Fluctuating asymmetry is a function of population isolation in island lizards

Journal of Zoology

Volumn 282, Issue 4, 2010, Pages 266-275

  Bǎncilǎ, Raluca ^a,b,c   Van Gelder, Iris ^c   Rotteveel, Erik ^c   Loman, Juke ^c   Arntzen, J W ^c  

^a EMIL RACOVI INSTITUTE OF SPELEOLOGY   (Romania)

^b OVIDIUS UNIVERSITY   (Romania)

^c NATURALIS BIODIVERSITY CENTER   (Netherlands)

Author keywords

Conservation biology; Geometric morphometrics; Isolated populations; Meristic characters; Podarcis; Shape asymmetry

Indexed keywords

ARCHIPELAGO; BODY SHAPE; CONSERVATION MANAGEMENT; FLUCTUATING ASYMMETRY; GENETIC ANALYSIS; HYPOTHESIS TESTING; ISOLATED POPULATION; LIZARD; MOLECULAR ANALYSIS; MORPHOLOGY; MORPHOMETRY; SPATIOTEMPORAL ANALYSIS;

GALICIA [SPAIN]; RIA DE AROSA; RIAS BAJAS; SPAIN;

PODARCIS; PODARCIS BOCAGEI; PODARCIS HISPANICA; SQUAMATA;

EID: 78650154869     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2010.00736.x     Document Type: Article

References (61)

