Skip to main content
SpringerLink
Log in

Modularity and developmental stability in segmented animals: variation in translational asymmetry in geophilomorph centipedes

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Does a modular body organization present a challenge for developmental control? We investigate the idea of a possible developmental cost of modularity by examining the relationship between modularity and developmental stability in a multi-segmented arthropod taxon: the geophilomorph centipedes. In a sample of eight species, we tested the correlation between developmental stability, estimated from measures of translational fluctuating asymmetry, and the number of trunk segments and some other morphological traits, both at the species and individual levels. We found sizeable differences in size and shape patterns of variation at the level of species. However, we did not find any clear evidence of correlation between fluctuating asymmetry and the number of trunk segments or the other morphological traits considered. Thus, our results provide no support to the idea of a possible trade-off between the cardinality of a modular system and the level of developmental precision in the phenotypic expression of its modules. The results of this exploratory study invite further investigations of patterns of translational fluctuating asymmetry in segmented animals and other modular organisms, as these have the potential to reveal features of developmental stability that cannot be captured by the study of bilateral asymmetry alone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aparicio JM (1998) Patterns of fluctuating asymmetry in developing primary feathers: a test of the compensational growth hypothesis. Proc R Soc B 265:2353–2357

    Article  PubMed Central  Google Scholar 

  • Astaurov BL (1930) Analyse der erblichen Störungsfälle der bilateralen Symmetrie. Z Indukt Abstamm Vererbungsl 55:183–262

    Google Scholar 

  • Berto D, Fusco G, Minelli A (1997) Segmental units and shape control in Chilopoda. Entomol Scand 51(Suppl):61–70

    Google Scholar 

  • Bonato L, Minelli A (2014) Chilopoda geophilomorpha of Europe: a revised list of species, with taxonomic and nomenclatorial notes. Zootaxa 3770:1–136

    Article  PubMed  Google Scholar 

  • Bonato L, Edgecombe GD, Zapparoli M (2011) Chilopoda—taxonomic overview. In: Minelli A (ed) Treatise on zoology—anatomy, taxonomy, biology, vol 1, The Myriapoda. Brill, Leiden, pp 363–443

    Google Scholar 

  • Bonato L, Drago L, Murienne J (2014) Phylogeny of Geophilomorpha (Chilopoda) inferred from new morphological and molecular evidence. Cladistics 30:485–507

    Article  Google Scholar 

  • Brena C (2014) The embryoid development of Strigamia maritima and its bearing on post-embryonic segmentation of geophilomorph centipedes. Front Zool 11:58

    Article  Google Scholar 

  • Brena C (2015) Myriapoda. In: Wanninger (ed) Evolutionary developmental biology of invertebrates, 3: Ecdysozoa I: non-Tetraconata. Springer Verlag, Berlin, pp 141–189

    Chapter  Google Scholar 

  • Clarke GM (1998) The genetic basis of developmental stability. IV. Individual and population asymmetry parameters. Heredity 80:553–561

    Article  Google Scholar 

  • Clune J, Mouret JB, Lipson H (2013) The evolutionary origins of modularity. Proc R Soc B 280:20122863

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org/

  • Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561

    Article  Google Scholar 

  • Debat V, Peronnet F (2013) Asymmetric flies: the control of developmental noise in Drosophila. Fly 7:70–77

    Article  PubMed  PubMed Central  Google Scholar 

  • Debat V, Bloyer S, Faradji F, Gidaszewski N, Navarro N, Orozco-terWengel P, Ribeiro V, Schlötterer C, Deutsch JS, Peronnet F (2011) Developmental stability: a major role for Cyclin G in Drosophila melanogaster. PLoS Genet 7, e1002314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Latte L, Bortolin F, Rota-Stabelli O, Fusco G, Bonato L (2015) Molecular-based estimate of species number, phylogenetic relationships and divergence times for the genus Stenotaenia (Chilopoda, Geophilomorpha) in the Italian region. Zookeys 510:31–47

    Article  PubMed  Google Scholar 

  • Félix MA, Barkoulas M (2015) Pervasive robustness in biological systems. Nat Rev Genet 16:483–496

    Article  PubMed  Google Scholar 

  • Freeman DC, Graham JH, Emlen JM (1993) Developmental stability in plants: symmetries, stress and epigenesis. Genetica 89:97–119

