Asymmetry in the common wall lizard Podarcis muralis under different levels of urbanization: the effect of trait and FA index selection

Marko Mirč, Nataša Tomašević Kolarov, Srđan Stamenković, Tanja D. Vukov

Abstract


Paper description:

  • Fluctuating asymmetry (FA), as a measure of developmental instability induced by environmental stress, is widely used but with different methodological approaches that result in discordant conclusions.
  • We tested for the first time whether the choice of different fluctuating asymmetry indices and meristic traits affect the assessment of the developmental instability induced by urbanization in the common wall lizard, Podarcis muralis.
  • Different indices and traits can have dissimilar patterns, which can affect conclusions about developmental instability induced by environmental stress. Caution must be practiced when deciding what indices and traits are going to be used for FA analysis.


Abstract: The use of fluctuating asymmetry (FA) as a measure of developmental instability and its relationship to stress and fitness is highly controversial. We examined whether the selection of different FA indices and traits influences the results of FA analysis. We chose four meristic traits and three FA indices (two single-trait and two multiple-trait indices) to assess FA levels in the common wall lizard (Podarcis muralis) from three different habitat types (urban, suburban and natural). Urbanization has already been linked to developmental instability in P. muralis. We therefore expected to detect different FA levels among the habitats. However, we also wanted to see whether we obtained the same patterns using different indices and traits. Our results showed that different traits can yield different FA patterns between habitats. The only statistically significant difference between habitats was detected for the FA2 index in femoral pores. The highest level of FA was detected in the urban population, while the lowest level was in the natural population. It is clear that caution must be exerted when deciding on which traits and indices are to be used for FA analysis.

https://doi.org/10.2298/ABS190225033M

Received: February 25, 2019; Revised: May 22, 2019; Accepted: May 22, 2019; Published online: May 29, 2019

How to cite this article: Mirč M, Tomašević-Kolarov N, Stamenković S, Vukov TD. Asymmetry in the common wall lizard Podarcis muralis under different levels of urbanization: The effect of trait and FA index selection. Arch Biol Sci. 2019;71(3):501-8.


Keywords


developmental instability; stress; fluctuating asymmetry; Lacertidae; meristic traits

Full Text:

PDF

References


Willmore KE, Hallgrímsson B. Within individual variation: developmental noise versus developmental stability. In: Hallgrímsson, B Hall BK, editors. Variation: A Central Concept in Biology. Burlington, MA, USA: Elsevier; 2005. p. 191-218.

Graham, JH, Freeman DC, Emlen JM. Developmental stability: a sensitive indicator of populations under stress. In: Wayne LG., Hughes JS, Lewis MA, editors. Environmental toxicology and risk assessment. ASTM STP 1179. Philadelphia: American Society for testing and Material;1993.p. 136-58.

Lens L, Van Dongen S, Matthysen E. Fluctuating asymmetry as an early warning system in the critically endangered Taita thrush. Conserv Biol. 2002;16(2):479-87.

Dongen SV. Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evolution Biol. 2006;19(6):1727-43.

Thoday JM. Homeostasis in a selection experiment. Heredity. 1958;12(4):401.

Van Valen L. A study of fluctuating asymmetry. Evolution. 1962;16(2):125-42.

Waddington CH. Canalization of development and the inheritance of acquired characters. Nature. 1942;150(3811):563.

Klingenberg CP. A developmental perspective on developmental instability: Theory, models and mechanisms. In Polak M, editor, Developmental Instability: Causes and Consequences. 1 ed. Oxford University Press. 2003. p. 14-34.

Lazić MM, Kaliontzopoulou A, Carretero MA, Crnobrnja-Isailović J. Lizards from urban areas are more asymmetric: using fluctuating asymmetry to evaluate environmental disturbance. PloS One. 2013;8(12):e84190.

Lazić MM, Carretero MA, Crnobrnja-Isailović J, Kaliontzopoulou A. Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. Am Nat. 2014;185(1):44-58.