1. Allendorf, F.W. & Luikart, G. (2007). Conservation and the genetics of populations. Malden: Blackwell.
2. Anciães, M. & Marini, M.Ã. (2000). The effects of fragmentation on fluctuating asymmetry in passerine birds of Brazilian tropical forests. J. Appl. Ecol. 37, 1013-1028.
3. Arnold, E.N., Arribas, O. & Carranza, S. (2007). Systematics of the Palaearctic and Oriental lizard tribe Lacertini (Squamata: Lacertidae: Lacertinae), with descriptions of eight new genera. Zootaxa 1430, 1-86.
4. Arntzen, J.W. & Sá-Sousa, P. (2007). Morphological and genetical differentiation of lizards (Podarcis bocagei and P. hispanica) in the Ria de Arosa archipelago (Galicia, Spain) resulting from vicariance and occasional dispersal. In Biogeography, time, and place: distributions, barriers, and islands: 365-401. Renema, W. (Ed.). Dordrecht: Springer.
5. Bookstein, F.L. (1982). Foundations of morphometrics. Annu. Rev. Ecol. Syst. 13, 451-470.
6. Brongersma, L.D. & Pannekoek, A.J. (1966). Investigations in and around the Ria de Arosa, north-west Spain, 1962-1964. Leidse Geologische Mededelingen 37, 1-5.
7. Cadée, G.C. (1968). Molluscan biocoenoses and thanatocoenoses in the Ria de Arosa, Galicia, Spain. Z. Verhandelingen 95, 1-121.
8. Cho, B.R. & Park, C. (2005). Robust design modeling and optimization with unbalanced data. Comput. Ind. Eng. 48, 173-180.
9. Clarke, G.M. (1993). The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica 89, 15-23.
10. Cnaan, A., Laird, N.M. & Slasor, P. (1997). Using the general linear mixed model to analyze unbalanced repeated measures and longitudinal data. Stat. Med. 16, 2349-2380.
11. Cole, C.J. (1996). Femoral glands in lizards: a review. Herpetologica 22, 199-206.
12. Crawford, D.J., Ruiz, E., Stuessy, T.F., Tepe, E., Aqeveque, P., Gonzalez, F., Jensen, R.J., Anderson, G.J., Bernardello, G., Baeza, C.M., Swenson, U. & Silva, M. (2001). Allozyme diversity in the endemic flowering plant species of the Juan Fernandez Archipelago, Chile: ecological and historical factors with implications for conservation. Am. J. Bot. 88, 2195-2203.
13. 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.
14. Crnokrak, P. & Roff, D.A. (1999). Inbreeding depression in the wild. Heredity 83, 260-270.
15. Cunningham, M. & Moritz, C. (1997). Genetic effects of forest fragmentation on a rainforest restricted lizard (Scincidae: Gnypetoscincus queenslandiae). Biol. Conserv. 83, 19-30.
16. Dias, J.M.A., Boski, T., Rodrigues, A. & Magalhães, F. (2000). Coast line evolution in Portugal since the last glacial maximum until present - a synthesis. Mar. Geol. 170, 177-186.
17. Eldridge, M.D.B, King, J.M., Loupis, A.K., Spencer, P.B.S., Taylor, A.C., Pope, L.C. & Hall, G.P. (1999). Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv. Biol. 13, 531-541.
18. Frankham, R. (1998). Inbreeding and extinction: island populations. Conserv. Biol. 12, 665-675.
19. Frankham, R. (2005). Genetics and extinction. Biol. Conserv. 126, 131-140.
20. Gillespie, R.G. & Roderick, G.K. (2002). Arthropods on islands: colonization, speciation, and conservation. Ann. Rev. Entomol. 47, 595-632.
21. Gilligan, D.M., Woodworth, L.M., Montgomery, M.E, Nurthern, R.K, Briscoe, D.A & Frankham, R. (2000). Can fluctuating asymmetry be used to detect inbreeding and loss of genetic diversity in endangered populations? Anim. Conserv. 3, 97-104.
22. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
23. Jobson, J.D. (1992). Applied multivariate data analysis. Vol. 2. Categorical and multivariate methods. New York: Springer.
24. King, R. (1987). Reptile distributions on islands in Lake Erie. J. Herpetol. 21, 65-67.
25. Klingenberg, C.P. & McIntyre, G.S. (1998). Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 54, 1363-1375.
26. Leary, R.F. & Allendorf, F.W. (1989). Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol. Evol. 4, 214-217.
27. Leary, R.F., Allendorf, F.W., Knudson, R.L. & Thorgaard, G.H. (1985). Heterozygosity and developmental stability in gynogenetic diploid and triploid rainbow trout. Heredity 54, 219-225.
28. Lens, L., Van Dongen, S., Galbusera, P., Schenck, T., Matthysen, E. & Van de Casteele, T. (2000). Developmental instability and inbreeding in natural bird populations exposed to different levels of habitat disturbance. J. Evol. Biol. 13, 889-896.
29. Leung, B., Forbes, M.R. & Houle, D. (2000). Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am. Nat. 155, 101-115.
30. Leung, L.K.-P., Dickman, C.R. & Moore, L.A. (1993). Genetic variation in fragmented populations of an Australian rainforest rodent, Melomys cervinipes. Pac. Conserv. Biol. 1, 58-65.