    Article  Google Scholar 

  • Fusco G (2005) Trunk segment numbers and sequential segmentation in myriapods. Evol Dev 7:608–617

    Article  PubMed  Google Scholar 

  • Fusco G, Minelli A (2000a) Developmental stability in geophilomorph centipedes. Fragm Faun 43(Suppl):73–82

    Google Scholar 

  • Fusco G, Minelli A (2000b) Measuring morphological complexity of segmented animals: centipedes as model systems. J Evol Biol 13:38–46

    Article  Google Scholar 

  • Fusco G, Minelli A (2010) Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc B 365:547–556

    Article  Google Scholar 

  • Fusco G, Minelli A (2013) Arthropod body segments and tagmata. In: Minelli A, Boxshall G, Fusco G (eds) Arthropod biology and evolution, Molecules, development, morphology. Springer Verlag, Berlin, pp 197–221

    Chapter  Google Scholar 

  • Fusco G, Brena C, Minelli A (2000) Cellular processes in the growth of lithobiomorph centipedes (Chilopoda: Lithobiomorpha). A cuticular view. Zool Anz 239:91–102

    Google Scholar 

  • Fusco G, Leśniewska M, Congiu L, Bertorelle G (2015) Population genetic structure of a centipede species with high levels of developmental instability. PLoS ONE 10, e0126245

    Article  PubMed  PubMed Central  Google Scholar 

  • Graham JH, Raz S, Hel-Or H, Nevo E (2010) Fluctuating asymmetry: methods, theory, and applications. Symmetry 2:466–540

    Article  Google Scholar 

  • Horneland EO, Meidell B (2009) Postembryonic development of Strigamia maritima (Leach, 1817) (Chilopoda: Geophilomorpha: Linotaeniidae) with emphasis on how to separate the different stadia. Soil Organ 81:373–386

    Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kent JT, Mardia KV (2001) Shape, procrustes tangent projections and bilateral symmetry. Biometrika 88:469–485

    Article  Google Scholar 

  • Klaus AV, Schawaroch V (2006) Novel methodology utilizing confocal laser scanning microscopy for systematic analysis in arthropods (Insecta). Integr Comp Biol 46:207–214

    Article  PubMed  Google Scholar 

  • Klingenberg CP (2003) A developmental perspective on developmental instability: theory, models and mechanisms. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 14–34

    Google Scholar 

  • Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934

    Article  Google Scholar 

  • Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52:1363–1375

    Article  Google Scholar 

  • Klingenberg CP, Nijhout HF (1998) Competition among growing organs and developmental control of morphological asymmetry. Proc R Soc Lond B 265:1135–1139

    Article  Google Scholar 

  • Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920

    Article  PubMed  Google Scholar 

  • Leamy L (1984) Morphometric studies in inbred and hybrid house mice. V. Directional and fluctuating asymmetry. Am Nat 123:579–593

    Article  Google Scholar 

  • Leamy L (1993) Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica 89:139–153

    Article  Google Scholar 

  • Leśniewska M, Bonato L, Minelli A, Fusco G (2009) Trunk anomalies in the centipede Stigmatogaster subterranea provide insight into late-embryonic segmentation. Arthropod Struct Dev 38:417–426

    Article  PubMed  Google Scholar 

  • Mardia KV, Bookstein FL, Moreton IJ (2000) Statistical assessment of bilateral symmetry of shapes. Biometrika 87:285–300

    Article  Google Scholar 

  • Minelli A, Fusco G (2004) Evo-devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429

    Article  PubMed  Google Scholar 

  • Minelli A, Fusco G (2013) Homology. In: Kampourakis K (ed) The philosophy of biology: a companion for educators. Springer Verlag, Berlin Heidelberg, pp 289–322

    Chapter  Google Scholar 

  • Moretto M, Minelli A, Fusco G (2015) Cell size versus body size in geophilomorph centipedes. Sci Nat 102:16

    Article  Google Scholar 

  • Murienne J, Edgecombe GD, Giribet G (2010) Including secondary structure, fossils and molecular dating in the centipede tree of life. Mol Phylogenet Evol 57:301–313

    Article  PubMed  Google Scholar 

  • Nijhout HF, Davidowitz G (2003) Developmental perspectives on phenotypic variation, canalization, and fluctuating asymmetry. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 3–13

