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Development and Evolution of Segmentation Assessed by Geometric Morphometrics: the Centipede Strigamia Maritima As a Case Study

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Development and Evolution of Segmentation Assessed by Geometric Morphometrics: the Centipede Strigamia Maritima As a Case Study Arthropod Structure & Development 46 (2017) 419e428 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd Development and evolution of segmentation assessed by geometric morphometrics: The centipede Strigamia maritima as a case study * Yoland Savriama a, Sylvain Gerber b, Matteo Baiocco c, Vincent Debat b, Giuseppe Fusco c, a Institute of Biotechnology, University of Helsinki, Helsinki, Finland b Institut de Systematique, Evolution, Biodiversite ISYEB e UMR 7205 e MNHN CNRS UPMC EPHE, Museum national d'Histoire naturelle, Sorbonne Universites, 57 rue Cuvier, CP 50, 75005 Paris, France c Department of Biology, University of Padova, Via U. Bassi 58/B, I-35131 Padova, Italy article info abstract Article history: Using the centipede model species Strigamia maritima as a subject of study, we illustrate the potential of Received 31 January 2017 geometric morphometrics for investigating the development and evolution of segmentation, with a Accepted 11 March 2017 specific focus on post-embryonic segmental patterning. We show how these techniques can contribute Available online 22 March 2017 detailed descriptive data for comparative purposes, but also precious information on some features of the developmental system that are considered relevant for the evolvability of a segmented body architecture, Keywords: such as developmental stability and canalization. Morphometric analyses allow to separately investigate Arthropods several sources of phenotypic variation along a segmented body axis, like constitutive and random Canalization fi Developmental stability segment heteronomy, both within and among individuals. Speci cally, in S. maritima, the segmental fl Evolvability pattern of ventral sclerite shapes mirrors that of their bilateral uctuating asymmetry and among- Fluctuating asymmetry individual variation in associating the most anterior and most posterior segments in diverging from Segmental patterning the central ones. Also, among segments, there seems to be a correlation between fluctuating asymmetry and shape variation among individuals, suggesting that canalization and developmental stability are somehow associated. Overall, these associations might stem from a joint influence of the segmental position on the two processes of developmental buffering. © 2017 Elsevier Ltd. All rights reserved. 1. Introduction done using techniques like in-situ hybridization to study gene expression, parental and embryonic RNA interference to study gene Segmentation is a key feature of arthropod body architecture, function, and sequencing of transcriptomes and genomes to reveal and as such considerable attention has been paid to its develop- the complete gene repertoires of some of these animals (Leite and ment and evolution, also in relation to tagmosis, the morpho- McGregor, 2016). However, despite remarkable recent progresses in functional regionalization of the main body axis (reviewed in developmental biology, especially in comparative developmental Fusco and Minelli, 2013). genetics, the study of post-embryonic development still remains The evolution of segmentation as a body feature, in connection insufficiently investigated, if compared to the preceding phase of to the developmental process of segmentation itself, is a favourite ontogeny. This is particularly unfortunate for arthropods, where subject of evolutionary developmental biology (evo-devo), as it is developmental processes of segmentation and tagmosis are not thought that the developmental mechanism of segmentation, along restricted to embryogenesis, but continue prominently through with the network of genetic interactions that controls it, can have post-embryonic life (Minelli and Fusco, 2013). significant influence on the evolution of segmentation as a Comparative analysis of the evolution of segmentation, including morphological trait (e.g., Davis and Patel, 1999; Peel et al., 2005; segmental patterning, needs other types of data, typically morpho- Vroomans et al., 2016). However, most of the more recent studies metric data,and different analytical approaches, such as those offered on the development of segmentation have focused on the embry- by geometric morphometric (GM) methods, a suite of analytical tools onic (often, early-embryonic) phase of development. This has been that provide a statistical description of biological forms in terms of their size and geometric shape (e.g., Klingenberg, 2010). Morphological variation along a segmental series (segment * Corresponding author. E-mail address: [email protected] (G. Fusco). heteronomy) within an individual has at least two different http://dx.doi.org/10.1016/j.asd.2017.03.002 1467-8039/© 2017 Elsevier Ltd. All rights reserved. 