(1) In contrast to mammals and birds, reptiles have been considered as indeterminate growers, whose growth reflects differential allocation of resources to growth versus other energetically demanding processes such as reproduction. (2) We monitored the growth and activity of bone growth plates, hormonal profiles, and reproductive activity in males and females of the male-larger gecko Paroedura picta. We show that growth plates fuse in this species in a sex-specific manner. The more abrupt epiphyseal closure and more pronounced growth deceleration in females coincide with the increased activity of their reproductive organs. (3) We conclude that at least some lizards are determinate growers whose sexual size dimorphism is potentially driven by ovarian hormones. The major difference in growth between endothermic and ectothermic amniotes appears to be in the magnitude of growth before and after the first reproduction, not in the mechanistic processes such as senescence of growth plate cells.

Department of Ecology Faculty of Science Charles University Prague Viničná 7 128 44 Praha 2 Czech Republic

Institute of Histology and Embryology 1st Faculty of Medicine Charles University Albertov 4 128 00 Praha 2 Czech Republic

Zobrazit více v PubMed

Atkinson D. Temperature and organism size: a biological law for ectotherms. Adv. Ecol. Res. 1994;25:1–58.

Badyaev A.V. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol. Evol. 2002;17:369–378.

Bauerová A., Kratochvíl L., Kubička L. Little if any role of male gonadal androgens in ontogeny of sexual dimorphism in body size and cranial casque in chameleons. Sci. Rep. 2020;10:2673. PubMed PMC

Bryden M.M. Control of growth in two populations of elephant seals. Nature. 1968;217:1106–1108.

Burnham K.P., Anderson D.R., Huyvaert K.P. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 2011;65:23–35.

Case T.J. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q. Rev. Biol. 1978;53:243–282. PubMed

Castanet J., Newman D.G., Girons H.S. Skeletochronological data on the growth, age, and population structure of the tuatara, Sphenodon punctatus, on Stephens and Lady Alice Islands, New Zealand. Herpetologica. 1988;44:25–37.

Chagin A.S., Lindberg M.K., Andersson N., Moverare S., Gustafsson J.A., Sävendahl L., Ohlsson C. Estrogen receptor-beta inhibits skeletal growth and has the capacity to mediate growth plate fusion in female mice. J. Bone Mineral Res. 2004;19:72–77. PubMed

Charnov E.L., Turner T.F., Winemiller K.O. Reproductive constraints and the evolution of life histories with indeterminate growth. Proc. Natl. Acad. Sci. U S A. 2001;98:9460–9464. PubMed PMC

Cox R.M., Calsbeek R. Severe costs of reproduction persist in Anolis lizards despite the evolution of a single-egg clutch. Evolution. 2010;64:1321–1330. PubMed

Cox R.M., John-Alder H.B. Testosterone has opposite effects on male growth in lizards (Sceloporus spp.) with opposite patterns of sexual size dimorphism. J. Exp. Biol. 2005;208:4679–4687. PubMed

Cox R.M., Skelly S.L., John-Alder H.B. Testosterone inhibits growth in juvenile male eastern fence lizards (Sceloporus undulatus): implications for energy allocation and sexual size dimorphism. Physiol. Biochem. Zool. 2005;78:531–545. PubMed

Cox R.M., Stenquist D.S., Calsbeek R. Testosterone, growth and the evolution of sexual size dimorphism. J. Evol. Biol. 2009;22:1586–1598. PubMed

Cox R.M., Lovern M.B., Calsbeek R. Experimentally decoupling reproductive investment from energy storage to test the functional basis of a life-history trade-off. J. Anim. Ecol. 2014;83:888–898. PubMed

Cox R.M. A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow's spiny lizard Sceloporus jarrovii. J. Anim. Ecol. 2006;75:1361–1369. PubMed

Cutler G.B. The role of estrogen in bone growth and maturation during childhood and adolescence. J. Steroid Biochem. Mol. Biol. 1997;61:141–144. PubMed

de Buffrénil V., Ineich I., Böhme W. Comparative data on epiphyseal development in the family Varanidae. J. Herpetol. 2005;39:328–335.

de Ricqlès A.J., Padian K., Horner J.R., Lamm E.T., Myhrvold N. Osteohistology of Confuciusornis sanctus (theropoda: aves) J. Vertebr. Paleontol. 2003;23:373–386.