    Google Scholar 

  • Orme D, Freckelton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2013) Caper: comparative analyses of phylogenetics and evolution in R. Available at: http://CRAN.R-project.org/package=caper

  • Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421

    Article  Google Scholar 

  • Palmer AR, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 279–319

    Google Scholar 

  • Piscart C, Moreteau J-C, Beisel J-N (2005) Decrease of fluctuating asymmetry among larval instars in an aquatic, holometabolous insect. C R Biol 328:912–917

    Article  PubMed  Google Scholar 

  • Polak M (ed) (2003) Developmental instability: causes and consequences. Oxford University Press, New York

    Google Scholar 

  • Raz S, Schwartz NP, Mienis HK, Nevo E, Graham JH (2012) Fluctuating helical asymmetry and morphology of snails (Gastropoda) in divergent microhabitats at ‘Evolution Canyons I and II’, Israel. PLoS ONE 7, e41840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohlf FJ (2015) The TPS series of software. Hystrix 26:9–12

    Google Scholar 

  • Savriama Y, Klingenberg CP (2011) Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry. BMC Evol Biol 11:280

    Article  PubMed  PubMed Central  Google Scholar 

  • Savriama Y, Gómez JM, Perfectti F, Klingenberg CP (2012) Geometric morphometrics of corolla shape: dissecting components of symmetric and asymmetric variation in Erysimum mediohispanicum (Brassicaceae). New Phytol 196:945–954

    Article  PubMed  Google Scholar 

  • Savriama Y, Stige LC, Gerber S, Pérez T, Alibert P, David B (2015) Impact of sewage pollution on two species of sea urchins in the Mediterranean Sea (Cortiou, France): radial asymmetry as a bioindicator of stress. Ecol Indic 54:39–47

    Article  CAS  Google Scholar 

  • Schlosser G, Wagner GP (eds) (2004) Modularity in development and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Swaddle JP, Witter MS (1997) On the ontogeny of developmental stability in a stabilized trait. Proc R Soc Lond B 264:329–334

    Article  Google Scholar 

  • Turcato A, Fusco G, Minelli A (1995) The sternal pore areas of geophilomorph centipedes (Chilopoda: Geophilomorpha). Zool J Linn Soc 115:185–209

    Article  Google Scholar 

  • Whitlock M (1996) The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc R Soc B 263:849–853

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Lucio Bonato for help with sample choice and for fruitful discussions, Małgorzata Leśniewska for kindly providing S. souletina and S. subterranea specimens and Fig. 1, Diego Maruzzo for the assistance with CLSM, Enrico L. Rezende for precious advice on the pgls analysis, and two anonymous referees for their insightful comments on a previous version of the article. This work has been supported by a grant (CPDA115439/11) from the Italian Ministry of Education, University and Research (MIUR) to GF.

Author information

Author notes

    Authors and Affiliations

    1. Institute of Biotechnology, University of Helsinki, Helsinki, Finland

      Yoland Savriama

    2. Department of Biology, University of Padova, Via U. Bassi 58/B, I-35131, Padova, Italy

      Marco Vitulo & Giuseppe Fusco

    3. Department of Earth Sciences, University of Cambridge, Cambridge, UK

      Sylvain Gerber

    4. Institut de Systématique, Évolution, Biodiversité – UMR 7205 – CNRS, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, Paris, France

      Sylvain Gerber & Vincent Debat

    Authors
    1. Yoland Savriama
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Marco Vitulo
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Sylvain Gerber
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Vincent Debat
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Giuseppe Fusco
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Giuseppe Fusco.

    Additional information

    Communicated by Nico Posnien and Nikola-Michael Prpic

    This article is part of the Special Issue “Size and Shape: Integration of morphometrics, mathematical modelling, developmental and evolutionary biology”, Guest Editors: Nico Posnien—Nikola-Michael Prpic

    Vincent Debat and Giuseppe Fusco contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Savriama, Y., Vitulo, M., Gerber, S. et al. Modularity and developmental stability in segmented animals: variation in translational asymmetry in geophilomorph centipedes. Dev Genes Evol 226, 187–196 (2016). https://doi.org/10.1007/s00427-016-0538-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00427-016-0538-3

    Keywords

    Search

    Navigation