Hybridization between distinct species of animals and subsequent genetic introgression plays a considerable role in the speciation process and the emergence of adaptive characters. Fitness of between-species hybrids usually sharply decreases with the divergence time of the concerned species and the divergence depth, which still allows for a successful crossing differs among principal clades of vertebrates. Recently, a review of hybridization events among distinct lizard species revealed that lizards belong to vertebrates with a highly developed ability to hybridize. In spite of this, reliable reports of experimental hybridizations between genetically fairly divergent species are only exceptional. Here, we show the results of the crossing of two distinct allopatric species of eyelid geckos possessing temperature sex determination and lacking sex chromosomes: Eublepharis macularius distributed in Pakistan/Afghanistan area and E. angramainyu, which inhabits Mesopotamia and adjacent areas. We demonstrated that F1 hybrids were viable and fertile, and the introgression of E. angramainyu genes into the E. macularius genome can be enabled via a backcrossing. The examined hybrids (except those of the F2 generation) displayed neither malformations nor a reduced survival. Analyses of morphometric and coloration traits confirmed phenotypic distinctness of both parental species and their F1 hybrids. These findings contrast with long-term geographic and an evolutionary separation of the studied species. Thus, the occurrence of fertile hybrids of comparably divergent species, such as E. angramainyu and E. macularius, may also be expected in other taxa of squamates. This would violate the current estimates of species diversity in lizards.

Department of Zoology Faculty of Science Charles University Prague Prague Czech Republic

Zobrazit více v PubMed

Darwin C. On the Origin of Species by means of Natural Selection, or the preservation of favoured races in the struggle for life London: John Murray; 1859. PubMed PMC

Arnold ML. Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics. 1992;23:237–61. 10.1146/annurev.es.23.110192.001321 . DOI

Grant PR, Grant BR. Hybridization of bird species. Science. 1992;256(5054):193–7. 10.1126/science.256.5054.193 . PubMed DOI

Dowling T, Secor C. The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics. 1997;28:593–619. 10.1146/annurev.ecolsys.28.1.593 . DOI

Barton NH. The role of hybridization in evolution. Molecular Ecology. 2001;10(3):551–68. 10.1046/j.1365-294x.2001.01216.x . PubMed DOI

Burke J, Arnold M. Genetics and the fitness of hybrids. Annual Review of Genetics. 2001;35:31–52. 10.1146/annurev.genet.35.102401.085719 . PubMed DOI

True J, Weir B, Laurie C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans . Genetics. 1996;142(3):819–37. . PubMed PMC

Mallet J, Beltran M, Neukirchen W, Linares M. Natural hybridization in heliconiine butterflies: the species boundary as a continuum. Bmc Evolutionary Biology. 2007;7 10.1186/1471-2148-7-28 . PubMed DOI PMC

Miralles L, Machado-Schiaffino G, Garcia-Vazquez E. Genetic markers reveal a gradient of hybridization between cape hakes (Merluccius capensis and Merluccius paradoxus) in their sympatric geographic distribution. Journal of Sea Research. 2014;86:69–75. 10.1016/j.seares.2013.11.009 . DOI

Vines TH, Kohler SC, Thiel A, Ghira I, Sands TR, MacCallum CJ, et al. The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata . Evolution. 2003;57(8):1876–88. . PubMed

Machado T, Silva VX, Silva MJD. Phylogenetic relationships within Bothrops neuwiedi group (Serpentes, Squamata): Geographically highly-structured lineages, evidence of introgressive hybridization and Neogene/Quaternary diversification. Molecular Phylogenetics and Evolution. 2014;71:1–14. 10.1016/j.ympev.2013.10.003 . PubMed DOI

Olave M, Martinez LE, Avila LJ, Sites JW, Morando M. Evidence of hybridization in the Argentinean lizards Liolaemus gracilis and Liolaemus bibronii (IGUANIA: LIOLAEMINI): An integrative approach based on genes and morphology. Molecular Phylogenetics and Evolution. 2011;61(2):381–91. 10.1016/j.ympev.2011.07.006 . PubMed DOI

Grant PR, Grant BR, Markert JA, Keller LF, Petren K. Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution. 2004;58(7):1588–99. . PubMed

Reifova R, Kverek P, Reif J. The first record of a female hybrid between the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (Luscinia luscinia) in nature. Journal of Ornithology. 2011;152(4):1063–8. 10.1007/s10336-011-0700-7 . DOI

Macholan M, Munclinger P, Sugerkova M, Dufkova P, Bimova B, Bozikova E, et al. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution. 2007;61(4):746–71. 10.1111/j.1558-5646.2007.00065.x . PubMed DOI

