ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah Acta Herpetologica 8(1): 75-78, 2013 Polydactyly in the Tyrrhenian wall lizard (Podarcis tiliguerta) Antigoni Kaliontzopoulou1,*, Daniele Salvi1, Verónica Gomes1, João P.M.C. Maia1,2,3, Panagiotis Kaliontzopoulos4 1 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661, Vairão, Portugal. *Cor- responding author. E-mail: antigoni@cibio.up.pt 2 Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre FC4 4169-007 Porto, Portugal 3 Institut de Biologia Evolutiva (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, 08003, Barcelona, Spain 4 Florinis 54, Vrilissia, Greece Submitted on: 2012, 30th November; revised on: 2013, 23rd April; accepted on: 2013, 28 th April. Abstract. Polydactyly is a fairly frequent phenomenon in tetrapod populations, but it is relatively rare in reptiles. Here we report the occurrence of polydactyly in a random sample of the Tyrrhenian wall lizard (Podarcis tiliguerta) from Sardinia. In the locality of Siniscola (NE Sardinia), we found two polydactylous female lizards, one of which showed polydactyly in one and the other in both hind limbs. This observation constitutes, to the best of our knowledge, the highest frequency of polydactyly ever reported in a single lizard population (4.54%). While providing a direct expla- nation for polydactyly is complicated, the genetic data available show that the two polydactylous individuals are not direct siblings, excluding the hypothesis of direct maternal inheritance of this condition. Keywords. Polydactyly, skeletal abnormalities, Tyrrhenian wall lizard. Polydactyly is an interesting phenomenon that fre- quently occurs in tetrapod populations but has never been evolutionarily truly re-established in any species. Strikingly, while a reduction in the number of digits has repeatedly occurred in several instances through- out tetrapod evolution, this condition has never been reversed (Lande, 1978; Tabin, 1992; Galis et al., 2001). This is intriguing, as a selective advantage of increased digit number exists under several evolutionary situations, enhancing for instance swimming, digging or grasping (Galis et al., 2001). However, this evolutionary advan- tage is always attained by extra digit-like structures that are in reality never “true” digits, but are rather modified wrist bones or extra phalanges (Caroll, 1997). The lack of polydactyly in evolution is not due to lack of heritable variation for that trait, as it is a condition very frequent- ly encountered in many tetrapod taxa. For instance, the presence of an additional finger or toe is the most com- mon anomaly at birth in humans (Castilla et al., 1996). Polydactyly is also quite frequent in other mammal spe- cies (Brignolo et al., 2002; Chapman, 2006; Moore et al., 2007; Gugolek et al., 2011), as well as birds (Fox, 1989; Huang et al., 2006; Sakai, 2006), and particularly amphib- ians (Mizgireuv et al., 1984; Johnson et al., 1999; Voro- byeva, 1999; Kiesecker, 2002; Taylor et al., 2005; Piha et al., 2006). It is less frequent in reptiles, with a single known case in chelonians (Martínez-Silvestre et al., 1998), and a few rare cases reported in lizards (Bauer et al., 2009). While sampling a population of Podarcis tiliguerta (Gmelin, 1789) near Siniscola (40.48° N, 9.78° E, Datum WGS1984; Fig. 1), Sardinia (Italy), we found two female lizards with postaxial polydactyly. The sampling site was located in a natural area characterised by low Mediter- ranean maqui vegetation and very low anthropogenic disturbance. The first lizard was 54 mm in snout vent length (SVL) and exhibited six digits in each of the hind feet (Fig. 2Ai and 2Aii). On the right foot the polydac- tyly cannot easily be described without radiography, but it seems to result from the duplication of digit III, while 76 Antigoni Kaliontzopoulou et al. on the left foot it is clearly a duplication of digit I. The second polydactylous lizard was 52 mm in SVL and pre- sented six toes on the left hind limb, which also seems to be the result of a metatarsal duplication of digit III (Fig. 1B). Unfortunately, the animals in question were released before noting this condition and could not be examined radiographically to identify the osteological basis of the polydactyly. However, at least in two of the three cases (those in Fig. 1Aii and 1B), the polydactyly