Little if any role of male gonadal androgens in ontogeny of sexual dimorphism in body size and cranial casque in chameleons.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
14 02 2020
Historique:
received: 11 10 2019
accepted: 30 01 2020
entrez: 16 2 2020
pubmed: 16 2 2020
medline: 18 11 2020
Statut: epublish

Résumé

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.

Identifiants

pubmed: 32060387
doi: 10.1038/s41598-020-59501-6
pii: 10.1038/s41598-020-59501-6
pmc: PMC7021717
doi:

Substances chimiques

Androgens 0
Testosterone 3XMK78S47O

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2673

Références

Kratochvíl, L. & Frynta, D. Body size, male combat and the evolution of sexual dimorphism in eublepharid geckos (Squamata: Eublepharidae). Biol. J. Linn. Soc. Lond. 76, 303–314 (2002).
doi: 10.1046/j.1095-8312.2002.00064.x
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. 208, 4679–4687 (2005).
pubmed: 16326949 doi: 10.1242/jeb.01948 pmcid: 16326949
Cox, R. M., Stenquist, D. S. & Calsbeek, R. Testosterone, growth and the evolution of sexual size dimorphism. J. Evol. Biol. 22, 1586–1598 (2009).
pubmed: 19549143 doi: 10.1111/j.1420-9101.2009.01772.x pmcid: 19549143
Starostová, Z., Kubička, L. & Kratochvíl, L. Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature-induced variation. J. Evol. Biol. 23, 670–677 (2010).
pubmed: 20487136 doi: 10.1111/j.1420-9101.2010.01933.x pmcid: 20487136
Cox, R. M. & Calsbeek, R. Severe costs of reproduction persist in Anolis lizards despite the evolution of a single-egg clutch. Evolution 64, 1321–1330 (2010).
pubmed: 19930451 doi: 10.1111/j.1558-5646.2009.00851.x pmcid: 19930451
Bonnet, X. et al. Which proximate factor determines sexual size dimorphism in tiger snakes? Biol. J. Linn. Soc. 103, 668–680 (2011).
doi: 10.1111/j.1095-8312.2011.01633.x
Kubička, L., Schořálková, T., Červenka, J. & Kratochvíl, L. Ovarian control of growth and sexual size dimorphism in a male-larger gecko. J. Exp. Biol. 220, 787–795 (2017).
pubmed: 27956485 pmcid: 27956485
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. 205, 133–141 (2014).
pubmed: 24852349 doi: 10.1016/j.ygcen.2014.05.012 pmcid: 24852349
Rhen, T., Ross, J. & Crews, D. Effects of testosterone on sexual behavior and morphology in adult female leopard geckos, Eublepharis macularius. Horm. Behav. 36, 119–128 (1999).
pubmed: 10506536 doi: 10.1006/hbeh.1999.1530 pmcid: 10506536
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. 99, 57–61 (2018).
pubmed: 29408690 doi: 10.1016/j.yhbeh.2018.01.007 pmcid: 29408690
Schořálková, T., Kratochvíl, L. & Kubička, L. Temporal organization: A novel mechanism of hormonal control of male-typical sexual behavior in vertebrates. Physiol. Behav. 170, 151–156 (2017).
pubmed: 28025090 doi: 10.1016/j.physbeh.2016.12.030 pmcid: 28025090
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. 97, 18–24 (2018).
pubmed: 29037971 doi: 10.1016/j.yhbeh.2017.10.006 pmcid: 29037971
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. 216, 1872–1880 (2013).
pubmed: 23393279 doi: 10.1242/jeb.079442 pmcid: 23393279
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. 224, 273–277 (2015).
pubmed: 26431613 doi: 10.1016/j.ygcen.2015.09.028 pmcid: 26431613
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. 188, 183–188 (2013).
pubmed: 23545460 doi: 10.1016/j.ygcen.2013.03.016 pmcid: 23545460
Pollock, N. B., Feigin, S., Drazenovic, M. & John-Alder, H. B. Sex hormones and the development of sexual size dimorphism: 5α-dihydrotestosterone inhibits growth in a female-larger lizard (Sceloporus undulatus). J. Exp. Biol. 220, 4068–4077 (2017).
pubmed: 28912255 doi: 10.1242/jeb.166553 pmcid: 28912255
Cox, C. L., Hanninen, A. F., Reedy, A. M. & Cox, R. M. Female anoles retain responsiveness to testosterone despite the evolution of androgen-mediated sexual dimorphism. Funct. Ecol. 29, 758–767 (2015).
doi: 10.1111/1365-2435.12383
Darwin, C. R. The descent of man and selection in relation to sex. (John Murray 1871).
Measey, G. J., Hopkins, K. & Tolley, K. A. Morphology, ornaments and performance in two chameleon ecomorphs: is the casque bigger than the bite? Zool. 112, 217–226 (2009).
doi: 10.1016/j.zool.2008.09.005