Duncan C.A., Cohick W.S., John-Alder H.B. Testosterone reduces growth and hepatic IGF-1 mRNA in a female-larger lizard, Sceloporus undulatus: evidence of an evolutionary reversal in growth regulation. Integr. Organismal. Biol. 2020;2:obaa036. PubMed PMC

Frýdlová P., Nutilová V., Dudák J., Žemlička J., Němec P., Velenský P., Jirásek T., Frynta D. Patterns of growth in monitor lizards (Varanidae) as revealed by computed tomography of femoral growth plates. Zoomorphology. 2017;136:95–106.

Frýdlová P., Mrzílková J., Šeremeta M., Křemen J., Dudák J., Žemlička J., Němec P., Velenský P., Moravec J., Koleška D., et al. Universality of indeterminate growth in lizards rejected: the micro-CT reveals contrasting timing of growth cartilage persistence in iguanas, agamas, and chameleons. Sci. Rep. 2019;9:18913. PubMed PMC

Frýdlová P., Mrzílková J., Šeremeta M., Křemen J., Dudák J., Žemlička J., Minnich B., Kverková K., Němec P., Zach P., Frynta D. Determinate growth is predominant and likely ancestral in squamate reptiles. Proc. R. Soc. B Biol. Sci. 2020;287:20202737. PubMed PMC

Frynta D., Frýdlová P., Hnízdo J., Simková O., Cikánová V., Velenský P. Ontogeny of sexual size dimorphism in monitor lizards: males grow for a longer period, but not at a faster rate. Zool. Sci. 2010;27:917–923. PubMed

Geiger M., Forasiepi A.M., Koyabu D., Sánchez-Villagra M.R. Heterochrony and post-natal growth in mammals – an examination of growth plates in limbs. J. Evol. Biol. 2014;27:98–115. PubMed

Hampl R. In: Advances in Steroid Analysis '93. Görög S., editor. Akadémiai Kiadó; 1994. Comparison of three immunoassays for testosterone determination; pp. 163–169.

Klein N., Scheyer T., Tütken T. Skeletochronology and isotopic analysis of a captive individual of Alligator mississippiensis Daudin, 1802. Fossil Rec. 2009;12:121–131.

Kratochvíl L., Frynta D. Body size, male combat and the evolution of sexual dimorphism in eublepharid geckos (Squamata: Eublepharidae) Biol. J. Linn. Soc. 2002;76:303–314.

Kratochvíl L., Kubička L. Why reduce clutch size to one or two eggs? Reproductive allometries reveal different evolutionary causes of invariant clutch size in lizards. Funct. Ecol. 2007;21:171–177.

Kubička L., Kratochvíl L. First grow, then breed and finally get fat: hierarchical allocation to life-history traits in a lizard with invariant clutch size. Funct. Ecol. 2009;23:595–601.

Kubička L., Golinski A., John-Alder H., Kratochvíl L. Ontogeny of pronounced female-biased sexual size dimorphism in the Malaysian cat gecko (Aeluroscalabotes felinus: squamata: Eublepharidae): a test of the role of testosterone in growth regulation. Gen. Comp. Endocrinol. 2013;188:183–188. PubMed

Kubička L., Starostová Z., Kratochvíl L. Endogenous control of sexual size dimorphism: gonadal androgens have neither direct nor indirect effect on male growth in a Madagascar ground gecko (Paroedura picta) Gen. Comp. Endocrinol. 2015;224:273–277. PubMed

Kubička L., Schořálková T., Červenka J., Kratochvíl L. Ovarian control of growth and sexual size dimorphism in a male-larger gecko. J. Exp. Biol. 2017;220:787–795. PubMed

Martin T., Thorbek P., Ashauer R. Common ground between growth models of rival theories: a useful illustration for beginners. Ecol. Model. 2019;407:108712.