appears to involve a normal number of metatarsals but an abnormal number of digits (brachydactyly sensu Bauer et al., 2009), as the supernumerary digits are clearly stemmed at a position posterior to the metatarsals. Both polydactylous females were adults, and their body size was within the normal range of the population (47-59 mm for the female individuals sampled in Sinis- cola). They both seemed in normal physical condition, and only presented a few red mite parasites (as seen in Fig. 2B), as was also the case for most of the individu- als examined from the same population. Both presented copulation marks, indicating that they had mated recent- ly, and the larger one was gravid when captured. Avail- able DNA sequence data for the mitochondrial 12S rRNA gene obtained following the procedure described in Salvi et al. (2011), showed that the two polydactylous individu- als present similar, but different haplotypes (Accession Numbers HF948026 and HF948027). Given the matrilin- eal inheritance of the mitochondrial genome, the occur- rence of different haplotypes in the two polydactylous individuals indicates that they are not siblings from a sin- gle clutch. Two aspects are worth noting in the case of polydac- tyly reported herein. First, this is the third case of poly- dactyly reported in wall lizards Podarcis (after P. pityu- sensis by Carretero et al., 1995 and P. muralis by Lazić and Crnobrnja-Isailović, 2012). Given the low number of reported cases in lizards, totalling seven that we are aware of (i.e. Carretero et al., 1995; Cuadrado, 1996; Pelegrin, 2007; Bauer et al., 2009; Minoli et al., 2009; Lazić and Crnobrnja-Isailović, 2012; Megía, 2012; but see also Nor- val et al., 2009), this means that a very high frequency of reported cases is observed in the genus Podarcis (repre- senting almost half of the existing observations). While this may be the result of a reporting bias, it may also indicate that this condition is for some unknown reason more frequent in Podarcis wall lizards. Similarly high fre- quencies are only known from chameleons, where poly- dactyly seems to be quite frequent and has been observed in several populations of the same species (Cuadrado, 1996). Second, this is the first time that two polydacty- lous individuals have been encountered in a random liz- ard sample. In fact, this is the highest reported frequency of polydactyly in a lizard population, since the two obser- vations come from a total, random sample, of 44 individ- uals (4.54%). This is remarkably high for lizards, where reported frequencies range between 0.2 and 0.6% (Bauer et al., 2009). According to genetic data, a direct sibling association could not be established between the two individuals. Consequently, while a genetic cause under- lying this observation of polydactyly cannot be excluded at the population level, the high frequency reported here does not seem to be the outcome of the reproduction of a single pair of lizards. The causes of polydactyly are difficult to decipher. Mutations in genes involved in digit development and specification (such as the Hedgehog, BmP, FgF and Hox gene families) are known to cause polydactyly in mam- mals, birds, and amphibians (Zákány et al., 1997; Vil- lagómez and Alonso, 1998; Yokoyama et al., 1998; Kraus et al., 2001; Huang et al., 2006). Polydactyly is also   Figure 1. Geographic location of the studied population of Podarcis tiliguerta from Siniscola in Sardinia (Italy). 77Polydactyly in Podarcis tiliguerta known to be frequently associated to chromosomal tri- somies, at least in mammals (Pugsley, 1985; Brignolo et al., 2002; Moore et al., 2007). In amphibians, polydactyly has been associated with infection from some parasites (Jonhson et al., 1999; Kiesecker, 2002) or viruses (Bor- kin and Pikulik, 1986), as well as environmental con- tamination due to the use of pesticides (Mizgireuv et al., 1984; Diana and Beasley, 1998; Kiesecker, 2002; Tay- lor et al., 2005; Piha et al., 2006). In reptiles, the endog- enous (genetic) and exogenous (environmental) causes of polydactyly are not fully understood, yet the case study reported herein and previous observations suggest that lizards of the genus Podarcis would be a promising model organism for investigating the occurrence of polydactyly and its proximate determinants. ACKNOWLEDGMENTS The Italian