Amaral AR, Lovewell G, Coelho MM, Amato G, Rosenbaum HC. Hybrid speciation in a marine mammal: The Clymene Dolphin (Stenella clymene). Plos One. 2014;9(1). 10.1371/journal.pone.0083645 . PubMed DOI PMC

Rieseberg LH, Archer MA, Wayne RK. Transgressive segregation, adaptation and speciation. Heredity. 1999;83:363–72. 10.1038/sj.hdy.6886170 . PubMed DOI

Stelkens R, Seehausen O. Genetic distance between species predicts novel trait expression in their hybrids. Evolution. 2009;63(4):884–97. 10.1111/j.1558-5646.2008.00599.x . PubMed DOI

Hedrick PW. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology. 2013;22(18):4606–18. 10.1111/mec.12415 . PubMed DOI

Lynch M. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution. 1991;45(3):622–9. 10.2307/2409915 . PubMed DOI

Edmands S. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution. 1999;53(6):1757–68. 10.2307/2640438 . PubMed DOI

Grant BR, Grant PR. High survival of Darwin's finch hybrids: Effects of beak morphology and diets. Ecology. 1996;77(2):500–9. 10.2307/2265625 . DOI

Lopez-Fernandez H, Bolnick DI. What Causes Partial F1 Hybrid Viability? Incomplete Penetrance versus Genetic Variation. Plos One. 2007;2(12). 10.1371/journal.pone.0001294 . PubMed DOI PMC

Baranwal VK, Mikkilineni V, Zehr UB, Tyagi AK, Kapoor S. Heterosis: emerging ideas about hybrid vigour. Journal of Experimental Botany. 2012;63(18):6309–14. 10.1093/jxb/ers291 . PubMed DOI

Grant BR, Grant PR. Fission and fusion of Darwin's finches populations. Philosophical Transactions of the Royal Society B-Biological Sciences. 2008;363(1505):2821–9. 10.1098/rstb.2008.0051 . PubMed DOI PMC

Edmands S. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology. 2007;16(3):463–75. 10.1111/j.1365-294X.2006.03148.x . PubMed DOI

Dobzhansky T. Studies on hybrid sterility. II. localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics. 1936;21:113–35. PubMed PMC

Dobzhansky T. Genetics and the Origin of the Species. [S.l.]: Columbia University Press; 1937.

Muller H. Bearing of the Drosophilla work on systematics In: Huxley J, editor. The New Systematics. Oxford: Claredon Press; 1940. p. 185–268.

Muller HJ. Isolating mechanisms, evolution and temperature. Biol Symp. 1942;6(811):71–125.

Presgraves DC. Darwin and the Origin of Interspecific Genetic Incompatibilities. American Naturalist. 2010;176:S45–S60. 10.1086/657058 . PubMed DOI

Sasa M, Chippindale P, Johnson N. Patterns of postzygotic isolation in frogs. Evolution. 1998;52(6):1811–20. 10.2307/2411351 . PubMed DOI

Lijtmaer D, Mahler B, Tubaro P. Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution. 2003;57(6):1411–8. . PubMed

Bolnick DI, Near TJ. Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution. 2005;59(8):1754–67. . PubMed

Orr HA, Coyne JA. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics. 1989;121(3):527–37. . PubMed PMC

Matute DR, Butler IA, Turissini DA, Coyne JA. A Test of the Snowball Theory for the Rate of Evolution of Hybrid Incompatibilities. Science. 2010;329(5998):1518–21. 10.1126/science.1193440 . PubMed DOI

Arrieta RS, Lijtmaer DA, Tubaro PL. Evolution of postzygotic reproductive isolation in galliform birds: analysis of first and second hybrid generations and backcrosses. Biological Journal of the Linnean Society. 2013;110(3):528–42. 10.1111/bij.12153 . DOI

Arntzen JW, Wielstra B, Wallis GP. The modality of nine Triturus newt hybrid zones assessed with nuclear, mitochondrial and morphological data. Biological Journal of the Linnean Society. 2014;113(2):604–22. 10.1111/bij.12358 . DOI

Schumer M, Cui RF, Powell D, Dresner R, Rosenthal G, Andolfatto P. High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species. Elife. 2014;3 10.7554/eLife.02535 . PubMed DOI PMC

Herrington SJ, Hettiger KN, Heist EJ, Keeney DB. Hybridization between longnose and alligator gars in captivity, with comments on possible gar hybridization in nature. Transactions of the American Fisheries Society. 2008;137(1):158–64. 10.1577/t07-044.1 . DOI

