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Calcitic Sclerites at Base of Malacostracan Pleopods (Crustacea) – Part of a Coxa Verena Kutschera*, Andreas Maas†, Gerd Mayer† and Dieter Waloszek†

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Calcitic Sclerites at Base of Malacostracan Pleopods (Crustacea) – Part of a Coxa Verena Kutschera*, Andreas Maas†, Gerd Mayer† and Dieter Waloszek† Kutschera et al. BMC Evolutionary Biology (2015) 15:117 DOI 10.1186/s12862-015-0357-6 RESEARCH ARTICLE Open Access Calcitic sclerites at base of malacostracan pleopods (Crustacea) – part of a coxa Verena Kutschera*, Andreas Maas†, Gerd Mayer† and Dieter Waloszek† Abstract Background: Cuticular specialisations such as joints and membranes play an important role in the function of arthropod limbs. This includes sclerotisations and mineral incrustations of cuticular areas to achieve either more rigidity or flexibility. The anterior eight thoracopods of Malacostraca have limb stems comprising a coxa and a basipod, which carries the two rami. Their pleopods, the limbs of the posterior trunk part, have for long been regarded to lack a coxa. Several calcitic sclerites occur in the area between ventral body and limb stem. This raises the questions: do these elements represent specialisations of the membrane due to functional requirements, and do they originate from an originally larger limb portion, i.e., the coxa, or in fact represent it. Results: We investigated 16 species of selected malacostracan taxa from all major in-groups. Calcitic sclerites occur in constant numbers and position within a species (no individual variation, and independent of specific modification such as in genital appendages). These are even constant within a supra-specific taxon, which facilitates comparisons. In general the sclerites connect via two pivot joints to the sternite medially and the tergopleura laterally, and two more to the limb stem. Based on this, we reconstructed putative ground-pattern conditions for the sclerites of the examined taxa of Malacostraca. Conclusions: The pattern of sclerites is characteristic for each monophyletic malacostracan taxon. The highest number of sclerites most likely represents the plesiomorphic state. Reduction of sclerite numbers occurs in Caridoida and its in-groups. Sclerite arrangement in these taxa provides an important character complex for phylogenetic studies. The presence of pivot joints to the body proximally and basipod distally demonstrates the existence of a coxa, which is just slightly less sclerotised, particularly on its posterior side. This can be explained by enhanced flexibility of the pleopods evolved in the course to their major role as swimming devices. Both the pivot joints and the proximal and distal extension of the calcitic sclerites demarcate the minimum area of the coxa. With this, sclerites appear as very valuable also in shedding more light on the putative relationships between Malacostraca, Myriapoda, Insecta, and Remipedia. Keywords: Proximal endite, Coxa, Basipod, Pleon, Alizarin Red, Fluorescence microscopy Background membrane. These reinforcements occur in the form of The membranous cuticle in the joint or articulation be- sclerites within the membrane [1]. Another option is that tween body proper and appendage of sclerotised arthropods more sclerotised cuticular elements approach each other by is an important structure that intermediates between rigid- the formation of simple to very complex joints [7]. ity and flexibility in order to facilitate the operability of an A well-developed basal membrane did not appear before appendage. Numerous variations occur among modern ar- the euarthropod level in connection with the development thropods ([1] and references therein for Chilopoda, Progo- of a rigid, antero-posteriorly flattened stem portion, the neata, and Hexapoda; [2] for Trilobita; [3] for Chelicerata, basipod, which carried the two rami endopod and exopod and crustaceans in particular [4-6]). One possibility to mod- [8,9]. This design permitted a more elaborate ex- and in- ify the design of arthropod joints is to stiffen parts of the trinsic musculature to extend from inside the body and inserting into the limb stem. Initially, the limb stem mainly * Correspondence: [email protected] moved in anterior and posterior direction. With the newly † Equal contributors formed basal membrane, interactions could now take place Biosystematic Documentation, University of Ulm, Helmholtzstraße 20, 89081 Ulm, Germany between the body and the stiffer limb stem, allowing © 2015 Kutschera et al. 