The prevalence of environmental sex determination (ESD) in squamate reptiles is often overestimated in the literature. This is surprising because we have reliable data demonstrating ESD in only a few species. The documentation of ESD in three species of geckos presented here has significantly increased our knowledge, given that satisfactory evidence for ESD existed in only eight other gecko species. For the first time, we document the occurrence of ESD in the family Sphaerodactylidae. Our finding of unexpected variability in the shapes of reaction norms among geckos highlights that traditional descriptions using parameters such as pivotal temperature, that is, temperature producing a 50:50 sex ratio, are unsatisfactory. For example, the gecko Pachydactylus tigrinus lacks any pivotal temperature and its sex ratios are strongly female-biased across the entire range of viable temperatures. We argue for the effective capture of the relationship between temperature and sex ratio using specific nonlinear models rather than using classical simplistic descriptions and classifications of reaction norms.

Department of Ecology Faculty of Science Charles University Prague Czech Republic

See more in PubMed

Anderson, A., & Oldham, C. (1988). Captive husbandry and propagation of the African fat‐tail gecko, Hemitheconyx caudicinctus. Tenth International Herpetological Symposium on Captive Propagsyion and Husbandry (pp. 75–85).

Andrews, R. M. (2015). Rigid shells enhance survival of gekkotan eggs. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 323, 607–615.

Augstenová, B., Pensabene, E., Veselý, M., Kratochvíl, L., & Rovatsos, M. (2021). Are geckos special in sex determination? Independently evolved differentiated ZZ/ZW sex chromosomes in carphodactylid geckos. Genome Biology and Evolution, 13, evab119.

Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67, 1–48.

Baudat, F., de Massy, B., & Veyrunes, F. (2019). Sex chromosome quadrivalents in oocytes of the African pygmy mouse Mus minutoides that harbors non‐conventional sex chromosomes. Chromosoma, 128, 397–411.

Beardmore, J. A., Mair, G. C., & Lewis, R. I. (2001). Monosex male production in finfish as exemplified by tilapia: Applications, problems, and prospects. Aquaculture, 197, 283–301.

Bókony, V., Milne, G., Pipoly, I., Székely, T., & Liker, A. (2019). Sex ratios and bimaturism differ between temperature‐dependent and genetic sex‐determination systems in reptiles. BMC Evolutionary Biology, 19, 57.

Bright Ross, J. G., Newman, C., Buesching, C. D., & Macdonald, D. W. (2020). What lies beneath? Population dynamics conceal pace‐of‐life and sex ratio variation, with implications for resilience to environmental change. Global Change Biology, 26, 3307–3324.

Budzinski, M. R. (1999). Induktion des männlichen Geschlechts bei Geckos der Gattung Phelsuma durch tägliche kurzzeitige Inkubation bei hoher Temperatur. Sauria, 21, 43–46.

Bull, J. J. (1983). Evolution of sex determining mechanisms. The Benjamin/Cummings Publishing Company, Inc.

Bull, J. J. (1987). Temperature‐dependent sex determination in reptiles: Validity of sex diagnosis in hatchling lizards. Canadian Journal of Zoology, 65, 1421–1424.

Burger, J., & Zappalorti, R. T. (1988). Effects of incubation temperature on sex ratios in pine snakes: Differential vulnerability of males and females. The American Naturalist, 132, 492–505.

Burnham, K. P., Anderson, D. R., & Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behavioral Ecology and Sociobiology, 65, 23–35.

Butka, E. G., & Freedberg, S. (2019). Population structure leads to male‐biased population sex ratios under environmental sex determination. Evolution, 73, 99–110.

Carter, A. L., Bodensteiner, B. L., Iverson, J. B., Milne‐Zelman, C. L., Mitchell, T. S., Refsnider, J. M., Warner, D. A., & Janzen, F. J. (2019). Breadth of the thermal response captures individual and geographic variation in temperature‐dependent sex determination. Functional Ecology, 33, 1928–1939.

Carter, A. W., Sadd, B. M., Tuberville, T. D., Paitz, R. T., & Bowden, R. M. (2018). Short heatwaves during fluctuating incubation regimes produce females under temperature‐dependent sex determination with implications for sex ratios in nature. Scientific Reports, 8, 3.

Charnier, M. (1966). Action de la température sur la sex‐ratio chezl'embryon d'Agama agama (Agamidae, Lacertilien). Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales, 160, 620–622.

