Proximate control of the development of sexual dimorphism is still hotly debated in reptiles. In some squamates, many male-typical exaggerated traits including body size were assumed to be controlled by masculinization by male gonadal androgens. We performed a manipulative experiment to test the importance of this mechanism in the development of pronounced sexual differences in body size and size of head casque in the chameleon Chamaeleo calyptratus. Castrated males attained male-typical body size highly deviating from the body size of control females. Ontogenetic allometries of casque size on head length revealed that sexes depart considerably in casque growth later in the ontogeny; however, castrated males still follow male-typical casque growth. Paradoxically, exogenous testosterone led in females to slight increase of casque size, which might reflect interference with the feminizing effects of female gonadal hormones. The results in males strongly suggest that masculinization by male gonadal androgens during growth is not required for the development of sexual dimorphism in body size and casque size in the chameleon. The ontogeny of sexually dimorphic body size and exaggerated traits in at least some squamates is likely controlled by other proximate mechanism, possibly by feminization by ovarian hormones.

Faculty of Science Charles University Department of Ecology Viničná 7 128 43 Prague 2 Czech Republic

Zobrazit více v PubMed

Kratochvíl L, Frynta D. Body size, male combat and the evolution of sexual dimorphism in eublepharid geckos (Squamata: Eublepharidae) Biol. J. Linn. Soc. Lond. 2002;76:303–314. doi: 10.1046/j.1095-8312.2002.00064.x. DOI

Cox RM, John-Alder HB. 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. doi: 10.1242/jeb.01948. PubMed DOI

Cox RM, Stenquist DS, Calsbeek R. Testosterone, growth and the evolution of sexual size dimorphism. J. Evol. Biol. 2009;22:1586–1598. doi: 10.1111/j.1420-9101.2009.01772.x. PubMed DOI

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. doi: 10.1111/j.1420-9101.2010.01933.x. PubMed DOI

Cox RM, Calsbeek R. Severe costs of reproduction persist in Anolis lizards despite the evolution of a single-egg clutch. Evolution. 2010;64:1321–1330. doi: 10.1111/j.1558-5646.2009.00851.x. PubMed DOI

Bonnet X, et al. Which proximate factor determines sexual size dimorphism in tiger snakes? Biol. J. Linn. Soc. 2011;103:668–680. doi: 10.1111/j.1095-8312.2011.01633.x. DOI

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

Adkins-Regan, E. Hormones and Animal Social Behavior. (Princeton University Press 2005).

Golinski A, Kubička L, John-Alder H, Kratochvíl L. Elevated testosterone is required for male copulatory behavior and aggression in Madagascar ground gecko (Paroedura picta) Gen. Comp. Endocrinol. 2014;205:133–141. doi: 10.1016/j.ygcen.2014.05.012. PubMed DOI

Rhen T, Ross J, Crews D. Effects of testosterone on sexual behavior and morphology in adult female leopard geckos, Eublepharis macularius. Horm. Behav. 1999;36:119–128. doi: 10.1006/hbeh.1999.1530. PubMed DOI

Cox, R. M., Skelly, S. L., Leo, A. & John-Alder, H. B. Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus. Copeia 597–608 (2005).

Schořálková T, Kratochvíl L, Kubička L. Female sexual attractiveness and sex recognition in leopard gecko: Males are indiscriminate courters. Horm. Behav. 2018;99:57–61. doi: 10.1016/j.yhbeh.2018.01.007. PubMed DOI

Schořálková T, Kratochvíl L, Kubička L. Temporal organization: A novel mechanism of hormonal control of male-typical sexual behavior in vertebrates. Physiol. Behav. 2017;170:151–156. doi: 10.1016/j.physbeh.2016.12.030. PubMed DOI

Schořálková T, Kratochvíl L, Kubička L. To fight or mate? Hormonal control of sex recognition, male sexual behavior and aggression in the gecko lizard. Horm. Behav. 2018;97:18–24. doi: 10.1016/j.yhbeh.2017.10.006. PubMed DOI

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. doi: 10.1242/jeb.079442. PubMed DOI

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. doi: 10.1016/j.ygcen.2015.09.028. PubMed DOI

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. doi: 10.1016/j.ygcen.2013.03.016. PubMed DOI

Pollock NB, Feigin S, Drazenovic M, John-Alder HB. Sex hormones and the development of sexual size dimorphism: 5α-dihydrotestosterone inhibits growth in a female-larger lizard (Sceloporus undulatus) J. Exp. Biol. 2017;220:4068–4077. doi: 10.1242/jeb.166553. PubMed DOI

Cox CL, Hanninen AF, Reedy AM, Cox RM. Female anoles retain responsiveness to testosterone despite the evolution of androgen-mediated sexual dimorphism. Funct. Ecol. 2015;29:758–767. doi: 10.1111/1365-2435.12383. DOI

Darwin, C. R. The descent of man and selection in relation to sex. (John Murray 1871).