420 Y. Savriama et al. / Arthropod Structure & Development 46 (2017) 419e428 components. The first is constitutive segmental variation in size and Conversely, if these patterns are different, then canalization and shape of the elements of the series, corresponding to the more stability might involve different processes. The literature has so far general concept of target phenotype, i.e. the phenotype specified by provided contrasting results (see Debat et al., 2009; Klingenberg, the genetic makeup of the organism and the environmental con- 2015 for reviews). In this context, an obviously appealing feature ditions during its development (Nijhout and Davidowitz, 2003; of segmented animals, is that they offer as many traits as their Fusco and Minelli, 2010). The second is random segmental varia- number of segments to assess this relationship, with the additional tion, i.e. variation around the target phenotype produced by question of whether it might differ across segments, and be influ- developmental noise, that can be manifested as deviations from the enced by the overall heteronomy. expected body symmetry, or fluctuating asymmetry (see below) Here, we illustrate the potential of geometric morphometrics for (Fusco and Minelli, 2000a; Savriama et al., 2016). Both constitutive investigating development and evolution of segmental patterning, and random segmental variation, metaphorically the “signal” and using the model centipede species Strigamia maritima as the sub- the “noise”, are of high interest for both developmental studies, ject of study. In particular, we present some general morphometric across ontogenetic stages within species, and evolutionary studies, approaches for the study of size and shape segment differentiation comparing species in a phylogenetic context. (constitutive heteronomy) and bilateral and translational FA. We At the same time, phenotypic variation observed in a population focus in particular on the patterns of bilateral shape asymmetry of is the outcome of two opposing sets of influences: on the one hand segments (as a proxy for developmental stability) and shape vari- are the sources of variation, including genetic and environmental ation among individuals (as a proxy for canalization), and explore differences among individuals and developmental noise; on the whether they might differ regarding the position of segments along other hand is a set of developmental processes that buffer those the main body axis. variations, including canalization and developmental stability (e.g., In the last two decades, together with the pill millipede Glomeris Debat and David, 2001; see below). Because developmental noise is marginata, the centipede S. maritima (Fig. 1A) has become a difficult to set apart from environmental effects, a strategy is to favourite subject of myriapod developmental biology, with a series focus on within-individual variation among repeated body parts. of studies on its embryonic (Chipman et al., 2004; Brena and Akam, These parts are indeed genetically identical and are usually facing 2012) and early-postembryonic (Brena, 2014) development, and the same environmental conditions, and thus differ only by sto- developmental gene expression (Brena et al., 2006; Chipman and chastic differences attributable to developmental noise (e.g., Van Akam, 2008; Brena and Akam, 2013; Brena, 2015). S. maritima is Valen, 1962). also the only myriapod with a fully sequenced genome (Chipman Within-individual deviations from the expected body symmetry et al., 2014). As typical of geophilomorph centipedes (Chilopoda, are known as fluctuating asymmetry (FA) (e.g., Debat and David, Geophilomorpha), S. maritima presents a highly polymerous and a 2001; Debat and Peronnet, 2013; Klingenberg, 2015). In organisms rather homonomous (i.e., morphologically little-differentiated) with bilateral symmetry, random deviations from left-right sym- segmental body organization, with respect to other arthropods. metry, or bilateral FA (Palmer and Strobeck, 1986), are often Nonetheless, as we will show, detailed quantitative morphometric employed to investigate developmental stability, i.e. the ability of an analyses, that can be equally applied to more complex segmental organism to buffer random perturbations of its developmental patterns, reveal a surprising richness in segmental patterning, in process (Nijhout and Davidowitz, 2003; Fusco and Minelli, 2010). the relationship between different aspects of developmental con- However, for segmented animals, or for organisms with a modular trol at the level of segments, and in the connections between body organization in general, other types of body symmetry, specific segmental patterning and developmental control. of their body architecture, can be exploited to study developmental The quantitative
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