression of the homeobox gene six3 defines the apical region of the larval body, peripherally overlapping the equatorial otx+ expression. The six3+ and otx+ regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm Pristina, as well as in the onychophoran Euperipatoides, the centipede Strigamia and the insects Tribolium and Drosophila, a six3/optix+ region likewise demarcates the tip of the developing animal, followed by a more posterior otx/otd+ region. Identification of six3+ head neuroectoderm in Drosophila reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids. In insects, onychophorans and Platynereis, the otx+ region instead harbours the eye anlagen, which thus occupy a more posterior position. CONCLUSIONS: These observations indicate that the annelid, onychophoran and arthropod head develops from a conserved anterior-posterior sequence of six3+ and otx+ regions. The six3+ anterior pole of the arthropod head and brain accordingly lies in an anterior-median embryonic region and, in consequence, the optic lobes do not represent the tip of the neuraxis. These results support the hypothesis that the last common ancestor of annelids and arthropods already possessed neurosecretory centres in the most anterior region of the brain. In light of its broad evolutionary conservation in protostomes and, as previously shown, in deuterostomes, the six3-otx head patterning system may be universal to bilaterian animals.RIGHTS : This article is licensed under the BioMed Central licence at http://www.biomedcentral.com/about/license which is similar to the 'Creative Commons Attribution Licence'. In brief you may : copy, distribute, and display the work; make derivative works; or make commercial use of the work - under the following conditions: the original author must be given credit; for any reuse or distribution, it must be made clear to others what the license terms of this work are

The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history.This work was supported by the following grants: NHGRIU54HG003273 to R.A.G; EU Marie Curie ITN #215781 “Evonet” to M.A.; a Wellcome Trust Value in People (VIP) award to C.B. and Wellcome Trust graduate studentship WT089615MA to J.E.G; Marine rhythms of Life” of the University of Vienna, an FWF (http://www.fwf.ac.at/) START award (#AY0041321) and HFSP (http://www.hfsp.org/) research grant (#RGY0082/2010) to KT-­‐R; MFPL Vienna International PostDoctoral Program for Molecular Life Sciences (funded by Austrian Ministry of Science and Research and City of Vienna, Cultural Department -­‐Science and Research to T.K; Direct Grant (4053034) of the Chinese University of Hong Kong to J.H.L.H.; NHGRI HG004164 to G.M.; Danish Research Agency (FNU), Carlsberg Foundation, and Lundbeck Foundation to C.J.P.G.; U.S. National Institutes of Health R01AI55624 to J.H.W.; Royal Society University Research fellowship to F.M.J.; P.D.E. was supported by the BBSRC via the Babraham Institute;This is the final version of the article. It first appeared from PLOS via http://dx.doi.org/10.1371/journal.pbio.100200

From sea monsters to charismatic megafauna: changes in perception and use of large marine animals

Marine megafauna has always elicited contrasting feelings. In the past, large marine animals were often depicted as fantastic mythological creatures and dangerous monsters, while also arousing human curiosity. Marine megafauna has been a valuable resource to exploit, leading to the collapse of populations and local extinctions. In addition, some species have been perceived as competitors of fishers for marine resources and were often actively culled. Since the 1970s, there has been a change in the perception and use of megafauna. The growth of marine tourism, increasingly oriented towards the observation of wildlife, has driven a shift from extractive to non-extractive use, supporting the conservation of at least some species of marine megafauna. In this paper, we review and compare the changes in the perception and use of three megafaunal groups, cetaceans, elasmobranchs and groupers, with a special focus on European cultures. We highlight the main drivers and the timing of these changes, compare different taxonomic groups and species, and highlight the implications for management and conservation. One of the main drivers of the shift in perception, shared by all the three groups of megafauna, has been a general increase in curiosity towards wildlife, stimulated inter alia by documentaries (from the early 1970s onwards), and also promoted by easy access to scuba diving. At the same time, environmental campaigns have been developed to raise public awareness regarding marine wildlife, especially cetaceans, a process greatly facilitated by the rise of Internet and the World Wide Web. Currently, all the three groups (cetaceans, elasmobranchs and groupers) may represent valuable resources for ecotourism. Strikingly, the economic value of live specimens may exceed their value for human consumption. A further change in perception involving all the three groups is related to a growing understanding and appreciation of their key ecological role. The shift from extractive to non-extractive use has the potential for promoting species conservation and local economic growth. However, the change in use may not benefit the original stakeholders (e.g. fishers or whalers) and there may therefore be a case for providing compensation for disadvantaged stakeholders. Moreover, it is increasingly clear that even non-extractive use may have a negative impact on marine megafauna, therefore regulations are needed.SFRH/BPD/102494/2014, UID/MAR/04292/2019, IS1403info:eu-repo/semantics/publishedVersio