Charnov, E. L., & Bull, J. J. (1989). Non‐Fisherian sex ratios with sex change and environmental sex determination. Nature, 338, 148–150.

Core Team, R. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing.

Crowther, C., Bonser, S. P., & Schwanz, L. E. (2024). Plasticity and the adaptive evolution of switchlike reaction norms under environmental change. Evolution Letter, 8, 64–75.

Darwin, C. (1888). The descent of man and selection in relation to sex. John Murray.

Deeming, D. C., & Ferguson, M. W. J. (1989). The mechanism of temperature dependent sex determination in crocodilians: A hypothesis. American Zoologist, 29, 973–985.

Deveson, I. W., Holleley, C. E., Blackburn, J., Marshall Graves, J. A., Mattick, J. S., Waters, P. D., & Georges, A. (2017). Differential intron retention in Jumonji chromatin modifier genes is implicated in reptile temperature‐dependent sex determination. Science Advances, 3, 1700731.

Ewert, M. A., Lang, J. W., & Nelson, C. E. (2005). Geographic variation in the pattern of temperature‐dependent sex determination in the American snapping turtle (Chelydra serpentina). Journal of Zoology, 265, 81–95.

Fisher, R. A. (1930). The genetical theory of natural selection. Clarendon.

Gamble, T. (2010). A review of sex determining mechanisms in geckos (Gekkota: Squamata). Sexual Development, 4, 88–103.

Gamble, T., Coryell, J., Ezaz, T., Lynch, J., Scantlebury, D. P., & Zarkower, D. (2015). Restriction site‐associated DNA sequencing (RAD‐seq) reveals an extraordinary number of transitions among gecko sex‐determining systems. Molecular Biology and Evolution, 32, 1296–1309.

Gardner, A. S. (2009). Two new gecko species records for the United Arab Emirates: Pristurus carteri (Gray, 1863) and Hemidactylus persicus (Anderson, 1872). Tribulus, 18, 18.

Ge, C., Ye, J., Weber, C., Sun, W., Zhang, H., Zhou, Y., Cai, C., Qian, G., & Capel, B. (2018). The histone demethylase KDM6B regulates temperature‐dependent sex determination in a turtle species. Science, 360, 645–648.

Georges, A., Beggs, K., Young, J. E., & Doody, J. S. (2005). Modelling development of reptile embryos under fluctuating temperature regimes. Physiological and Biochemical Zoology, 78, 18–30.

González, E. J., Martínez‐López, M., Morales‐Garduza, M. A., García‐Morales, R., Charruau, P., & Gallardo‐Cruz, J. A. (2019). The sex‐determination pattern in crocodilians: A systematic review of three decades of research. Journal of Animal Ecology, 88, 1417–1427.

Hamilton, W. D. (1967). Extraordinary sex ratios: A sex‐ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science, 156, 477–488.

Harlow, P. S., & Harlow, M. F. (1997). Captive reproduction and longevity in the eastern water dragon (Physignathus lesueurii). Herpetofauna, 27, 14–19.

Harlow, P. S., & Shine, R. (1999). Temperature‐dependent sex determination in the frillneck lizard, Chlamydosaurus kingii (Agamidae). Herpetologica, 55, 205–212.

Harlow, P. S., & Taylor, J. E. (2000). Reproductive ecology of the jacky dragon (Amphibolurus muricatus): An agamid lizard with temperature‐dependent sex determination. Austral Ecology, 25, 640–652.

Hartig, F. (2022). DHARMa: Residual diagnostics for hierarchical (multi‐level/mixed) regression models. R package version 0.4.6. http://florianhartig.github.io/DHARMa/

Hastie, T. (2011). Gam: Generalized additive models. R package version 1.06.2.

Heredero Saura, L., Jáñez‐Escalada, L., López Navas, J., Cordero, K., & Santidrián Tomillo, P. (2022). Nest‐site selection influences offspring sex ratio in green turtles, a species with temperature‐dependent sex determination. Climatic Change, 170, 39.

Holleley, C. E., O'Meally, D., Sarre, S. D., Marshall Graves, J. A., Ezaz, T., Matsubara, K., Azad, B., Zhang, X., & Georges, A. (2015). Sex reversal triggers the rapid transition from genetic to temperature‐dependent sex. Nature, 523, 79–82.