Hedges SB, Dudley J, Kumar S. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics. 2006;22(23):2971–2. 10.1093/bioinformatics/btl505 . PubMed DOI

Karl SA, Bowen BW, Avise JC. Hybridization among the ancient marineres: Characterization of marine turtle hybrids with molecular genetic assays. Journal of Heredity. 1995;86(4):262–8. . PubMed

Smith SA, Stephens PR, Wiens JJ. Replicate patterns of species richness, historical biogeography, and phylogeny in holarctic treefrogs. Evolution. 2005;59(11):2433–50. . PubMed

Jancuchova-Laskova J, Landova E, Frynta D. Are genetically distinct lizard species able to hybridize? A review. Current Zoology. 2015;61(1):155–80. .

Wilson AC, Maxson LR, Sarich VM. Two types of molecular evolution. Evidence from studies of interspecific hybridization. Proceedings of the National Academy of Sciences of the United States of America. 1974;71(7):2843–7. 10.1073/pnas.71.7.2843 . PubMed DOI PMC

Prager E, Wilson A. Slow evolutionary loss of the potential for interspecific hybridization in birds: A manifestation of slow regulatory evolution. Proceedings of the National Academy of Sciences of the United States of America. 1975;72(1):200–4. 10.1073/pnas.72.1.200 . PubMed DOI PMC

Fitzpatrick BM. Rates of evolution of hybrid inviability in birds and mammals. Evolution. 2004;58(8):1865–70. . PubMed

Naro-Maciel E, Le M, FitzSimmons NN, Amato G. Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution. 2008;49(2):659–62. 10.1016/j.ympev.2008.08.004 . PubMed DOI

Schilde M, Barth D, Fritz U. An Ocadia sinensis x Cyclemys shanensis hybrid (Testudines: Geoemydidae). Asiatic Herpetological Research. 2004;10:120–5.

Buskirk JR, Parham JF, Feldman CR. On the hybridisation between two distance related Asian turtles (Testudines: Sacalia x Mauremys). Salamandra. 2005;41(1/2):21–6.

Georges A, Adams M, McCord W. Electrophoretic delineation of species boundaries within the genus Chelodina (Testudines: Chelidae) of Australia, New Guinea and Indonesia. Zoological Journal of the Linnean Society. 2002;134(4):401–21. 10.1046/j.1096-3642.2002.00007.x . DOI

Lourenco JM, Glemin S, Chiari Y, Galtier N. The determinants of the molecular substitution process in turtles. Journal of Evolutionary Biology. 2013;26(1):38–50. 10.1111/jeb.12031 . PubMed DOI

Polet G, Murphy DJ, Phan VL, Tran VM. Crocodile conservation at work in Vietnam, re-establishing Crocodylus siamensis in Cat Tien National Park. Proceedings of the 16th Working Meeting of the IUCN-SSC Crocodile Specialist Group Gainesville, Florida, 7–10 October 2002. 2002:86–95.

Brochu CA. Phylogenetic relationships and divergence timing of Crocodylus based on morphology and the fossil record. Copeia. 2000;(3):657–73. .

Darevsky IS, Kupriyanova LA. Two new all-female lizard species of the genus Leiolepis Cuvier, 1829 from Thailand and Vietnam (Squamata: Sauria: Uromastycinae). Herpetozoa. 1993;6(1–2):3–20. .

Uzzell T, Darevsky IS. Biochemical evidence for hybrid origin of parthenogenetic species of Lacerta saxicola complex (Sauria: Lacertidae), with a discussion of some ecological and evolutionary implications. Copeia. 1975;(2):204–22. .

Wright JW, Lowe CH. Weeds polyploids parthenogenesis and geographical and ecological distribution of all-female species of Cnemidophorus . Copeia. 1968;(1):128–38. .

Cuellar O, Kluge AG. Natural parthenogenesis in gekkonid lizard Lepidodactylus lugubris . Journal of Genetics. 1972;61(1):14–26. 10.1007/bf02984098 . DOI

Darevsky IS, Kupriyanova LA, Roshchin VV. A New All-Female Triploid Species of Gecko and Karyological Data on the Bisexual Hemidactylus frenatus from Vietnam. Journal of Herpetology. 1984;18(3):277–84. 10.2307/1564081 . DOI

Moritz C. Parthenogenesis in the endemic australian lizard Heteronotia binoei (Gekkonidae). Science. 1983;220(4598):735–7. 10.1126/science.220.4598.735 . PubMed DOI

Moritz C. Parthenogenesis in the tropical gekkonid lizard, Nactus arnouxii (Sauria, Gekkonidae). Evolution. 1987;41(6):1252–66. 10.2307/2409091 . PubMed DOI

Rassmann K, Trillmich F, Tautz D. Hybridization between the Galapagos land and marine iguana (Conolophus subcristatus and Amblyrhynchus cristatus) on Plaza Sur . Journal of Zoology. 1997;242:729–39. .