Ancestral patterning of tergite formation in a centipede suggests derived mode of trunk segmentation in trilobites.

Trilobites have a rich and abundant fossil record, but little is known about the intrinsic mechanisms that orchestrate their body organization. To date, there is disagreement regarding the correspondence, or lack thereof, of the segmental units that constitute the trilobite trunk and their associated exoskeletal elements. The phylogenetic position of trilobites within total-group Euarthropoda, however, allows inferences about the underlying organization in these extinct taxa to be made, as some of the fundamental genetic processes for constructing the trunk segments are remarkably conserved among living arthropods. One example is the expression of the segment polarity gene engrailed, which at embryonic and early postembryonic stages is expressed in extant panarthropods (i.e. tardigrades, onychophorans, euarthropods) as transverse stripes that define the posteriormost region of each trunk segment. Due to its conservative morphology and allegedly primitive trunk tagmosis, we have utilized the centipede Strigamia maritima to study the correspondence between the expression of engrailed during late embryonic to postembryonic stages, and the development of the dorsal exoskeletal plates (i.e. tergites). The results corroborate the close correlation between the formation of the tergite borders and the dorsal expression of engrailed, and suggest that this association represents a symplesiomorphy within Euarthropoda. This correspondence between the genetic and phenetic levels enables making accurate inferences about the dorsoventral expression domains of engrailed in the trunk of exceptionally preserved trilobites and their close relatives, and is suggestive of the widespread occurrence of a distinct type of genetic segmental mismatch in these extinct arthropods. The metameric organization of the digestive tract in trilobites provides further support to this new interpretation. The wider evolutionary implications of these findings suggest the presence of a derived morphogenetic patterning mechanism responsible for the reiterated occurrence of different types of trunk dorsoventral segmental mismatch in several phylogenetically distant, extinct and extant, arthropod groups

Cellular processes in the growth of lithobiomorph centipedes (Chilopoda: Lithobiomorpha). A cuticular view

The cuticle of lithobiomorph centipedes (Chilopoda, Lithobiomorpha) offers a special opportunity for studying cellular processes of morphogenesis during postembryonic growth. The present paper shows that in lithobiomorph centipedes the polygonal surface pattern of the cuticle can record the geometry of the external face of hypodermal cells at the stage of deposition of the very first layers of the cuticle (epicuticle). Based on this hypodermis-to-cuticle correspondence, cuticular patterns are used to study the hypodermal behaviour during growth of an area of the cephalic shield. Growth is isometric and intercalary and mitosis is the fundamental cellular process responsible for its realization, but adjustments of cell size and shape are also extensively involved in the global control of sclerite form. The observed spatial distribution of mitoses is evaluated against the statistics predicted by a null model of random distribution. The observed growth patterns show a character of local randomness, but some constraints at the level of the whole sclerite seem to be at work. No effect of lateral inhibition is observed

Major body components in stage 7–8 embryos of <i>Strigamia maritima.</i>

<p>Specimens photographed with fluorescent nuclear staining (Sytox Green) to show the morphology. <b>A.</b> Lateral view of whole-mount embryo corresponding to Fig. 4D, head on the upper left. The juxtaposed ventral surface (<i>arrow</i>) of the embryo is obscured and out of sight. <b>B.</b> Flat-mounted posterior region of embryo corresponding to Fig. 2C, anterior to the left. In both A and B dots indicate the approximate boundary between the prospective dorsal and lateral tissues as observed in the adult. Squares indicate the approximate boundary between the prospective lateral and ventral tissues as observed in the adult.</p

Schematic models of comparative dorsoventral expression of <i>engrailed</i> (blue), and correspondence with the tergite borders in extant arthropods.