Iannucci, A., Altmanová, M., Ciofi, C., Ferguson‐Smith, M., Milan, M., Pereira, J. C., Pether, J., Rehák, I., Rovatsos, M., Stanyon, R., Velenský, P., Ráb, P., Kratochvíl, L., & Johnson Pokorná, M. (2019). Conserved sex chromosomes and karyotype evolution in monitor lizards (Varanidae). Heredity, 123, 215–227.

IUCN (International Union for Conservation of Nature). (2023a). Pachydactylus tigrinus (spatial data). The IUCN Red List of Threatened Species 2023(1). Retrieved December 21, 2023, from https://www.iucnredlist.org

IUCN (International Union for Conservation of Nature). (2023b). Chondrodactylus laevigatus (spatial data). The IUCN Red List of Threatened Species 2023(1). Retrieved December 21, 2023, from https://www.iucnredlist.org

Kappeler, P. M., Benhaiem, S., Fichtel, C., Fromhage, L., Höner, O. P., Jennions, M. D., Kaiser, S., Krüger, O., Schneider, J. M., Tuni, C., van Schaik, J., & Goymann, W. (2022). Sex roles and sex ratios in animals. Biological Reviews, 98, 462–480.

Kato, M., Takehana, Y., Sakaizumi, M., & Hamaguchi, S. (2010). A sex‐determining region on the Y chromosome controls the sex‐reversal ratio in interspecific hybrids between Oryzias curvinotus females and Oryzias latipes males. Heredity, 104, 191–195.

Kobayashi, K., & Hasegawa, E. (2016). A female‐biased sex ratio reduces the twofold cost of sex. Scientific Reports, 6, 23982.

Kobayashi, K., Hasegawa, E., Yamamoto, Y., Kawatsu, K., Vargo, E. L., Yoshimura, J., & Matsuura, K. (2013). Sex ratio biases in termites provide evidence for kin selection. Nature Communications, 4, 2048.

Kostmann, A., Kratochvíl, L., & Rovatsos, M. (2021). Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proceedings of the Royal Society B: Biological Sciences, 288, 20202139.

Krueger, C. J., & Janzen, F. J. (2023). On the origin of patterns of temperature‐dependent sex determination. Evolution, 77, 1091–1100.

Langerwerf, B. (1983). Über die Haltung und Zucht von Agama caucasia (EICHWALD, 1831) (Sauria: Agamidae), nebst Bemerkungen zur erfolgreichen Zucht weiterer palaearktischer Echsen. Salamandra, 19, 11–12.

Lolavar, A., & Wyneken, J. (2020). The impact of sand moisture on the temperature‐sex ratio responses of developing loggerhead (Caretta caretta) sea turtles. Zoology, 138, 125739.

Marques, V., Riaño, G., Carretero, M. A., Silva‐Rocha, I., & Rato, C. (2023). Sex determination and optimal development in the Moorish gecko, Tarentola mauritanica. Acta Zoologica, 104, 419–433.

Mezzasalma, M., Guarino, F. M., & Odierna, G. (2021). Lizards as model organisms of sex chromosome evolution: What we really know from a systematic distribution of available data? Genes, 12, 1341.

Mitchell, N. J., Nelson, N. J., Cree, A., Pledger, S., Keall, S. N., & Daugherty, C. H. (2006). Support for a rare pattern of temperature‐dependent sex determination in archaic reptiles: Evidence from two species of tuatara (Sphenodon). Frontiers in Zoology, 3, 9.

Mrosovsky, N., & Pieau, C. (1991). Transitional range of temperature, pivotal temperatures and thermosensitive stages for sex determination in reptiles. Amphibia‐Reptilia, 12, 169–179.

Nettmann, H. K., & Rykena, S. (1985). Verhaltens‐und fortpflanzungsbiologische Notizen über kanarische und nordafrikanische Tarentola‐Arten. Bonner Zoologische Beitraege, 36, 287–305.

Organ, C. L., & Janes, D. E. (2008). Evolution of sex chromosomes in Sauropsida. Integrative and Comparative Biology, 48, 512–519.

Pawluk, J. J., & Zagalska‐Neubauer, M. (2024). Paternal influences over offspring sex ratio in mammals–tested hypotheses and potential mechanisms. Mammal Review, 54, 78–91.

Pensabene, E., Yurchenko, A., Kratochvíl, L., & Rovatsos, M. (2023). Madagascar leaf‐tail geckos (Uroplatus spp.) share independently evolved differentiated ZZ/ZW sex chromosomes. Cells, 12, 260.

Pieau, C. (1996). Temperature variation and sex determination in reptiles. BioEssays, 18, 19–26.