Measey GJ, Hopkins K, Tolley KA. Morphology, ornaments and performance in two chameleon ecomorphs: is the casque bigger than the bite? Zool. 2009;112:217–226. doi: 10.1016/j.zool.2008.09.005. PubMed DOI

Rieppel O. The skull and jaw adductor musculature in chameleons. Rev. Suisse Zool. 1981;88:433–445. doi: 10.5962/bhl.part.82383. DOI

Ligon JD, Thornhill R, Zuk M, Johnson K. Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav. 1990;40:367–373. doi: 10.1016/S0003-3472(05)80932-7. DOI

Setchell JM, Jean Wickings E. Dominance, status signals and coloration in male mandrills (Mandrillus sphinx) Ethol. 2005;111:25–50. doi: 10.1111/j.1439-0310.2004.01054.x. DOI

Schmidt, W. Chamaeleo calyptratus, the Yemen Chameleon. (Natur und Tier – Verlag 2001).

Andrews RM, Donoghue S. Effects of temperature and moisture on embryonic diapause of the veiled chameleon (Chamaeleo calyptratus) J. Exp. Zool. Part. A. 2004;301:629–635. doi: 10.1002/jez.a.56. PubMed DOI

Andrews RM. Incubation temperature and sex ratio of the veiled chameleon (Chamaeleo calyptratus) J. Herpetol. 2005;39:515–518. doi: 10.1670/33-05N.1. DOI

Krysko K, Enge K, King F. The veiled chameleon Chamaeleo calyptratus: A new exotic lizard species in Florida. Fla. Scientist. 2004;67:249–253.

Kummrow MS, Gilman C, Mackie P, Smith DA, Mastromonaco GF. Noninvasive analysis of fecal reproductive hormone metabolites in female veiled chameleons (Chamaeleo calyptratus) by enzyme immunoassay. Zoo. Biol. 2010;30:95–115. PubMed

Diaz RE, Jr., et al. The veiled chameleon (Chamaeleo calyptratus Duméril and Duméril 1851): A model for studying reptile body plan development and evolution. Cold Spring Harb. Protoc. 2015;10:889–894. PubMed

Pinto, B. J. et al. The transcriptome of the veiled chameleon (Chamaeleo calyptratus): A resource for studying the evolution and development of vertebrates. Dev Dyn. 248, 702–708 (2019). PubMed

Andrews RM. Effects of incubation temperature on growth and performance of the veiled chameleon (Chamaeleo calyptratus) J. Exp. Zool. Part. A. 2008;309:435–446. doi: 10.1002/jez.470. PubMed DOI

Sosvorova L, Vitku J, Chlupacova T, Mohapl M, Hampl R. Determination of seven selected neuro- and immunomodulatory steroids in human cerebrospinal fluid and plasma using LC-MS/MS. Steroids. 2015;98:1–8. doi: 10.1016/j.steroids.2015.01.019. PubMed DOI

Sathyapalan T, et al. Androstenedione and testosterone levels correlate with in vitro fertilization rates in insulin-resistant women. BMJ Open. Diabetes Res. Care. 2017;5:e000387. doi: 10.1136/bmjdrc-2017-000387. PubMed DOI PMC

Hampl R, Putz Z, Stárka L. Radioimmunologic determination of dihydrotestosterone and its value in laboratory diagnosis (In Czech) Biochem. Clin. Bohemoslov. 1990;19:157–163.

St. Clair RC. Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination. Oecologia. 1998;115:501–507. doi: 10.1007/s004420050547. PubMed DOI

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. doi: 10.1111/j.1365-2435.2008.01518.x. DOI

Burnham KP, Anderson DR, Huyvaert KP. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 2011;65:23–35. doi: 10.1007/s00265-010-1029-6. DOI

Symonds MRE, 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. doi: 10.1007/s00265-010-1037-6. DOI

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/ (2013).

Norris, D. O. & Carr, J. A. Vertebrate endocrinology, 5 edition. (Academic Press 2013).

Zhou R, Bird IM, Dumesic DA, Abbott DH. Adrenal hyperandrogenism is induced by fetal androgen excess in a rhesus monkey model of polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 2005;90:6630–6637. doi: 10.1210/jc.2005-0691. PubMed DOI PMC

Massetti F, Gomes V, Perera A, Rato C, Kaliontzopoulou A. Morphological and functional implications of sexual size dimorphism in the Moorish gecko, Tarentola mauritanica. Biol. J. Linn. Soc. 2017;122:197–209. doi: 10.1093/biolinnean/blx060. DOI

Kratochvíl L, Flegr J. Differences in the 2nd to 4th digit length ratio in humans reflect shifts along the common allometric line. Biol. Lett. 2009;5:643–646. doi: 10.1098/rsbl.2009.0346. PubMed DOI PMC

Pélabon C, et al. On the relationship between ontogenetic and static allometry. Am. Nat. 2013;181:195–212. doi: 10.1086/668820. PubMed DOI

Nielsen SV, Banks JL, Diaz RE, Jr., Trainor PA, Gamble T. Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae) J. Evol. Biol. 2018;31:484–490. doi: 10.1111/jeb.13242. PubMed DOI

Rovatsos M, et al. Evolution of karyotypes in chameleons. Genes. 2017;8:382. doi: 10.3390/genes8120382. PubMed DOI PMC

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

Sex-specific growth arrest in a lizard