Meiri S. Evolution and ecology of lizard body sizes. Glob. Ecol. Biogeogr. 2008;17:724–734.

Meter B., Starostová Z., Kubička L., Kratochvíl L. The limits of the energetical perspective: life-history decisions in lizard growth. Evol. Ecol. 2020;34:469–481.

Myhrvold N.P. Revisiting the estimation of dinosaur growth rates. PLoS One. 2013;8:e81917. PubMed PMC

Nilsson O., Marino R., de Luca F., Phillip M., Baron J. Endocrine regulation of the growth plate. Horm. Res. 2005;64:157–165. PubMed

Nilsson O., Weise M., Landman E.B., Meyers J.L., Barnes K.M., Baron J. Evidence that estrogen hastens epiphyseal fusion and cessation of longitudinal bone growth by irreversibly depleting the number of resting zone progenitor cells in female rabbits. Endocrinology. 2014;155:2892–2899. PubMed PMC

Oosterbaan R.J. SegReg software. 2011. https://www.waterlog.info/segreg.htm

Peters R. Cambridge University Press; 1983. The Ecological Implications of Body Size (Cambridge Studies in Ecology)

R Core Team . R Foundation for Statistical Computing; 2021. R: A Language and Environment for Statistical Computing.https://www.R-project.org/

Ricklefs R.E. Patterns of growth in birds. Ibis. 1968;110:419–451.

Shohoji T., Sasaki H. An aspect of growth analysis of weight in savannah baboon. II. Gender comparison by adjusting age. Growth. 1987;51:425–431. PubMed

Sibly R.M., Brown J.H. Toward a physiological explanation of juvenile growth curves. J. Zool. 2020;311:286–290.

St Clair R.C. Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination. Oecologia. 1998;115:501–507. PubMed

Stamps J.A. Sexual size dimorphism in species with asymptotic growth after maturity. Biol. J. Linn. Soc. 1993;50:123–145.

Starostová Z., Kubička L., Kratochvíl L. Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature-induced variation. J. Evol. Biol. 2010;23:670–677. PubMed

Starostová Z., Angilletta M.J., Kubička L., Kratochvíl L. Thermal dependence of reproductive allocation in a tropical lizard. J. Therm. Biol. 2012;37:159–163.

Starostová Z., Kubička L., Golinski A., Kratochvíl L. Neither male gonadal androgens nor female reproductive costs drive development of sexual size dimorphism in lizards. J. Exp. Biol. 2013;216:1872–1880. PubMed

StatSoft, Inc. (2011). STATISTICA (Data Analysis Software System), Version 10. http://www.statsoft.com.

Symonds M.R.E., Moussalli A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav. Ecol. Sociobiol. 2010;65:13–21.

Taylor E.N., Denardo D.F. Sexual size dimorphism and growth plasticity in snakes: an experiment on the Western Diamond-backed Rattlesnake (Crotalus atrox) J. Exp. Zool. A Comp. Exp. Biol. 2005;303:598–607. PubMed

Twigg G.I. Studies on Holochilus sciureus berbicensis, a cricetine rodent from the coastal region of British Guiana. J. Zool. 1965;145:263–283.

Vitt L.J., Caldwell J.P. Fourth edition. Academic Press; 2014. Herpetology: An Introductory Biology of Amphibians and Reptiles.

von Bertalanffy L. Quantitative laws in metabolism and growth. Q. Rev. Biol. 1957;32:217–231. PubMed

Weise M., De-Levi S., Barnes K.M., Gafni R.I., Abad V., Baron J. Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc. Natl. Acad. Sci. U S A. 2001;98:6871–6876. PubMed PMC

West G.B., Brown J.H., Enquist B.J. A general model for ontogenetic growth. Nature. 2001;413:628–631. PubMed

Woodward H.N., Horner J.R., Farlow J.O. Osteohistological evidence for determinate growth in the American alligator. J. Herpetol. 2011;45:339–342.

Catch-up growth and overweight adults in the offspring of young gecko mothers resembling low birth weight infants

Development of male-larger sexual size dimorphism in a lizard: IGF1 peak long after sexual maturity overlaps with pronounced growth in males