31. Losos, J.B., Warheit, K.I. & Schoener, T.W. (1997). Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387, 70-73.
32. MacArthur, R.H. & Wilson, E.O. (1967). The theory of island biogeography. Princeton: Princeton University Press.
33. Madsen, T., Stille, B. & Shine, R. (1997). Inbreeding depression in an isolated population of adders (Vipera berus). Biol. Conserv. 75, 113-118.
34. May, R.M., Lawton, J.H. & Stork, N.E. (1995). Assessing extinction rates. In Extinction rates: 1-24. Lawton, J.H. & May, R.M. (Eds). New York: Oxford University Press.
35. Møller, A.P. & Swaddle, J.P. (1997). Asymmetry, developmental stability, and evolution. Oxford: Oxford University Press.
36. Palmer, A.R. (1994). Fluctuating asymmetry analysis: a primer. In Markow, Developmental instability: its origins and evolutionary implications: 335-364. Markow, T.A. (Ed.). Dordrecht: Kluwer Academic Publishers.
37. Palmer, A.R. & Strobeck, C. (1986). Fluctuating asymmetry: measurement, analysis, patterns. Ann. Rev. Ecol. Syst. 17, 391-421.
38. Palmer, A.R. & Strobeck, C. (2003). Fluctuating asymmetry analysis revisited. In Developmental instability (DI): causes and consequences: 279-319. Polak, M. (Ed.). Oxford: Oxford University Press.
39. Pannekoek, A.J. (1966). The Ria problem. The role of antecedence, deep weathering, and Pleistocene slope-wash in the formation of the west-Galician rias. Tijdschrift Koninklijk Nederlands Aardrijkskundig Genootschap 83, 289-297.
40. Parsons, P.A. (1990). Fluctuating asymmetry: an epigenetic measure of stress. Biol. Rev. 65, 131-145.
41. Pethick, J. (1984). An introduction to coastal geomorphology. London: Edward Arnold.
42. Pertoldi, C., Kristensen, T.N., Andersen, D.H. & Loeschcke, V. (2006). Developmental instability as an estimator of genetic stress. Heredity 96, 122-127.
43. Pinho, C., Ferrand, N. & Harris, D.J. (2006). Reexamination of the Iberian and North African Podarcis (Squamata: Lacertidae) phylogeny based on increased mitochondrial DNA sequencing. Mol. Phylogenet. Evol. 38, 266-273.
44. Pinho, C., Harris, D.J. & Ferrand, N. (2002) Post-glacial expansion of Podarcis bocagei: evidence from protein electrophoretic data. Abstracts of the 7th Portuguese-Spanish Congress of Herpetology, Portuguese Herpetological Society, Évora, p. 147.
45. Polak, M. & Starmer, W.T. (2001). The quantitative genetics of fluctuating asymmetry. Evolution 55, 498-511.
46. Richtsmeier, J.T., Deleon, V.B. & Lele, S.R. (2002). The promise of geometric morphometrics. Yearb. Phys. Anthropol. 45, 63-91.
47. Rohlf, F.J. (1999a). TpsDig, version 1.18. Stony Brook: Department of Ecology and Evolution, State University of New York at Stony Brook, USA.
48. Rohlf, F.J. (1999b). Shape statistics procrustes superimpositions and tangent space. J. Classif. 16, 1977-223.
49. Sarre, S. (1996). Habitat fragmentation promotes fluctuating asymmetry but not morphological divergence in two geckos. Res. Popul. Ecol. 38, 57-64.
50. Sarre, S. & Dearn, J.D. (1991). Morphological variation and fluctuating asymmetry among insular populations of the sleepy lizard, Trachydosaurus rugosus Gray (Squamata, Scincidae). Aust. J. Zool. 39, 91-104.
51. Sarre, S., Dearn, J.D. & Georges, A. (1994). The application of fluctuating asymmetry in the monitoring of animal populations. Pac. Conserv. Biol. 1, 118-122.
52. Sheets, H.D. (2003). Integrated morphometrics package (IMP). Available at (accessed 4 November 2008).
53. Soulé, M.E. (1967). Phenetics of natural populations II. Symmetry and evolution in a lizard. Am. Nat. 101, 141-160.
54. Soulé, M.E. (1986). Conservation biology: the science of scarcity and diversity. Sunderland: Sinauer.
55. Swaddle, P.J. (2003). Fluctuating asymmetry, animal behavior and evolution. Adv. Stud. Behav. 32, 169-205.
56. Taning, A. (1952). Experimental study of meristic characters in fishes. Biol. Rev. 27, 169-193.
57. Van Dongen, S., Lens, L. & Molenberghs, G. (1999). Mixture analysis of asymmetry: modeling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry. Ecol. Lett. 2, 387-396.
58. Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution 16, 125-142.
59. Vervust, B., Van Dongen, S., Grbac, I. & Van Damme, R. (2008). Fluctuating asymmetry, physiological performances, and stress in island populations of the Italian wall lizard (Podarcis sicula). J. Herpetol. 42, 369-377.
60. Young, A., Boyle, T. & Brown, T. (1996). The population genetic consequences of habitat fragmentation for plants. Trends Ecol. Evol. 11, 413-418.
61. Watson, P.J. & Thornhill, R. (1994). Fluctuating asymmetry and sexual selection. Trends Ecol. Evol. 9, 21-25.