Abstract
Developmental stability (DS) and canalization are key determinants of phenotypic variation. To provide a better understanding of how postnatal growth is involved in determining the effects of DS and canalization on phenotypic variation, we studied within- and among-individual variation in head shape in ontogenetic series of lizards inhabiting urban and rural environments. Urban lizards exhibited increased fluctuating asymmetry during the early postnatal stages, but asymmetry levels decreased during growth. By contrast, asymmetry remained constant across the investigated size range in the rural population. In addition, urban juveniles were more variable for symmetric shape and deviated more from the group shape-size allometric trajectory, but both indices declined across ontogeny. Congruent patterns of within- and among-individual variation suggest that both DS and canalization may rely on similar underlying mechanisms. Further, the ontogenetic reduction of variation in the urban population suggests that compensatory growth may aid in buffering phenotypic variation and correcting deviances from the established developmental path. Alternatively, passive mechanisms and population dynamics may also explain the decrease of phenodeviants in urban populations. Significant correlations between symmetric and asymmetric shape, as well as similar integration patterns between the two populations, suggest that similar developmental mechanisms regulate head shape in both environments. Overall, these results highlight the relevance of both pre- and post-natal dynamics in determining levels of phenotypic variation, enhancing our understanding of how organisms respond to perturbations to DS and canalization under stressful conditions.
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Adams, D. C., & Otarola-Castillo, E. (2013). geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399.
Adams, D. C., Otarola-Castillo, E., & Sherratt, E. (2014). geomorph: Software for geometric morphometric analyses. R package version 2.0. http://cran.r-project.org/web/packages/geomorph/index.html.
Aparicio, J. (1998). Patterns of fluctuating asymmetry in developing primary feathers: A test of the compensational growth hypothesis. Proceedings of the Royal Society of London B: Biological Sciences, 265, 2353–2357.
Barišić-Klisarić, N., Miljković, D., Avramov, S., Živković, U., & Tarasjev, A. (2014). Fluctuating asymmetry in Robinia pseudoacacia leaves—Possible in situ biomarker? Environmental Science Pollution Research, 21, 1298–12940.
Beasley, D. A. E., Bonisoli-Alquati, A., & Mousseau, T. A. (2013). The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecological Indicators, 30, 218–226.
Bellairs, A., & Kamal, A. M. (1981). The chondrocranium and the development of the skull in recent reptiles. In C. Gans & T. S. Parsons (Eds.), Biology of the reptilia. Vol. 11. Morphology F (pp. 1–263). London: Academic Press.
Bergman, A., & Siegal, M. L. (2003). Evolutionary capacitance as a general feature of complex gene networks. Nature, 424, 549–552.
Bookstein, F. L. (1997). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.
Chippindale, A. K., & Palmer, A. R. (1993). Persistence of subtle departures from symmetry over multiple molts in individual brachyuran crabs: relevance to developmental stability. Genetica, 89, 185–199.
Costantini, D., Lapresa Alonso, M., Moazen, M., & Bruner, E. (2009). The relationship between cephalic scales and bones in lizards: A preliminary microtomographic survey on three lacertid species. Anatomical Record, 293, 183–194.
Crnobrnja-Isailović, J., Aleksić, I., & Bejaković, D. (2005). Fluctuating asymmetry in Podarcis muralis populations from Southern Montenegro: Detection of environmental stress in insular populations. Amphibia-Reptilia, 26, 149–158.
Debat, V., Alibert, P., David, P., Paradis, E., & Auffray, J. C. (2000). Independence between developmental stability and canalization in the skull of the house mouse. Proceedings of the Royal Society of London B: Biological Sciences, 267, 423–430.
Debat, V., & David, P. (2001). Mapping phenotypes: Canalization, plasticity and developmental stability. Trends in Ecology & Evolution, 16, 555–561.
Emlen, J. M., Freeman, D. C., & Graham, J. H. (1993). Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica, 89, 77–96.
Ferreira, D. S. (2015). Genetic and morphological impacts of a repeated fire regime on Podarcis guadarramae. Master thesis, University of Porto.
Fischer-Rousseau, L., Cloutier, R., & Zelditch, M. L. (2009). Morphological integration and developmental progress during fish ontogeny in two contrasting habitats. Evolution and Development, 11, 740–753.