Lücker H, Feiler A. Beobachtungen einer Paarung zwischen Meerechsen-Männchen (Amblyrhynchus cristatus) und Landleguan-Weibchen (Conolophus subcristatus) auf Plaza-Sur/Galapagos-Inseln sowie Beobachtungen an einem adulten Gattungshybriden (Amblyrhynchus x Conolophus). Elaphe. 2002;10:49–54.

Gutsche A, Köhler G. A fertile hybrid between Ctenosaura similis (Gray, 1831) and C. bakeri Stejneger, 1901 (Squamata: Iguanidae) on Isla de Utila, Honduras. Salamandra. 2004;40(3/4):201–6.

Breuil M. Taxon report: Lesser Antilles Iguana delicatissima and Iguana iguana . West Indian Iguana Specialist Group Newsletter. 2000;3(2):11–5.

Rykena S, Henke L. Bastardierung von Lacerta viridis und Lacerta agilis im Terrarium (Reptilia: Sauria:Lacertidae). Salamandra. 1978;14(3):147–52.

Rykena S. Kreuzungsexperimente zur Prüfung der Artgrenzen im Genus Lacerta sensu stricto. Mitt Zool Mus Berlin. 1991;67(1):55–68.

Rykena S. Experimental interspecific hybridization in the genus Lacerta . Israel Journal of Zoology. 1996;42(2):171–84. .

Rykena S. Experimental hybridization in Green Lizards (Lacerta s.str.), a tool to study species boundaries. Mertensiella. 2002;13:78–88.

Peek R. Morfologische en gedragsafwijkingen in een kruising tussen de Westelijke smaragdhagedis (Lacerta bilineata) en de Reuzensmaragdhagedis (Lacerta trilineata). Lacerta. 2009;67(6):251–4.

Capula M. Natural hybridization in Podarcis sicula and P. wagleriana (Reptilia: Lacertidae). Biochemical Systematics and Ecology. 1993;21(3):373–80. 10.1016/0305-1978(93)90028-P . DOI

Capula M. Genetic evidence of natural hybridization between Podarcis sicula and Podarcis tiliguerta (Reptilia: Lacertidae). Amphibia-Reptilia. 2002;23(3):313–21. 10.1163/15685380260449199 . DOI

Hoser R. Problems of python classification and hybrid pythons. Litteratura Serpentium. 1988;8(3):134–9.

Branch B, Erasmus H. Captive breeding of pythons in south Africa, including details of an interspecific hybrid (Python sebae natalensis x Python molurus bivittatus). Journal of the Herpetological Association of Africa. 1984;30:1–10.

LeClere JB, Hoaglund EP, Scharosch J, Smith CE, Gamble T. Two Naturally Occurring Intergeneric Hybrid Snakes (Pituophis catenifer sayi x Pantherophis vulpinus; Lampropeltini, Squamata) from the Midwestern United States. Journal of Herpetology. 2012;46(2):257–62. 10.1670/10-260 . DOI

Zinenko O. First generation hybrids between the Nikolsky's adder, Vipera nikolskii, and the common adder, Vipera berus (Reptilia, Serpentes, Viperidae). Vestnik Zoologii. 2003;37(1):101–4.

Zinenko O. New data about hybridization between Vipera nikolskii VEDMEDERYA, GRUBANT & RUDAEVA, 1986 and Vipera berus berus (LINNAEUS, 1758) and their contact zones in Ukraine. Mertensiella. 2004;15:17–28.

Frankham R. Conservation genetics. Annual Review of Genetics. 1995;29:305–27. 10.1146/annurev.ge.29.120195.001513 . PubMed DOI

Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, et al. Predicting the Probability of Outbreeding Depression. Conservation Biology. 2011;25(3):465–75. 10.1111/j.1523-1739.2011.01662.x . PubMed DOI

Lande R. Genetics and demography in biological conservation. Science. 1988;241(4872):1455–60. 10.1126/science.3420403 . PubMed DOI

Dobson AP, Lovejoy TE. Conservation and biodiversity: Scientific American Library Freeman^ eNew York; New York; 1996.

Frankham R, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, et al. Implications of different species concepts for conserving biodiversity. Biological Conservation. 2012;153:25–31. 10.1016/j.biocon.2012.04.034 . DOI

Anderson SC. The lizards of Iran: Society for the Study of Amphibians and Reptiles,[c/o] Cornell University, Department of Neurobiology and Behavior; 1999.