Ministry of Environment issued per- mits, DPN-2009-0005106, for the capture of the lizards. AK and DS were supported by post-doctoral grants (SFRH/ BPD/68493/2010 and SFRH/BPD/66592/2009 respectively) and JPMCM by a pre-doctoral grant (SFRH/BD/74305/2010), all by Fundação para a Ciência e Tecnologia (FCT, Portu- gal). Support was also provided by FCT project PTDC/BIA- BEC/101256/2008. REFERENCES Bauer, A.M., Hathaway, S.A., Fisher, R.N. (2009): Poly- dactyly in the Central Pacific Gecko, Lepidodactylus sp. (Squamata: Gekkonidae). Herpetol. Notes 2: 243- 246. Borkin, L.J., Pikulik, M.M. (1986): The occurrence of polymely and polydactyly in natural populations of anurans of the USSR. Amphibia-Reptilia 7: 205-216. Brignolo, L., Tarara, R., Peterson, P.E., Hendrickx, A.G. (2002): Two cases of digital defects in Macaca mulatta infants and a survey of the literature. J. Med. Primatol. 31: 98-103. Caroll, R.L. (1997): Patterns and Processes of Vertebrate Evolution. Cambridge University Press, Cambridge. Castilla, E.E., Lugarinho da Fonseca, R., da Graça Dutra, M., Bermejo, E., Cuevas, L., Martínez-Frías, M.L. (1996): Epidemiological analysis of rare polydactylies. Am. J. Med. Genet. 65: 295-303. Carretero, M. A., Llorente, G. A., Santos, X., Montori, A. (1995): Un caso de polidactilia en lacértidos. Bol. Asoc. Herpetol. Esp. 6: 11-13. Chapman, N.G. (2006): Polydactyly in roe deer (Capreo- lus capreolus). Eur. J. Wildl. Res. 52: 142-144. Cuadrado, M. (1996): Tasa de polidactilía en el camaleón común Chamaeleo chamaeleon. Bol. Asoc. Herpetol. Esp. 7: 23-24. Figure 2. Polydactyly in two female individuals of the Siniscola population of Podarcis tiliguerta, encompassing polydactyly in both hind feet in the first (Ai and Aii) and only in the left hind limb in the second (B). 78 Antigoni Kaliontzopoulou et al. Diana, S.G., Beasley, V.R. (1998): Amphibian toxicology. In: Status and Conservation of Midwestern Amphib- ians, pp. 266-277. Lannoo, M.J. Ed, University of Iowa Press, Iowa City. Fox, N.C. (1989): A unilateral extra digit in a wild com- mon buzzard (Buteo buteo). Avian Pathol. 18: 193- 195. Galis, F., van Alphen, J.J. M., Metz, J.A.J. (2001): Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol. Evol. 16: 637-646. Gugołek, A., Strychalski, J., Konstantynowicz, M. (2011): Polydactyly in Arctic foxes (Vulpes lagopus). Turk. J. Vet. Anim. Sci. 35: 277-280. Huang, Y.Q., Deng, X.M., Du, Z.Q., Qiu, X., Du, X., Chen, W., Morisson, M., Leroux, S., Ponce de Léon, F.A., Da, Y., Li, N. (2006): Single nucleotide polymor- phisms in the chicken Lmbr1 gene are associated with chicken polydactyly. Gene 374: 10-18. Johnson, P.T.J., Lunde, K.B., Ritchie, E.G., Launer, A.E. (1999): The effect of trematode infection on amphib- ian limb development and survivorship. Science 284: 802-804. Kiesecker, J.M. (2002): Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature? P. Natl. Acad. Sci. USA 99: 9900-9904. Kraus, P., Fraidenraich, D., Loomis, C.A. (2001): Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech. Develop. 100: 45-58. Lande, R. (1978): Evolutionary mechanisms of limb loss in tetrapods. Evolution 32: 73-92. Lazić, M.M., Crnobrnja-Isailović, J. (2012): Polydactyly in the common wall lizard Podarcis muralis (Squamata: Lacertidae). Herpetol. Notes 5: 277-279. Martínez-Silvestre, A., Soler, J., Solé, R., Sampere, X. (1998): Polidactilia en Testudo hermanni y causas teratogénicas en reptiles. Bol. Asoc. Herpetol. Esp. 9: 35-38. Megía, R. (2012): Un caso de polidactilia en Lacerta schreiberi en el Sistema Central. Bol. Asoc. Herpetol. Esp. 23: 54-57. Minoli, I., Feltrin, N., Ávila, L.J. (2009): Un caso de poli- dactilia en Liolaemus petrophilus (Iguania: Squamata: Liolaemini). Cuader. Herpetol. 23: 89-92. Mizgireuv, I.V., Flax, N.L., Borkin, L.J., Khudoley, V. V. (1984): Dysplastic lesions and abnormalities in amphibians associated with environmental conditions. Neoplasma 31: 175-181. Moore, C.M., Hubbard, G.B., Dick, E., Dunn, B.G., Raveendran, M., Rogers, J., Williams, V., Gomez, J.J., Butler, S.D., Leland, M.M., Schlabritz-Loutsevitch, N.E. (2007): Trisomy 17 in a baboon (Papio hama- dryas) with polydactyly, patent foramen ovale and pyelectasis. Am. J. Primatol. 69: 1105-1118. Norval, G., Mao, J.J., Bursey, C.R., Goldberg, S.R. (2009): A deformed hind limb of an invasive free-living brown anole (Anolis sagrei Duméril & Bibron, 1837) from Hualien City, Taiwan. Herpetol. Notes. 