<p>Anterior facing left. <b>A.</b> The expression of <i>engrailed</i> in the trunk segments of <i>Strigamia maritima</i> is reflective of the plesiomorphic condition of the arthropod trunk, consisting of a continuous dorsoventral stripe adjacent to the intersegmental boundary, and that extends into the limbs (<i>dotted line</i>). The posterior limit of the dorsal <i>engrailed</i> stripe is directly correlated with the posterior (meta)tergite (<i>mt</i>) border and the intersegmental boundary, and does not overlap with the anterior edge of the following (pro)tergite (<i>pt</i>). <b>B.</b> The expression of <i>engrailed</i> in the segments of the insect abdomen is similar to that observed in <i>Strigamia</i>, but differs in the absence of limbs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Rogers1" target="_blank">[41]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Campbell1" target="_blank">[47]</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Krzemien1" target="_blank">[50]</a>. <b>C.</b> In the haplosegments of <i>Glomeris marginata,</i> the dorsal <i>engrailed</i> stripe is not expressed adjacent to the ventral intersegmental boundary, but rather anteriorly, approximately above the limbs; nevertheless, the tergite borders maintain the correlation with the expression of <i>engrailed</i> observed in <i>Strigamia</i> (A) and insects (B). The ventral side shows the typical activity of <i>engrailed</i> in the posterior portion of each segment <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Janssen1" target="_blank">[43]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Janssen2" target="_blank">[51]</a>. Other abbreviations: <i>Tn</i>, trunk tergite number <i>n</i>; <i>An</i>, abdominal tergite number <i>n</i>. Numbering in C follows the nomenclature used by Janssen et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Janssen1" target="_blank">[43]</a>.</p

Reconstructions of the dorsoventral morphology of trilobites and trilobite-like arthropods.

<p>Anterior to the left. <b>A.</b> Exsagittal longitudinal section of the phacopid <i>Phacops</i> showing typical trilobite exoskeletal organization <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Hessler1" target="_blank">[20]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Whittington3" target="_blank">[27]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Bruton1" target="_blank">[32]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Bruton2" target="_blank">[33]</a>. The biomineralized tergites (<i>Tn</i>) overlay the lightly sclerotized series of sternites (<i>stn</i>) that are connected by flexible tendinous bars (<i>tnb</i>). Each sternite bears a pair of laterally attached gnathobasic (<i>gnb</i>) walking legs. The reconstruction of the dorsal (<i>dlm</i>) and ventral (<i>vlm</i>) longitudinal muscles follow the functional requirements for typical arthropod locomotion, and are shown attached to specific regions of the visceral exoskeleton such as the articulating furrow (<i>af</i>) and the apodemes (<i>apm</i>); note that although the apodemes actually are in direct contact with the visceral side of the tergite at the level of the articulating furrow (see Fig. 8f), such connection is not shown in here due to the schematic nature of this representation. The trilobite-like articulation consists of the anteriorly shifted position of the tergite borders relative to the sternite borders; consequently, a pair of cephalic legs (<i>Cln</i>) is located under the cephalo-thoracic articulation, and the thoracic legs (<i>Tln</i>) under each tergite-to-tergite junction. <b>B.</b> Longitudinal section of the nektaspidid <i>Misszhouia longicaudata</i> showing exoskeletal organization in an unmineralized trilobite-like arthropod <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0052623#pone.0052623-Edgecombe1" target="_blank">[13]</a>. The tergites of nektaspidids are fused into a thoracopygidial shield (<i>TS</i>), with a single articulation at the cephalo-thoracic junction; as diagnostic for the trilobite-like articulation, a pair of cephalic legs is positioned directly under this region. Aspects of the ventral morphology, such as the sternite series, tendinous bars and limb attachment sites, are very similar to those of trilobites; however, there is no clear indication for muscle attachment sites on the visceral side of the thoracopygidial shield. Other abbreviations: <i>OR</i>, occipital ring; <i>ahr</i>, articulating half ring; <i>dvm</i>, dorsoventral muscle; <i>CS</i>, cephalic shield.</p