Mouthereau F. Timing of uplift in the Zagros belt/Iranian plateau and accommodation of late Cenozoic Arabia-Eurasia convergence. Geological Magazine. 2011;148(5–6):726–38. 10.1017/s0016756811000306 . DOI

Mouthereau F, Lacombe O, Verges J. Building the Zagros collisional orogen: Timing, strain distribution and the dynamics of Arabia/Eurasia plate convergence. Tectonophysics. 2012;532:27–60. 10.1016/j.tecto.2012.01.022 . DOI

Smit JHW, Cloetingh S, Burov E, Tesauro M, Sokoutis D, Kaban M. Interference of lithospheric folding in western Central Asia by simultaneous Indian and Arabian plate indentation. Tectonophysics. 2013;602:176–93. 10.1016/j.tecto.2012.10.032 . DOI

Macey JR, Schulte JA, Ananjeva NB, Larson A, Rastegar-Pouyani N, Shammakov SM, et al. Phylogenetic relationships among agamid lizards of the Laudakia caucasia species group: Testing hypotheses of biogeographic fragmentation and an area cladogram for the Iranian Plateau. Molecular Phylogenetics and Evolution. 1998;10(1):118–31. 10.1006/mpev.1997.0478 . PubMed DOI

Macey J, Schulte J, Kami H, Ananjeva N, Larson A, Papenfuss T. Testing hypotheses of vicariance in the agamid lizard Laudakia caucasia from mountain ranges on the Northern Iranian Plateau. Molecular Phylogenetics and Evolution. 2000;14(3):479–83. 10.1006/mpev.1999.0722 . PubMed DOI

Pouyani ER, Pouyani NR, Noureini SK, Joger U, Wink M. Molecular phylogeny of the Eremias persica complex of the Iranian plateau (Reptilia: Lacertidae), based on mtDNA sequences. Zoological Journal of the Linnean Society. 2010;158(3):641–60. 10.1111/j.1096-3642.2009.00553.x . DOI

Smid J, Frynta D. Genetic variability of Mesalina watsonana (Reptilia: Lacertidae) on the Iranian plateau and its phylogenetic and biogeographic affinities as inferred from mtDNA sequences. Acta Herpetologica. 2012;7(1):139–53. .

Flores D, Tousignant A, Crews D. Incubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius). Physiology & Behavior. 1994;55(6):1067–72. 10.1016/0031-9384(94)90389-1 . PubMed DOI

Huang V, Crews D. Differences induced by incubation temperature, versus androgen manipulation, in male leopard geckos (Eublepharis macularius) . Physiology & Behavior. 2012;107(1):121–4. 10.1016/j.physbeh.2012.06.014 . PubMed DOI

Rhen T, Sakata J, Zeller M, Crews D. Sex steroid levels across the reproductive cycle of female leopard geckos, Eublepharis macularius, from different incubation temperatures. General and Comparative Endocrinology. 2000;118(2):322–31. 10.1006/gcen.2000.7477 . PubMed DOI

Starostova Z, Kubicka L, Konarzewski M, Kozlowski J, Kratochvil L. Cell Size but Not Genome Size Affects Scaling of Metabolic Rate in Eyelid Geckos. American Naturalist. 2009;174(3):E100–E5. 10.1086/603610 . PubMed DOI

Starostova Z, Konarzewski M, Kozlowski J, Kratochvil L. Ontogeny of Metabolic Rate and Red Blood Cell Size in Eyelid Geckos: Species Follow Different Paths. Plos One. 2013;8(5):8 10.1371/journal.pone.0064715 . PubMed DOI PMC

LaDage L, Ferkin M. Male leopard geckos (Eublepharis macularius) can discriminate between two familiar females. Behaviour. 2006;143:1033–49. 10.1163/156853906778623644 . DOI

Landova E, Jancuchova-Laskova J, Musilova V, Kadochova S, Frynta D. Ontogenetic switch between alternative antipredatory strategies in the leopard gecko (Eublepharis macularius): defensive threat versus escape. Behavioral Ecology and Sociobiology. 2013;67(7):1113–22. 10.1007/s00265-013-1536-3 . DOI

Kratochvil L, Frynta D. Body size, male combat and the evolution of sexual dimorphism in eublepharid geckos (Squamata: Eublepharidae). Biological Journal of the Linnean Society. 2002;76(2):303–14. 10.1111/j.1095-8312.2002.tb02089.x . DOI

Kratochvil L, Frynta D. Body-size effect on egg size in eublepharid geckos (Squamata: Eublepharidae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal. Biological Journal of the Linnean Society. 2006;88(4):527–32. 10.1111/j.1095-8312.2006.00627.x . DOI

Seufer H, Kaverkin Y, Kirschner A, Boone J, Ernst T, Holfert T. The Eyelash Geckos: Care, Breeding and Natural History: Kirschner & Seufer Verlag; 2005.