Rieppel, O. The skull and jaw adductor musculature in chameleons. Rev. Suisse Zool. 88, 433–445 (1981).
doi: 10.5962/bhl.part.82383
Ligon, J. D., Thornhill, R., Zuk, M. & Johnson, K. Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav. 40, 367–373 (1990).
doi: 10.1016/S0003-3472(05)80932-7
Setchell, J. M. & Jean Wickings, E. Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethol. 111, 25–50 (2005).
doi: 10.1111/j.1439-0310.2004.01054.x
Schmidt, W. Chamaeleo calyptratus, the Yemen Chameleon. (Natur und Tier – Verlag 2001).
Andrews, R. M. & Donoghue, S. Effects of temperature and moisture on embryonic diapause of the veiled chameleon (Chamaeleo calyptratus). J. Exp. Zool. Part. A 301, 629–635 (2004).
doi: 10.1002/jez.a.56
Andrews, R. M. Incubation temperature and sex ratio of the veiled chameleon (Chamaeleo calyptratus). J. Herpetol. 39, 515–518 (2005).
doi: 10.1670/33-05N.1
Krysko, K., Enge, K. & King, F. The veiled chameleon Chamaeleo calyptratus: A new exotic lizard species in Florida. Fla. Scientist 67, 249–253 (2004).
Kummrow, M. S., Gilman, C., Mackie, P., Smith, D. A. & Mastromonaco, G. F. Noninvasive analysis of fecal reproductive hormone metabolites in female veiled chameleons (Chamaeleo calyptratus) by enzyme immunoassay. Zoo. Biol. 30, 95–115 (2010).
Diaz, R. E. 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. 10, 889–894 (2015).
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).
Andrews, R. M. Effects of incubation temperature on growth and performance of the veiled chameleon (Chamaeleo calyptratus). J. Exp. Zool. Part. A 309, 435–446 (2008).
doi: 10.1002/jez.470
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 98, 1–8 (2015).
pubmed: 25676787 doi: 10.1016/j.steroids.2015.01.019 pmcid: 25676787
Sathyapalan, T. et al. Androstenedione and testosterone levels correlate with in vitro fertilization rates in insulin-resistant women. BMJ Open. Diabetes Res. Care 5, e000387 (2017).
pubmed: 28761656 pmcid: 5530251 doi: 10.1136/bmjdrc-2017-000387
Hampl, R., Putz, Z. & Stárka, L. Radioimmunologic determination of dihydrotestosterone and its value in laboratory diagnosis (In Czech). Biochem. Clin. Bohemoslov. 19, 157–163 (1990).
St. Clair, R. C. Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination. Oecologia 115, 501–507 (1998).
doi: 10.1007/s004420050547
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. 23, 595–601 (2009).
doi: 10.1111/j.1365-2435.2008.01518.x
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. 65, 23–35 (2011).
doi: 10.1007/s00265-010-1029-6
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. 65, 13–21 (2010).
doi: 10.1007/s00265-010-1037-6
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
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, I. M., Dumesic, D. A. & Abbott, D. H. Adrenal hyperandrogenism is induced by fetal androgen excess in a rhesus monkey model of polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 90, 6630–6637 (2005).
pubmed: 16174719 pmcid: 1350929 doi: 10.1210/jc.2005-0691
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. 122, 197–209 (2017).
doi: 10.1093/biolinnean/blx060
Kratochvíl, L. & Flegr, J. Differences in the 2nd to 4th digit length ratio in humans reflect shifts along the common allometric line. Biol. Lett. 5, 643–646 (2009).
pubmed: 19553247 pmcid: 2781964 doi: 10.1098/rsbl.2009.0346
Pélabon, C. et al. On the relationship between ontogenetic and static allometry. Am. Nat. 181, 195–212 (2013).
pubmed: 23348774 doi: 10.1086/668820
Nielsen, S. V., Banks, J. L., Diaz, R. E. Jr., Trainor, P. A. & Gamble, T. Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae). J. Evol. Biol. 31, 484–490 (2018).
pubmed: 29345015 doi: 10.1111/jeb.13242
Rovatsos, M. et al. Evolution of karyotypes in chameleons. Genes. 8, 382 (2017).
pmcid: 5748700 doi: 10.3390/genes8120382 pubmed: 5748700

Auteurs

Anna Bauerová (A)

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

Lukáš Kratochvíl (L)

Faculty of Science, Charles University, Department of Ecology, Viničná 7, 128 43, Prague 2, Czech Republic. lukas.kratochvil@natur.cuni.cz.

Lukáš Kubička (L)

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

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