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. Kutschera et al. BMC Evolutionary Biology (2015) 15:117 Page 2 of 27 inward-outward and rotating movements. Such a "eu- demanded for more data to be collected, compared and arthropodium" was a multi-functional unit, with the limb interpreted. Therefore, it seemed of high relevance for us to stem medially armed with setae and spines to serve for food study the details of the pleon morphology with particular manipulation, and endopod and exopod serving more for regard to the basal joint and its structures associated with food gathering (grabbing things) and locomotion (walking it. We started to particularly search for structures that as much as swimming) ([9], see [10] for an extensive dis- mighthintattheoriginalsituationatthebaseofthepleo- cussion of the evolution of crustacean appendages). pods of malacostracans. Our goal was to find hints for the With few changes, this limb type was continued into the original presence of either the "proximal endite", or a "coxa". euarthropodan in-group lineages including Crustacea. This We examined what appears to be the exclusively membran- allowed the evolution as one of the crustacean novelties, a ous area extending between the ventral body surface and setae-bearing endite, the proximal endite, which occurred the comprehensive pleopod limb stem ("the pleopod-body medially just below the limb stem [11-16]. articulation") in a wide array of malacostracan taxa with In the stem species of Labrophora, the taxon that in- Alizarin-Red staining (which highlights calcified areas) and cludes Phosphatocopina and Eucrustacea, the proximal fluorescence microscopy (Figures 1, 2, 3, 4 and 5; Table 1). endite of the anterior two postantennular appendages We detected several small, calcified areas (termed "sclerites" became modified into a distinct ring-like sclerotised herein) within the pleopod-body articulation (Figures 2, 3 proximal unit, the coxa [6,9,11,17-19]. and 4; Table 1). Considering up to eight individuals for each In entomostracan crustaceans, the occurrence of a coxa is species and similar patterns in closely related species indi- restricted to exactly those appendages, the antenna and cate that the patterns presented here are real and not arte- mandible. The maxillula, the still trunk-limb shaped maxilla, facts produced either by fixation methods, or by the time lag and the trunk limbs retain the proximal endite. Malacos- to the next moult. We also used normal light and scanning traca in this context are characterised by calcification of the electron microscopy to check the proximal limb area for its cuticle, which apparently was a major trigger for the devel- structural composition. Besides discussion of the possible opment of different life strategies within the diverse lineages. role of the sclerites in the functionality of the articulations, In all malacostracans, the eight appendages of the anterior we will also evaluate their potential for phylogenetic con- part of the two-part thorax (thoracopods 1–8ofthoraxI siderations (Figure 6; Table 2 and Table 3) and provide a [20]) have a divided limb stem, comprising a coxa and basi- suggestion about the morphology of the pleopods. pod [4,5]. However, it is still unclear if the coxa of these limbsisderivedfromaproximalenditeorisevolvedina Results different way. By contrast, the six appendages of the second Details revealed on the ventral side of a pleomere and its part of the limb-bearing trunk region of Malacostraca body–limb articulations include the shape of tergo- (thorax II [20]), the so-called pleopods or swimmerets are pleurae, sternites, and insertion of limbs, as well as the traditionally thought to have an undivided limb stem number, shape, and position of the sclerites within the [21-24]. In fact, details of the limb stem are even omitted in arthrodial membranes. In all species we examined, the the descriptive literature. With regard to the common oc- morphology is generally similar for the first to fifth currence of a coxa for all postantennular head limbs and pleomeres (4 in Nebalia bipes (Fabricius, 1780) and those of thorax I of Malacostraca, one might expect an ori- Nebaliopsis sp.) (Figure 1). Therefore, we describe the ginal coxa also on the pleopods, but which is absent, maybe situation in a general way for each species, applicable to it has been lost. Other scenarios are also possible. For ex- pleomeres 1–5(1–4) (see below, Table 1). Additionally, we ample,acoxaoriginallybepresentonthepleopodsmight indicate sexual dimorphism occurring in some of these have fused to the limb stem [15,25-27]; or perhaps it was species, including the sternites, and also record excep- originally absent [8], which would reflect the phylogenetic- tions we uncovered from what one can read in general- ally older situation of the euarthropod condition of a limb ised descriptions. comprising only three limb parts, i.e., even lacking the prox- imal endite developed
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