Turelli M, Orr HA. Dominance, epistasis and the genetics of postzygotic isolation. Genetics. 2000;154(4):1663–79. . PubMed PMC

Frynta D, Moravec J, Cihakova J, Sadlo J, Hodkova Z, Kaftan M, et al. Results of the Czech Biological Expedition to Iran. Part 1. Notes on the distribution of amphibians and reptiles. Acta Societatis Zoologicae Bohemicae. 1997;61(1):3–17. .

Autumn K, Denardo DF. Behavioral termoregulation increases growth-rate in a nocturnal lizard. Journal of Herpetology. 1995;29(2):157–62. 10.2307/1564552 . DOI

Bull J, Gutzke W, Bulmer M. Nest choice in a captive lizard with temperature-dependent sex determination. Journal of Evolutionary Biology. 1988;1(2):177–84. 10.1046/j.1420-9101.1988.1020177.x . DOI

Bragg W, Fawcett J, Bragg T, Viets B. Nest-site selection in two eublepharid gecko species with temperature-dependent sex determination and one with genotypic sex determination. Biological Journal of the Linnean Society. 2000;69(3):319–32. 10.1111/j.1095-8312.2000.tb01208.x . DOI

Viets BE, Tousignant A, Ewert MA, Nelson CE, Crews D. Temperature-dependent sex determination in the leopard gecko, Eublepharis macularius . Journal of Experimental Zoology. 1993;265(6):679–83. 10.1002/jez.1402650610 . PubMed DOI

Kratochvil L, Fokt M, Rehak I, Frynta D. Misinterpretation of character scaling: a tale of sexual dimorphism in body shape of common lizards. Canadian Journal of Zoology-Revue Canadienne De Zoologie. 2003;81(6):1112–7. 10.1139/z03-078 . DOI

Frydlova P, Velensky P, Simkova O, Cikanova V, Hnizdo J, Rehak I, et al. Is body shape of mangrove-dwelling monitor lizards (Varanus indicus; Varanidae) sexually dimorphic? Amphibia-Reptilia. 2011;32(1):27–37. 10.1163/017353710X532184 . DOI

Somers KM. Multivariate Allometry and Removal of Size with Principal Components Analysis. Systematic Zoology. 1986;35(3):359–68. 10.2307/2413387 . DOI

Somers K. Allometry, Isometry and Shape in Principal Components Analysis. Systematic Zoology. 1989;38(2):169–73. 10.2307/2992386 . DOI

Thompson GG, Withers PC. Shape of Western Australian dragon lizards (Agamidae). Amphibia-Reptilia. 2005;26(1):73–85. 10.1163/1568538053693369 . DOI

Thompson GG, Withers PC. Size-free shape differences between male and female Western Australian dragon lizards (Agamidae). Amphibia-Reptilia. 2005;26(1):55–63. 10.1163/1568538053693332 . DOI

Thompson GG, Withers PC. The relationship between size-free body shape and choice of retreat for Western Australian Ctenophorus (Agamidae) dragon lizards. Amphibia-Reptilia. 2005;26(1):65–72. 10.1163/1568538053693323 . DOI

Glover KA, Kanda N, Haug T, Pastene LA, Oien N, Seliussen BB, et al. Hybrids between common and Antarctic minke whales are fertile and can back-cross. Bmc Genetics. 2013;14 10.1186/1471-2156-14-25 . PubMed DOI PMC

Zhang PJ, Han JB, Lu ZC, Chen RJ. Molecular Evidence of a Captive-Born Intergeneric Hybridization Between Bottlenose and Risso's Dolphins: Tursiops truncatus x Grampus griseus . Aquatic Mammals. 2014;40(1):5–8. 10.1578/am.40.1.2014.5 . DOI

Price T, Bouvier M. The evolution of F1 postzygotic incompatibilities in birds. Evolution. 2002;56(10):2083–9. . PubMed

Turelli M, Moyle LC. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics. 2007;176(2):1059–88. 10.1534/genetics.106.065979 . PubMed DOI PMC

Bolnick DI, Turelli M, Lopez-Fernandez H, Wainwright PC, Near TJ. Accelerated mitochondrial evolution and "Darwin's corollary": Asymmetric viability of reciprocal F1 hybrids in centrarchid fishes. Genetics. 2008;178(2):1037–48. 10.1534/genetics.107.081364 . PubMed DOI PMC

