Worawitoo MEESOOK, Taksin ARTCHAWAKOM, Anchalee AOWPHOL, Panas TUMKIRATIWONG

Reproductive pattern and sex hormones of Calotesemma Gray 1845 andCalotesversicolor Daudin 1802 (Squamata; Agamidae)

We monitored testicular and ovarian morphologies, seminiferous tubules, the sexual segments of the kidneys (SSK), follicular histologies, and male testosterone and female estradiol to define the reproductive pattern of Calotes emma and Calotesversicolor. Samples were collected monthly at Sakaerat Environmental Research Station in Thailand for 1 year. Testicular hypertrophies occurred at a time characteristic for each species, with their time course corresponding well to both active spermatogenesis and the hypertrophied SSK. Gravid females were also found at a time characteristic for each species. In active reproductive females, oviductal eggs were concomitantly encountered with ovarian vitellogenic follicles. The previtellogenic and vitellogenic follicles corresponded well to granulosa layer alterations. The distinct large pyriform cells were present in the granulosa layer of previtellogenic follicles but disappeared from the vitellogenic follicles. Male testosterone levels rose during testicular and SSK hypertrophies, and female estradiol levels increased during active reproductive stages of late vitellogenic follicles and gestation. We suggest that the reproductive patterns of C. emma and C. versicolor fall into the same reproductive pattern of annual continual reproduction, but that the time courses of such events are different in the 2 Calotes, and even in individuals of the same Calotes population.

PDF

___

Aldridge RD, Goldberg SR, Wisniewski SS, Bufalino AP, Dillman CB (2009). The reproductive cycle and estrus in the colubrid snakes of temperate North America. Contemp Herpetol 4: 1-31.
Amey AP, Whittier JM (2000). Seasonal patterns of plasma steroid hormones in males and females of the bearded dragon lizard, Pogona barbata.Gen Comp Endocrinol117: 335-342.
Andreuccetti P (1992). An ultrastructural study of differentiation of pyriform cells and their contribution to oocyte growth in representative Squamata. J Morphol 212: 1-11.
Ando S, Panno ML, Ciarcia G, Imbrogno E, Buffone M, Beraldi E, Sisci D, Angelini F, Botte V (1990). Plasma sex hormone concentrations during the reproductive cycle in the male lizard, Podarcis s. sicula.J Reprod Fertil 90: 353-360.
Ando S, Ciarcia G, Panno ML, Imbrogno E, Tarantino G, Buffone M, Beraldi E, Angelini F, Botte V (1992). Sex steroids levels in the plasma and testis during the reproductive cycle of lizard Podarcis s. sicula Raf. Gen Comp Endocrinol 85: 1-7.
Arslan MJ, Lobo J, Zaidi AA, Jalali S, Qazi MH (1978a). Annual androgen rhythm in the spiny-tailed lizard, Uromastix hardwicki.Gen Comp Endocrinol36: 16-22.
Arslan MJ, Zaidi P, Lobo J, Zaidi AA, Qazi MH (1978b). Steroid levels in preovulatory and gravid lizards (Uromastix hardwicki). Gen Comp Endocrinol34: 300-303.
Avwioro G (2011). Histochemical uses of haematoxylin-a review. J Pham Clin Sci 1: 24-34.
Bishop JE (1959). A histological and histochemical study of the kidney tubule of the common garter snake, Thamnophis sirtalis, with special reference to the sexual segment in the male. J Morphol 104: 307-358.
Bourne AR, Taylor JL, Watson TG (1986). Annual cycles of plasma and testicular androgens in the lizard Tiliqua (Trachydosaurus) rugosa. Gen Comp Endocrinol61: 278-286.
Courty Y, Dufaure JP (1982). Circannual testosterone, dihydrotestosterone and androstenedione in the plasma and testis of Lacerta vivipara,a seasonally breeding viviparous lizard. Steroids 39: 517-529.
Cox RM, Skelly SL, Leo A, John-Alder HB (2005). Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus. Copeia 2005: 597-608.