Sacchi R, Polo MF, Coladonato AJ, Mangiacotti M, Scali S, Zuffi MA. The exposition to urban habitat is not enough to cause developmental instability in the common wall lizards (Podarcismuralis). Ecol Indic. 2018;93:856-63.

Ljubisavljević K, Tome S, Džukić G, Kalezić ML. Morphological differentiation of an isolated population of the Italian wall lizard (Podarcissicula) of the southeastern Adriatic coast. Biologia. 2005;60:189-95.

Băncilǎ R, Van Gelder I, Rotteveel E, Loman J, Arntzen JW. Fluctuating asymmetry is a function of population isolation in island lizards. J Zool. 2010;282(4):266-75.

Crnobrnja-Isailović J, Aleksić I, Bejaković D. Fluctuating asymmetry in Podarcismuralis populations from Southern Montenegro: detection of environmental stress in insular populations. Amphibia-Reptilia. 2005;26(2):149-58.

Braña F, Ji X. Influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcismuralis). J Exp Zool. 2000;286(4):422-33.

Martín J, López P. Pre-mating mechanisms favoring or precluding speciation in a species complex: chemical recognition and sexual selection between types in the lizard Podarcishispanica. EvolEcol Res. 2006;8(4):643-58.

Vervust B, Lailvaux SP, Grbac I, Van Damme R. Do morphological condition indices predict locomotor performance in the lizard Podarcissicula?.ActaOecol. 2008;34(2):244-51.

López P, Martín J. Locomotor capacity and dominance in male lizards Lacerta monticola: a trade-off between survival and reproductive success?.Biol J Linn Soc. 2002;77(2):201-9.

Amaral MJ, Carretero MA, Bicho RC, Soares AM, Mann RM. The use of a lacertid lizard as a model for reptile ecotoxicology studies: Part 1 Field demographics and morphology. Chemosphere. 2012;87(7):757-64.

López P, Amo L, Martín J. Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol. 2006;32(2):473-88.

Martín J, López P. Links between males quality, males chemical signals, and female mate choise in Iberian Rock Lizards. Funct Ecol. 2006:20:1087-96.

Palmer AR, Strobeck C. CH 17. Fluctuating asymmetry analyses revisited. In: Polak M, editor. Developmental Instability: Causes and Consequences, Oxford: Oxford University Press. 2003. p. 279-319.

Valverde JA. Estructura de unacomunidadmediterránea de vertebradosterrestres. 1967.

Graziani F, Corti C, Dapporto L, Berti R. " Podarcis" Lizards in anaAgro-Environment in Tuscany (Central Italy): Preliminary Data on the Role of Olive Tree Plantations. In: Corti C, Lo Cascio P, Biaggini M, editors. Mainland and Insular Lizards: A Mediterrean Perspective. Florence: Firenze University Press; 2006. p. 1000-8.

Galán P. Demography and population dynamics of the lacertid lizard Podarcisbocagei in north-west Spain. J Zool. 1999;249(2):203-18.

Carretero MA. From set menu to a la carte. Linking issues in trophic ecology of Mediterranean lacertids. Ital J Zool. 2004;71(S2):121-33.

Soule M. Phenetics of natural populations. II. Asymmetry and evolution in a lizard. Am Nat. 1967;101(918):141-60.

Sillero N, Campos J, Bonardi A, Corti C, Creemers R, Crochet PA, Isailović JC, Denoël M, Ficetola GF, Gonçalves J, Kuzmin S. Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia-Reptilia. 2014;35(1):1-31.

Barbault R, Mou YP. Population dynamics of the common wall lizard, Podarcismuralis, in southwestern France. Herpetologica. 1988;44(1):38-47.

Radovanović M. Vodozemci I gmizavcinašezemlje. IzdavačkoPreduzećeNarodneRepublikeSrbije. 1951.

Parent GH. Contribution à la connaissance du peuplementherpétologique de la Belgique. Le caractererelictueld'âgeAtlantique de l'aire du lézard des murailles, Lacerta muralismuralis (LAURENTI) au Benelux. Nat Belg. 1978;59:209-22.