Arnold SJ, Verrell PA, Tilley SG. The evolution of asymmetry in sexual isolation: A model and a test case. Evolution. 1996;50(3):1024–33. 10.2307/2410643 . PubMed DOI

Devitt TJ, Baird SJE, Moritz C. Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone. Bmc Evolutionary Biology. 2011;11 10.1186/1471-2148-11-245 . PubMed DOI PMC

Robbins TR, Walker LE, Gorospe KD, Karl SA, Schrey AW, McCoy ED, et al. Rise and fall of a hybrid zone: Implications for the roles of aggression, mate choice, and secondary succession. Journal of Heredity. 2014;105(2):226–36. 10.1093/jhered/est093 . PubMed DOI

Sanchez-Guillen RA, Wullenreuther M, Rivera AC. Strong asymmetry in the relative strengths of prezygotic and postzygotic barriers between two damselfly sister species. Evolution. 2012;66(3):690–707. 10.1111/j.1558-5646.2011.01469.x . PubMed DOI

Berry OF. Inbreeding and promiscuity in the endangered grand skink. Conservation Genetics. 2006;7(3):427–37. 10.1007/s10592-005-9054-0 . DOI

Olsson M, Gullberg A, Tegelstrom H. Malformed offspring, sibling matings, and selection against inbreeding in the sand lizard (Lacerta agilis). Journal of Evolutionary Biology. 1996;9(2):229–42. 10.1046/j.1420-9101.1996.9020229.x . DOI

Wagner E. Temperature-dependent sex determination in a gekko lizard. Quarterly Review of Biology. 1980;55:21.

Bull JJ. Sex determination in reptiles. Quarterly Review of Biology. 1980;55(1):3–21. 10.1086/411613 . DOI

Bull JJ. Temperature-dependent sex determination in reptiles: validity of sex diagnosis in hatchling lizards. Canadian Journal of Zoology-Revue Canadienne De Zoologie. 1987;65(6):1421–4. .

Fitzpatrick BM, Shaffer HB. Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(40):15793–8. 10.1073/pnas.0704791104 . PubMed DOI PMC

Van der Sluijs I, Van Dooren T, Seehausen O, Van Alphen J. A test of fitness consequences of hybridization in sibling species of Lake Victoria cichlid fish. Journal of Evolutionary Biology. 2008;21(2):480–91. 10.1111/j.1420-9101.2007.01495.x . PubMed DOI

Fuller RC. Genetic incompatibilities in killifish and the role of environment. Evolution. 2008;62(12):3056–68. 10.1111/j.1558-5646.2008.00518.x . PubMed DOI

Pokorna M, Rabova M, Rab P, Ferguson-Smith M, Rens W, Kratochvil L. Differentiation of sex chromosomes and karyotypic evolution in the eye-lid geckos (Squamata: Gekkota: Eublepharidae), a group with different modes of sex determination. Chromosome Research. 2010;18(7):809–20. 10.1007/s10577-010-9154-7 . PubMed DOI

Haldane JBS. Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics. 1922;12(2):101–9.

Turelli M, Orr HA. The dominance theory of Haldane`s rule. Genetics. 1995;140(1):389–402. . PubMed PMC

Shine R, Phillips B, Waye H, Lemaster M, Mason RT. Species-isolating mechanisms in a mating system with male mate choice (garter snakes, Thamnophis spp.). Canadian Journal of Zoology-Revue Canadienne De Zoologie. 2004;82(7):1091–8. 10.1139/z04-086 . DOI

Placyk JS, Fitzpatrick BM, Casper GP, Small RS, Reynolds RG, Noble DWA, et al. Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction? Conservation Genetics. 2012;13(3):649–63. 10.1007/s10592-012-0315-4 . DOI

Pokorna M, Kratochvil L. Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zoological Journal of the Linnean Society. 2009;156(1):168–83. 10.1111/j.1096-3642.2008.00481.x . DOI

Baur B. Krötenechsen-Bastarde (Phrynosoma) (Sauria: Iguanidae). Salamandra. 1984;20(2/3):70–87.

Galán P. Hibridación en laboratorio de Podarcis bocagei y Podarcis carbonelli . Bol Asoc Herpetol Esp. 2002;13(1–2):28–31.

Kohler J, Hahn M, Kohler G. Divergent evolution of hemipenial morphology in two cryptic species of mainland anoles related to Anolis polylepis . Salamandra. 2012;48(1):1–11. .