Galán, P. (1999). Demography and population dynamics of the lacertid lizard Podarcis bocagei in north-west Spain. Journal of Zoology, 249, 203–218.
García-Muñoz, E., & Sillero, N. (2010). Two new types of noose for capturing herps. Acta Herpetologica, 5, 259–263.
Gonzalez, P. N., Hallgrímsson, B., & Oyhenart, E. E. (2011a). Developmental plasticity in covariance structure of the skull: Effects of prenatal stress. Journal of Anatomy, 218, 243–257.
Gonzalez, P. N., Lotto, F. P., & Hallgrímsson, B. (2014). Canalization and developmental instability of the fetal skull in a mouse model of maternal nutritional stress. American Journal of Physical Anthropology, 154, 544–553.
Gonzalez, P. N., Oyhenart, E. E., & Hallgrímsson, B. (2011b). Effects of environmental perturbations during postnatal development on the phenotypic integration of the skull. Journal of Experimental Zoology B, 316, 547–561.
Goswami, A., Polly, P. D., Mock, O. B., & Sánchez-VIllagra, M. R. (2012). Shape, variance and integration during craniogenesis: Contrasting marsupial and placental mammals. Journal of Evolutionary Biology, 25, 862–872.
Gvoždík, L., & Damme, R. (2003). Evolutionary maintenance of sexual dimorphism in head size in the lizard Zootoca vivipara: A test of two hypotheses. Journal of Zoology, 259, 7–13.
Hallgrímsson, B. (1993). Fluctuating asymmetry in Macaca fascicularis: A study of the etiology of developmental noise. International Journal of Primatology, 14, 421–444.
Hallgrímsson, B. (1998). Fluctuating asymmetry in the mammalian skeleton: Evolutionary and developmental implications. Evolutionary Biology, 30, 187–251.
Hallgrímsson, B. (1999). Ontogenetic patterning of skeletal fluctuating asymmetry in rhesus macaques and humans: Evolutionary and developmental implications. International Journal of Primatology, 20, 121–151.
Hallgrímsson, B., & Hall, B. K. (Eds.). (2005). Variation: A central concept in biology. London: Academic Press.
Hallgrímsson, B., Miyake, T., Wilmore, K., & Hall, B. K. (2003). Embryological origins of developmental stability: Size, shape and fluctuating asymmetry in prenatal random bred mice. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 296, 40–57.
Herrel, A., Aerts, P., Fret, J., & De Vree, F. (1999). Morphology of the feeding system in agamid lizards: Ecological correlates. Anatomical Record, 254, 496–507.
Herrel, A., de Grauw, E., & Lemos-Espinal, J. A. (2001). Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology, 290, 101–107.
Hoffmann, A. A., & Hercus, M. J. (2000). Environmental stress as an evolutionary force. BioScience, 50, 217–226.
Husak, J. F., Lappin, A. K., Fox, S. F., & Lemos-Espinal, J. A. (2006). Bite-force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus). Copeia, 2006, 301–306.
Ivanović, A., & Kalezić, M. L. (2009). Evoluciona morfologija - teorijske postavke i geometrijska morfometrija. Beograd: Biološki fakultet. Univerzitet u Beogradu.
Ivanović, A., & Kalezlć, M. L. (2005). Facultative paedomorphosis and developmental stability in European newts (Triturus spp, Salamandridae): Ontogenetic aspect. Italian Journal of Zoology, 72, 265–270.
Kaliontzopoulou, A. (2011). Geometric morphometrics in herpetology: Modern tools for enhancing the study of morphological variation. Basic and Applied Herpetology, 25, 5–32.
Kaliontzopoulou, A., Adams, D. C., van der Meijden, A., Perera, A., & Carretero, M. A. (2012a). Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards. Evolutionary Ecology, 26, 825–845.
Kaliontzopoulou, A., Carretero, M. A., & Llorente, G. A. (2012b). Morphology of the Podarcis wall lizards (Squamata: Lacertidae) from the Iberian Peninsula and North Africa: Patterns of variation in a putative cryptic species complex. Zoological Journal of the Linnean Society, 164, 173–193.
Kellner, J. R., & Alford, R. A. (2003). The ontogeny of fluctuating asymmetry. American Naturalist, 161, 931–947.
Klingenberg, C. P. (2002). Morphometrics and the role of the phenotype in studies of the evolution of developmental mechanisms. Gene, 287, 3–10.