Tomović L, Kalezć M, Džukić G, editors. Red Book of Fauna of Serbia II - Reptiles. Belgrade: Faculty of Biology, University of Belgrade; 2015.

IUCN 2019: The IUCN Red List of Threatened Species [Internet]. Version 2019-1. International Union for Conservation of Nature and Natural Resources-SSC.c2001 - [cited 2019 May 28]. Available from: http://www.iucnredlist.org.

McKinney M, Yoon K, Zahedi F. Urbanization, biodiversity, and conservation. Bioscience. 2002;52:883-90.

Tomović L, Ajtić R, Ljubisavljević K, Urošević A, Jović D, Krizmanić I, Labus N, Đorđević S, Kalezić ML, Vukov T, Džukić G. Reptiles in Serbia: Distribution and diversity patterns. Bull Nat HistMuseum. 2014;7:129-58.

Kaliontzopoulou A, Carretero MA, Llorente GA. Morphology of the Podarcis wall lizards (Squamata: Lacertidae) from the Iberian Peninsula and North Africa: patterns of variation in a putative cryptic species complex. Zool J Linn Soc-Lond. 2011;164(1):173-93.

Sarre S, Dearn JM. Morphological Variation and Fluctuating Asymmetry Among Insular Populations of the Sleepy Lizard, Trachydosaurusrugosus Gray (Squamata, Scincidae). Aust J Zool. 1991;39(1):91-104.

Trokovic N, Herczeg G, AbGhani NI, Shikano T, Merilä J. High levels of fluctuating asymmetry in isolated stickleback populations. BMC Evol Biol. 2012;12(1):115.

Swaddle JP. Fluctuating asymmetry, animal behavior, and evolution. Adv Stud Behav. 2003;32:169-206.

Crespi BJ, Vanderkist BA. Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity. 1997;79(6):624.

McGill BJ, Enquist BJ, Weiher E, Westoby M. Rebuilding community ecology from functional traits. Trend EcolEvol. 2006;21:178-85.

Geber MA, Griffen LR. Inheritance and natural selection on functional traits. Int J Pant Sci. 2003;164:21-42.

Tocts AM, Johnson DW, Carter AJ. Strong nonlinear selection against fluctuating asymmetry in wild populations of a marine fish. Evolution. 2016;70(12):2899-908.

Eggert AK, Sakaluk SK. Fluctuating asymmetry and variation in the size of courtship food gifts in decorated crickets. Am Nat. 1994;144(4):708-16.

Leung B, Forbes MR. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience. 1996;3(4):400-13.

Laia RC, Pinto MP, Menezes VA, Rocha CF. Asymmetry in reptiles: What do we know so far? Springer Sci Rev. 2015;3(1):13-26.

Brown GP, Madsen T, Dubey S, Shine R. The causes and ecological correlates of head scale asymmetry and fragmentation in a tropical snake. Sci Rep. 2017;7(1):11363.

Beasley DAE, Bonisoli-Alquati A, Mousseau TA. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecol Indic. 2013;30:218-26.

Dosselman DJ, Schaalje GB, Sites Jr JW. An analysis of fluctuating asymmetry in a hybrid zone between two chromosome races of the Sceloporusgrammicus complex (Squamata: Phrynosomatidae) in central Mexico. Herpetologica. 1998;434-47.

Tull JC, Brussard PF. Fluctuating Asymmetry as an Indicator of Environmental Stress From OffHighway Vehicles. J Wildlife Manage. 2007;71(6):1944-8.

Polak M, Starmer WT. The quantitative genetics of fluctuating asymmetry. Evolution. 2001;55(3):498-511.

Palmer AR. Fluctuating asymmetry analyses: a primer. In: Markow TA, editor. Developmental instability: its origins and evolutionary implications. Dordrecht, Netherlands: Kluwer; 1994. p. 335-64.


Refbacks

  • There are currently no refbacks.


Copyright (c) 2019 ARCHIVES OF BIOLOGICAL SCIENCES

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.