Crews D (1976). Hormonal control of male courtship behavior and female attractively in the garter snake (Thamnophis sirtalis parietalis). Horm Behav 7: 451-460.
Crews D (1980). Interrelationships among ecological, behavioral, and neuroendocrine processes in the reproductive cycle of Anolis carolinensis and other reptiles. Adv Stud Behav 11: 1-74.
Crews D (1984). Gamete production, sex hormone secretion and mating behavior uncoupled. Horm Behav 14: 22-28.
Crews D (1999). Reptilian reproduction, overview. In: Knobil E, Neil JD, editors. Encyclopedia of Reproduction. New York, NY, USA: Academic Press, pp. 239-243.
Crews D, Camazine B, Diamond M, Mason R, Tokarz R, Garstka WR (1984). Hormonal independence of courtship behavior in the male garter snake. Horm Behav 14: 29-41.
Crews D (2005). Evolution of neuroendocrine mechanisms that regulate sexual behavior. Trends Endocrinol Metab 16: 354-361.
Del Conte E (1972). Granular secretion in the kidney Rss of female lizards, Cnemidophorus l. lemniscatus (Sauria, Teiidae). J Morphol 137: 181-191.
Del Conte E, Tamayo JG (1973). Ultrastructure of the Rss of the kidneys in male and female lizards, Cnemidophorus l. lemniscatus (L.). Z Zellforsch 144: 325-327.
Diaz JA, Alonso-Gomez AL, Delgado MJ (1994). Seasonal variation of gonadal development, sexual steroids, and lipid reserves in a population of the lizard Psammodromus algirus.J Herpetol 28: 199-205.
Fitch HS (1970). Reproductive Cycles in Lizards and Snakes. 2nd ed. Lawrence, KS, USA: The University of Kansas Museum of Natural History.Fox W (1952). Seasonal variation in the male reproductive system of Pacific coast garter snakes. J Morphol 90: 481-553.
French SS, Moore MC (2008). Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. Gen Comp Endocrinol 155: 148-156.
Garstka WR, Camazine B, Crews D (1982). Interactions of behavior and physiology during the annual reproductive cycle of the red-garter snake(Thamnophissirtalis parietalis). Herpetologica 38: 104-123.
Goldberg SR, Kraus F, Bursey CR (2002). Reproduction in an introduced population of the brown anole, Anolis sagrei, from Oahu, Hawaii. Pac Sci 56: 163-168.
Gouder BYM, Nadkarni VB (1979). Histometric and histochemical changes in the seminiferous epithelium, Leydig cells and Sertoli cells in the testis of Calotes versicolor. Biol Bull India 1: 15-22.
Guillette LJ Jr, Casas-Andreu G (1980). Fall reproductive activity in the high altitude Mexican lizard, Sceloporus grammicus microlepidotus. J Herpetol 14: 143-147.
Guillette LJ Jr, Casas-Andreu G (1981). Seasonal variation in fat body weights of the Mexican high elevation lizard Sceloporus grammicus microlepidotus. J Herpetol 15: 366-371.
Guillette LJ Jr, Spielvogel S, Moore FL (1981). Luteal development, placentation, and plasma progesterone concentration in the viviparous lizard, Sceloporus jarrovi. Gen Comp Endocrinol27: 389-400.
Hartmann T, Geissler P, Poyarkov AN Jr, Ihlow F, Galoyan AE, Rödder D, Böhme W (2013). A new species of the genus Calotes Cuvier, 1817 (Squamata: Agamidae) from southern Vietnam. Zootaxa 3599: 246-260.
Inger RF, Greenberg B (1966). Annual reproductive patterns of lizards from a Bornean rainforest. Ecology 47: 1007-1021.
Jimenez-Cruz E, Ramırez-Bautista A, Marshall JC, Lizana-Avia M, Nieto-Montes De Oca A (2005). Reproductive cycle of Sceloporus grammicus (Squamata: Phrynosomatidae) from Teotihuacan, Mexico. Southwest Natur 50: 178-187.