Pinto, B. J., Keating, S. E., Nielsen, S. V., Scantlebury, D. P., Daza, J. D., & Gamble, T. (2022). Chromosome‐level genome assembly reveals dynamic sex chromosomes in neotropical leaf‐litter geckos (Sphaerodactylidae: Sphaerodactylus). Journal of Heredity, 113, 272–287.

Pokorná, M., & Kratochvíl, L. (2009). Phylogeny of sex‐determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap? Zoological Journal of the Linnean Society, 156, 168–183.

Pokorná, M. J., & Kratochvíl, L. (2016). What was the ancestral sex‐determining mechanism in amniote vertebrates? Biological Reviews, 91, 1–12.

Pruginin, Y., Rothbard, S., Wohlfarth, G., Halevy, A., Moav, R., & Hulata, G. (1975). All‐male broods of Tilapia nilotica × T. aurea hybrids. Aquaculture, 6, 11–21.

Pyron, R., Burbrink, F. T., & Wiens, J. J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93.

Rovatsos, M., Altmanová, M., Augstenová, B., Mazzoleni, S., Velenský, P., & Kratochvíl, L. (2019). ZZ/ZW sex determination with multiple neo‐sex chromosomes is common in Madagascan chameleons of the genus Furcifer (Reptilia: Chamaeleonidae). Genes, 10, 1020.

Rovatsos, M., Vukić, J., Mrugała, A., Suwala, G., Lymberakis, P., & Kratochvíl, L. (2019). Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards. Scientific Reports, 9, 7832.

Seipp, R., & Henkel, F. W. (2000). Rhacodactylus: Biology, natural history & husbandry. Edition Chimaira.

Shine, R. (1999). Why is sex determined by nest temperature in many reptiles? Trends in Ecology & Evolution, 14, 186–189.

Simoncini, M. S., Cruz, F. B., Larriera, A., & Piña, C. I. (2014). Effects of climatic conditions on sex ratios in nests of broad‐snouted caiman. Journal of Zoology, 293, 243–251.

Smith, J. M., & Maynard‐Smith, J. (1978). The evolution of sex. Cambridge University Press.

Steele, A. L., Wibbels, T., & Warner, D. A. (2018). Revisiting the first report of temperature‐dependent sex determination in a vertebrate, the African redhead agama. Journal of Zoology, 306, 16–22.

Tokunaga, S. (1985). Temperature‐dependent sex determination in Gekko japonicus (Gekkonidae, Reptilia). Development, Growth & Differentiation, 27, 117–120.

Toni, P., Forsyth, D. M., & Festa‐Bianchet, M. (2021). Determinants of offspring sex in kangaroos: A test of multiple hypotheses. Behavioral Ecology, 32, 297–305.

Uetz, P., Freed, P., Aguilar, R., Reyes, F., & Hošek, J. (Eds.) (2023). The reptile database. http://www.reptile-database.org

Valenzuela, N., & Lance, V. (Eds.). (2004). Temperature‐dependent sex determination in vertebrates. Smithsonian Books.

Viets, B. E., Ewert, M. A., Talent, L. G., & Nelson, C. E. (1994). Sex‐determining mechanisms in squamate reptiles. Journal of Experimental Zoology, 270, 45–56.

Viets, B. E., Tousignant, A., Ewert, M. A., Nelson, C. E., & Crews, D. (1993). Temperature‐dependent sex determination in the leopard gecko, Eublepharis macularius. Journal of Experimental Zoology, 265, 679–683.

Whiteley, S. L., Castelli, M. A., Dissanayake, D. S., Holleley, C. E., & Georges, A. (2021). Temperature‐induced sex reversal in reptiles: Prevalence, discovery, and evolutionary implications. Sexual Development, 15, 148–156.

Whiteley, S. L., Georges, A., Weisbecker, V., Schwanz, L. E., & Holleley, C. E. (2021). Ovotestes suggest cryptic genetic influence in a reptile model for temperature‐dependent sex determination. Proceedings of the Royal Society B, 288, 20202819.

Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer‐Verlag.

Yntema, C. L., & Mrosovsky, N. (1982). Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Canadian Journal of Zoology, 60, 1012–1016.

Yoshida, M. C., & Itoh, M. (1974). Karyotype of the gecko, Gekko japonicus. Chromosome Research, 17, 29–31.

Environmental (and Random?) Sex Determination in Endangered and Invasive Phelsuma Geckos