Trobisch D, Glässer-Trobisch A. Ein Hybrid zwischen Lacerta pamphylica SCHMIDTLER, 1975 und Lacerta strigata EICHWALD, 1831. Die Eidechse. 2005;16(1):25–9.

Godinho R, Crespo EG, Ferrand N, Harris DJ. Phylogeny and evolution of the green lizards, Lacerta spp. (Squamata: Lacertidae) based on mitochondrial and nuclear DNA sequences. Amphibia-Reptilia. 2005;26(3):271–85. 10.1163/156853805774408667 . DOI

Watts PC, Buley KR, Boardman W, Ciofi C, Gibson O R. Parthenogenesis in komodo dragons. Nature. 2006;444(7122):1021–2. 10.1038/nature4441021a . PubMed DOI

Lampert KP. Facultative Parthenogenesis in Vertebrates: Reproductive Error or Chance? Sexual Development. 2008;2(6):290–301. 10.1159/000195678 . PubMed DOI

Neaves WB, Baumann P. Unisexual reproduction among vertebrates. Trends in Genetics. 2011;27(3):81–8. 10.1016/j.tig.2010.12.002 . PubMed DOI

Booth W, Smith CF, Eskridge PH, Hoss SK, Mendelson JR, Schuett GW. Facultative parthenogenesis discovered in wild vertebrates. Biology Letters. 2012;8(6):983–5. 10.1098/rsbl.2012.0666 . PubMed DOI PMC

Kinney ME, Wack RF, Grahn RA, Lyons L. Parthenogenesis in a Brazilian Rainbow Boa (Epicrates cenchria cenchria). Zoo Biology. 2013;32(2):172–6. 10.1002/zoo.21050 . PubMed DOI

Grabbe J, Koch A. First and repeated cases of parthenogenesis in the varanid subgenus Euprepiosaurus (Varanus indicus species group) and the first successful breeding of V. rainerguentheri in captivity. Biawak. 2014;8(2):79–87.

Robbins TR, Pruitt JN, Straub LE, McCoy ED, Mushinsky HR. Transgressive aggression in Sceloporus hybrids confers fitness through advantages in male agonistic encounters. Journal of Animal Ecology. 2010;79(1):137–47. 10.1111/j.1365-2656.2009.01594.x . PubMed DOI

Hiadlovska Z, Bimova BV, Mikula O, Pialek J, Macholan M. Transgressive segregation in a behavioural trait? Explorative strategies in two house mouse subspecies and their hybrids. Biological Journal of the Linnean Society. 2013;108(1):225–35. 10.1111/j.1095-8312.2012.01997.x . DOI

Nichols P, Genner MJ, van Oosterhout C, Smith A, Parsons P, Sungani H, et al. Secondary contact seeds phenotypic novelty in cichlid fishes. Proceedings of the Royal Society B-Biological Sciences. 2015;282(1798). 10.1098/rspb.2014.2272 . PubMed DOI PMC

Strasburg J, Kearney M. Phylogeography of sexual Heteronotia binoei (Gekkonidae) in the Australian arid zone: climatic cycling and repetitive hybridization. Molecular Ecology. 2005;14(9):2755–72. 10.1111/j.1365-294X.2005.02627.x . PubMed DOI

Garland T Jr., Losos JB. Ecological morphology of locomotor performance in squamate reptiles In: Wainwright PC, Reilly S, editors. Ecological Morphology: Integrative Organismal Biology. Chicago: University of Chicago Press; 1994. p. 240–302.

Vitt L, Caldwell J, Zani P, Titus T. The role of habitat shift in the evolution of lizard morphology: Evidence from tropical Tropidurus . Proceedings of the National Academy of Sciences of the United States of America. 1997;94(8):3828–32. 10.1073/pnas.94.8.3828 . PubMed DOI PMC

Herrel A, Meyers J, Vanhooydonck B. Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis. Biological Journal of the Linnean Society. 2001;74(3):305–14. 10.1006/bijl.2001.0579 . DOI

Kearney M, Shine R. Morphological and physiological correlates of hybrid parthenogenesis. American Naturalist. 2004;164(6):803–13. 10.1086/425986 . PubMed DOI

Kearney M, Wahl R, Autumn K. Increased capacity for sustained locomotion at low temperature in parthenogenetic geckos of hybrid origin. Physiological and Biochemical Zoology. 2005;78(3):316–24. 10.1086/430033 . PubMed DOI

Seehausen O. Hybridization and adaptive radiation. Trends in Ecology & Evolution. 2004;19(4):198–207. 10.1016/j.tree.2004.01.003 . PubMed DOI

A comparative study of growth: different body weight trajectories in three species of the genus Eublepharis and their hybrids