Jenssen TA, Nunez SC (1994). Male and female reproductive cycles of the Jamaican lizard, Anolis opalinus. Copeia 1994: 767-780.
Lance VA (1998). Female reproductive system, reptiles. In: Knobil E, Neill JD, editors. Encyclopedia of Reproduction. New York, NY, USA: Academic Press, pp. 239-243.
Lee JC, Clayton D, Eisenstein S, Perez I (1989). The reproductive cycle of Anolis sagrei in southern Florida. Copeia 1989: 930-937.
Laohachinda W (2009). Herpetology. Bangkok, Thailand: Kasetsart University Press.
Licht P (1984). Seasonal cycles in reptilian reproductive physiology. In: Lamming GE, editor. Marshalls Physiology of Reproduction. New York, NY, USA: Churchill-Livingstone.
Licht P, Gorman GC (1970). Reproductive and fat cycles in Caribbean Anolis lizards. Univ Calif Publ Zool 95: 1-52.
Lofts B (1977). Patterns of spermatogenesis and steroidogenesis in male reptiles. In: Calaby JH, Tyndale-Biscoe CH, editors. Reproduction and Evolution. Canberra, Australia: Australian Academic Science, pp. 127-136.
Lovern MB, Holmes MM, Wade J (2004). The green anole (Anolis carolinensis): a reptilian model for laboratory studies of reproductive morphology and behavior. ILAR J 45: 54-64.
Lovern MB (2011). Hormones and reproductive cycles in lizards. In: Norris DO, Lopez KH, editors. Hormones and Reproduction of Vertebrates, Vol 3. Reptiles. New York: Academic Press, pp. 321-353.
Masson GR, Guillette LJ Jr (1987). Changes in oviductal vascularity during the reproductive cycle of three oviparous lizards (Eumeces obsoletus, Sceloporus undulatus and Crotaphytus collaris). J Reprod Fertil80: 361-371.
Maurizii MG, Alibardi L, Taddei C (2004). Alpha-tubulin and acetylated alpha-tubulin during ovarian follicle differentiation in the lizard Podarcis sicula Raf. J Exp Zool 301: 532-541.
Mendez-De La Cruz FR, Villagran-Santa Cruz M, Cuellar O (1994). Geographic variation of spermatogenesis in the Mexican viviparous lizard Sceloporus mucronatus. Biogeographica 70: 59-67.
Menezes VA, Rocha CFD, Dutra GF (2004). Reproductive ecology of the parthenogenetic whiptail lizard Cnemidophorus nativo in a Brazilian restinga habitat. J Herpetol 38: 280-282.
Moreira PL, Birkhead TR (2003). Copulatory plugs in the Iberian rock lizard do not prevent insemination by rival males. Funct Ecol 17: 796-802.
Norris DO (2013). Vertebrate Endocrinology. 5th ed. Tokyo, Japan: Elsevier Academic Press.
Ortega-Leon AM, Villagran-Santa Cruz M, Zuniga-Vega JJ, Cuevadel Castillo R, Mendez-De La Cruz FR (2009). Sperm viability in the reproductive tract of females in a population of Sceloporus mucronatus exhibiting asynchronous reproduction. West N Am Naturalist 69: 96-104.
Phillips JA, Millar RP (1998). Reproductive biology of the white-throated savanna monitor, Varanus albigularis. J Herpetol 32: 366-377.
Pianka ER, Vitt LJ (2003). Lizards: Windows to the Evolution of Diversity. Berkeley, CA, USA: University of California Press.
Putti R, Varricchio E, Gay F, Elena C, Paolucci M (2009). Leptin effects on testis and epididymis in the lizard Podarcis sicula, during summer regression. Gen Comp Endocrinol 160: 168-175.
Radder RS, Shanbhag BA, Saidapur K (2001). Pattern of plasma sex steroid hormone levels during reproductive cycles of male and female tropical lizard, Calotes versicolor. Gen Comp Endocrinol 124: 285-292.