2: 219- 221. Pelegrin, N. (2007): Presence of a polydactylous Tropi- durus etheridgei (Squamata: Iguanidae: Tropidurinae) in the Dry Chaco of Córdoba Province, Argentina. Cuader. Herpetol. 21: 115-116. Piha, H., Pekkonen, M., Merilä, J. (2006): Morphological abnormalities in amphibians in agricltural habitats: a case study of the common frog Rana temporaria. Copeia 2006: 810-817. Pugsley, S. L. (1985): Congenital malformations in a com- mon marmoset (Callithrix jacchus) similar to human 13-trisomy syndrome. Lab. Anim. 19: 123-124. Sakai, W. H. (2006): Polydactyly in a Vaux’s swift. Wilson J. Ornithol. 118: 424-426. Salvi, D., Harris, D.J., Perera A., Bologna, M.A., Carret- ero, M.A. (2011): Preliminary survey on genetic vari- ation within the Pygmy Algyroides, Algyroides fitz- ingeri, across Corsica and Sardinia. Amphibia-Reptilia 32: 281-286. Tabin, C.J. (1992): Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development 116: 289-296. Taylor, B., Skelly, D., Demarchis, L.K., Slade, M.D., Galu- sha, D., Rabinowitz, P. M. (2005): Proximity to pollu- tion sources and risk of amphibian limb malforma- tion. Environ. Health Persp. 113: 1497-1501. Vorobyeva, E.I. (1999): The problem of polydactyly in amphibians. Russ. J. Herpetol. 6: 95-103. Villagómez, D.A., Alonso, R.A. (1998): A distinct Mende- lian autosomal recessive syndrome involving the asso- ciation of anotia, palate agenesis, bifid tongue, and polydactyly in the dog. Can. Vet. J. 39: 642-643. Yokoyama, H., Endo, T., Tamura, K., Yajima, H., Ide, H. (1998): Multiple digit formation in Xenopus limb bud recombinants. Dev. Biol. 196: 1-10. Zákány, J., Fromental-Ramain, C., Warot, X., Duboule, D. (1997): Regulation of number and size of digits by posterior Hox genes: a dose-dependent mecha- nism with potential evolutionary implications. P. Natl. Acad. Sci. USA 94: 13695-13700. Acta Herpetologica Vol. 8, n. 1 - June 2013 Firenze University Press The oogenic cycle of the Caspian bent-toed gecko, Cyrtopodion caspium (Squamata: Gekkonidae) in Iran Vida Hojati1*, Kazem Parivar2, Eskandar Rastegar-Pouyani3, Abdolhossein Shiravi1 Altitudinal effects on life history parameters in populations of Liolaemus pictus argentinus (Sauria: Liolaemidae) Joel Antú Gutiérrez1,*, Carla Piantoni2, Nora R. Ibargüengoytía1,3 Recent cryptic extinction of squamate reptiles on Yoronjima Island of the Ryukyu Archipelago, Japan, inferred from garbage dump remains Yasuyuki Nakamura1,*, Akio Takahashi2, Hidetoshi Ota3 Trophic niche and feeding biology of the Italian wall lizard, Podarcis siculus campestris (De Betta, 1857) along western Mediterranean coast Marco A.L. Zuffi*, Chiara Giannelli Novel, non-invasive method for distinguishing the individuals of the fire salamander (Salamandra salamandra) in capture-mark-recapture studies Goran Šukalo1,*, Sonja Đorđević2, Dragojla Golub1, Dejan Dmitrović1, Ljiljana Tomović2,3 Going out tonight? When insular Hierophis viridiflavus breaks the Whip Snakes Rules Delaugerre Michel-Jean First evidence of a paedomorphic population of the smooth newt (Lissotriton vulgaris) in the Czech Republic Václav Gvoždík1,2, Veronika Javůrková4, Oldřich Kopecký5,* No detection of chytrid in first systematic screening of Bombina variegata pachypus (Anura: Bombinatoridae) in Liguria, northern Italy Stefano Canessa1,*, An Martel2, Frank Pasmans2 Status of the European pond turtle, Emys orbicularis (Reptilia: Testudines: Emydidae) in Vorarlberg, Austria Andreas Kleewein1, Günther Wöss2 Comparative cytogenetics of two species of ground skinks: Scincella assata and S. cherriei (Squamata: Scincidae: Lygosominae) from Chiapas, Mexico Riccardo Castiglia1,*, Alexandra M.R. Bezerra2, Oscar Flores-Villela3, Flavia Annesi1, Antonio Muñoz4, Ekaterina Gornung1 Polydactyly in the Tyrrhenian wall lizard (Podarcis tiliguerta) Antigoni Kaliontzopoulou1,*, Daniele Salvi1, Verónica Gomes1, João P. M. C. Maia1,2,3, Panagiotis Kaliontzopoulos4 Book Review: Roberto Sindaco, Alberto Venchi, Cristina Grieco. The Reptiles of the Western Palearctic. 2. Annotated checklist and distributional atlas of the snakes of Europe, North Africa, Middle East and Central Asia, with an update to the Vol. 1. Edoardo Razzetti ACTA HERPETOLOGICA Journal of the Societas Herpetologica Italica