Klingenberg, C. P. (2003). Developmental instability as a research tool: Using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. In M. Polak (Ed.), Developmental instability: Causes and consequences (pp. 427–442). Oxford: Oxford University Press.
Klingenberg, C. P. (2004). Integration, modules, and development: Molecules to morphology to evolution. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 213–230). Oxford: Oxford University Press.
Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology Evolution and Systematics, 39, 115–132.
Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635.
Klingenberg, C. P. (2015). Analyzing fluctuating asymmetry with geometric morphometrics: Concepts, methods, and applications. Symmetry, 7, 843–934.
Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., & Beckwith, N. J. (2001). Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings. American Naturalist, 157, 11–23.
Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56, 1909–1920.
Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52, 1363–1375.
Klingenberg, C. P., & Nijhout, H. F. (1999). Genetics of fluctuating asymmetry: A developmental model of developmental instability. Evolution, 53, 358–375.
Lande, R. (1977). On comparing coefficients of variation. Systematic Zoology, 26, 214–217.
Lazić, M. M. (2015). Fluctuating asymmetry as an indicator of environmental stress in populations of the common wall lizard (Podarcis muralis Laurenti 1768) in urban and rural environments. Ph.D. thesis, University of Belgrade.
Lazić, M. M., Carretero, M. A., Crnobrnja-Isailović, J., & Kaliontzopoulou, A. (2015). Effects of environmental disturbance on phenotypic variation: An integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. American Naturalist, 185, 44–58.
Lazić, M. M., Kaliontzopoulou, A., Carretero, M. A., & Crnobrnja-Isailović, J. (2013). Lizards from urban areas are more asymmetric: Using fluctuating asymmetry to evaluate environmental disturbance. PLoS ONE, 8, e84190.
Leamy, L. (1993). Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica, 89, 139–153.
Leamy, L. J., Klingenberg, C. P., Sherratt, E., Wolf, J. B., & Cheverud, J. M. (2015). The genetic architecture of fluctuating asymmetry of mandible size and shape in a population of mice: Another look. Symmetry, 7, 146–163.
Manly, B. F. J. (1991). Randomization and Monte Carlo methods in biology. London: Chapman & Hall.
Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.
Mardia, K. V., Bookstein, F. L., & Moreton, I. J. (2000). Statistical assessment of bilateral symmetry of shapes. Biometrika, 87, 285–300.
Martín, J., & López, P. (2001). Hindlimb asymmetry reduces escape performance in the lizard Psammodromus algirus. Physiological and Biochemical Zoology, 74, 619–624.
Møller, A. P., & Van Dongen, S. (2003). Ontogeny of asymmetry and compensational growth in elm Ulmus glabra leaves under different environmental conditions. International Journal of Plant Sciences, 164, 519–526.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. (2013). vegan: Community ecology package. R package. Version 2.0-9. http://CRAN.R-project.org/packagepvegan. Accessed 2 Feb 2015.
Palmer, A. R. (1999). Detecting publication bias in meta-analyses: A case study of fluctuating asymmetry and sexual selection. American Naturalist, 154, 220–233.
Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review in Ecology and Systematics, 17, 391–421.
Palmer, A. R., & Strobeck, C. (2003). Fluctuating asymmetry analyses revisited. In M. Polak (Ed.), Developmental instability: Causes and consequences (pp. 279–319). Oxford: Oxford University Press.
Parsons, P. A. (1990). Fluctuating asymmetry: An epigenetic measure of stress. Biological Reviews, 65, 131–145.
Parsons, P. A. (1992). Fluctuating asymmetry: A biological monitor of environmental and genomic stress. Heredity, 68, 361–364.
Parsons, P. A. (1997). Extreme environmental change and evolution. Cambridge: Cambridge University Press.
Parsons, K. J., Skúlason, S., & Ferguson, M. (2010). Morphological variation over ontogeny and environments in resource polymorphic arctic charr (Salvelinus alpinus). Evolution and Development, 12, 246–257.
Pavlicev, M., Cheverud, J. M., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.
Pélabon, C., Hansen, T. F., Carlson, M. L., & Armbruster, W. S. (2006). Patterns of asymmetry in the twining vine Dalechampia scandens (Euphorbiaceae): Ontogenetic and hierarchical perspectives. New Phytologist, 170, 65–74.