Regaud C, Policard A (1903). Recherches sur la structure du rein de quelques ophidiens. Arch Anat Microsc 6: 191-282.
Rhen T, Sakata JT, Crews D (2005). Effects of gonadal sex and incubation temperature on the ontogeny of gonadal steroid concentrations and secondary sex structure in leopard geckos, Eublepharis macularius. Gen Comp Endocrinol 142: 289-296.
Ruibal RR, Philibosian R, Adkins JL (1972). Reproductive cycle and growth in the lizard Anolis acutus. Copeia 1972: 509-518.
Sever DM, Hopkins WA (2005). Renal sexual segment of the ground skink, Scincella laterale (Reptilia, Squamata, Scincidae). J Morphol 266: 46-59.
Sever DM, Ryan TJ, Stephens R, Hamlett WC (2002). Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). III. Rss of the male kidney. J Morphol 252: 238-254.
Sexton OJ, Ortlet EP, Hathaway LM, Ballinger RE, Licht P (1971). Reproductive cycles of three species of anoline lizards from the Isthmus of Panama. Ecology 52: 201-215.
Sexton OJ, Brown KM (1977). The reproductive cycle of an iguanid lizard Anolissagrei, from Belize. J Nat Hist 11: 241-250.
Shanbhag BA (2003). Reproductive strategies in the lizard, Calotes versicolor. Curr Sci India 84: 646-652.
Shanbhag BA, Prasad BSK (1993). Follicular dynamics and germinal bed activity during the annual ovarian cycle of the lizard, Calotes versicolor. J Morphol 216: 1-7.
Shanbhag BA, Radder RS, Saidapur SK (2000). Maternal size determines clutch mass, whereas breeding timing influences the clutch and egg sizes in the tropical lizard, Calotes versicolor (Agamidae). Copeia 2000: 1062-1067.
Tokarz RR, McMann S, Seitz L, John-Alder H (1998). Plasma corticosterone and testosterone levels during the annual reproductive cycle of male brown anoles (Anolis sagrei). Physiol Zool 71: 139-146.
Tumkiratiwong P, Meesuk W, Chanhome L, Aowphol A (2012). Reproductive patterns of captive male and female monocled cobra, Naja kaouthia (Lesson, 1831). Zool Stud 51: 692-700.
Uribe MCA, Portales BGL, Guillette LJ Jr (1996). Ovarian folliculogenesis in the oviparous Mexican lizard Ctenosaura pectinata. J Morph 230: 99-112.
Van Wyk JH (1984). Physiological changes during ovarian cycle of the female rock lizard, Agama atra (Sauria: Agamidae). S Afr J Zool 19: 253-260.
Vercken E, Clobert J (2008). Ventral color polymorphism correlates with alternative behavioral patterns in female common lizards (Lacerta vivipara). Ecoscience 15: 320-326.
Villagran-Santa Cruz M, Mendez-De La Cruz FR, Parra-Gamez L (1994). Spermatogenesis in the lizard Sceloporus mucronatus(Reptilia, Phrynosomatidae). Rev Biol Trop 42: 289-296.
Vitt LJ, Caldwell JP (2009). Herpetology. 3rd ed. Tokyo, Japan: Elsevier Academic Press.Volsøe H (1944). Structure and seasonal variation of the male reproductive organs of Viper aberus (L.). Spolia Zool Mus Hauniensis 5: 1-157.
Woodley SK, Moore MC (1999). Female territorial aggression and steroid hormones in mountain spiny lizards. Anim Behav 57: 1083-1089.
Zug GR, Brown HHK, Schulte II JA, Vindum JV (2006). Systematics of the garden lizards, Calotes versicolor group (Reptilia, Squamata, Agamidae), in Myanmar: central dry zone populations. Proc Calif Acad Sci 57: 35-68.
Zuniga-Vega JJ, Mendez-De La Cruz FR, Cuellar O (2008). Demography of the lizard Sceloporus grammicus: exploring temporal variation in population dynamics. Can J Zool 86: 1397-1409.