Piscart, C., Moreteau, J. C., & Beisel, J. N. (2005). Decrease of fluctuating asymmetry among larval instars in an aquatic, holometabolous insect. Comptes Rendus Biologies, 328, 912–917.
Rohlf, F. J. (2005). tpsDig, digitize landmarks and outlines. Version 2.04. Department of Ecology and Evolution, State University of New York at Stony Brook.
Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.
RStudio. (2012). RStudio: Integrated development environment for R. Version 3.0.1. http://www.rstudio.org/.
Scharloo, W. (1991). Canalization: Genetic and developmental aspects. Annual Review of Ecology and Systematics, 22, 65–93.
Schulte, U. (2008). Die Mauereidechse. Bielefeld: Laurenti-Verlag.
Servia, M. J., Cobo, F., & González, M. A. (2002). Ontogeny of individual asymmetries in several traits of larval Chironomus riparius Meigen, 1804 (Diptera, Chironomidae). Canadian Journal of Zoology, 80, 1470–1479.
Soulé, M. E. (1982). Allomeric variation 1: The theory and some consequences. American Naturalist, 120, 751–764.
Stige, L. C., Hessen, D. O., & VØLlestad, L. A. (2006). Fitness, developmental instability, and the ontogeny of fluctuating asymmetry in Daphnia magna. Biological Journal of the Linnean Society, 88, 179–192.
Swaddle, J. P., & Witter, M. S. (1997). On the ontogeny of developmental stability in a stabilized trait. Proceedings of the Royal Society of London B: Biological Sciences, 264, 329–334.
Urošević, A., Ljubisavljević, K., & Ivanović, A. (2015). Fluctuating asymmetry and individual variation in the skull shape of the common wall lizard (Podarcis muralis Laurenti, 1768) estimated by geometric morphometrics. The Herpetological Journal, 25, 177–186.
Van Dongen, S. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: Past, present and future. Journal of Evolutionary Biology, 19, 1727–1743.
Van Valen, L. M. (1962). A study of fluctuating asymmetry. Evolution, 16, 125–142.
Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature, 150, 563–565.
Waddington, C. H. (1952). Canalization of the development of a quantitative character. In C. H. Waddington (Ed.), Quantitative inheritance (pp. 43–46). London: Her Majesty’s Stationery Office.
Wagner, G. P. (1990). A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Journal of Zoological Systematics and Evolutionary Research, 28, 48–61.
Warner, A., & Shine, R. (2006). Morphological variation does not influence locomotor performance within a cohort of hatchling lizards (Amphibolurus muricatus, Agamidae). Oikos, 114, 126–134.
Willmore, K. E., Leamy, L., & Hallgrímsson, B. (2006). Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution and Development, 8, 550–567.
Young, N. M. (2006). Function, ontogeny and canalization of shape variance in the primate scapula. Journal of Anatomy, 209, 623–636.
Zakharov, V. M. (1992). Population phenogenetics: Analysis of developmental stability in natural populations. Acta Zoologica Fennica, 191, 7–30.
Zelditch, M. L., Bookstein, F. L., & Lundrigan, B. L. (1992). Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution, 46, 1164–1180.
Zelditch, M. L., Bookstein, F. L., & Lundrigan, B. L. (1993). The ontogenetic complexity of developmental constraints. Journal of Evolutionary Biology, 6, 621–641.
Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution and Development, 6, 194–206.
Acknowledgments
We are grateful to two anonymous reviewers for insightful comments on an early version of the manuscript. M.M.L. and J.C.I. were supported by Grant No. 173025, funded by the Ministry of Education, Science and Technological Development of Republic of Serbia (http://www.mpn.gov.rs/). A.K. was supported by an IF contract (IF/00641/2014/CP1256/CT0008) by Fundação para a Ciência e Tecnologia (FCT, Portugal). M.A.C. and A.K. were partially supported by project “Biodiversity, Ecology and Global Change” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2—O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF). Lizards were collected and handled with permits of the Ministry of Environment and Spatial Planning of Republic of Serbia No.: 353-01-312/2014-08.
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Lazić, M.M., Carretero, M.A., Crnobrnja-Isailović, J. et al. Postnatal Dynamics of Developmental Stability and Canalization of Lizard Head Shape Under Different Environmental Conditions. Evol Biol 43, 368–379 (2016). https://doi.org/10.1007/s11692-016-9377-4
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DOI: https://doi.org/10.1007/s11692-016-9377-4