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Continuous Spermatogenesis in the Lizard Sceloporus Bicanthalis (Sauria: Phrynosomatidae) from High Elevation Habitat of Central Mexico

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Continuous Spermatogenesis in the Lizard Sceloporus Bicanthalis (Sauria: Phrynosomatidae) from High Elevation Habitat of Central Mexico Herpetologica, 58(4), 2002, 415±421 q 2002 by The Herpetologists' League, Inc. CONTINUOUS SPERMATOGENESIS IN THE LIZARD SCELOPORUS BICANTHALIS (SAURIA: PHRYNOSOMATIDAE) FROM HIGH ELEVATION HABITAT OF CENTRAL MEXICO OSWALDO HERNAÂ NDEZ-GALLEGOS1,FAUSTO ROBERTO MEÂ NDEZ-DE LA CRUZ1, MARICELA VILLAGRAÂ N-SANTA CRUZ2, AND ROBIN M. ANDREWS3,4 1Laboratorio de HerpetologõÂa, Departamento de ZoologõÂa, Instituto de BiologõÂa, Universidad Nacional AutoÂnoma de MeÂxico, A. P. 70-515, C. P. 04510, MeÂxico, D. F. MeÂxico 2Laboratorio de BiologõÂa de la ReproduccioÂn Animal, Facultad de Ciencias, Universidad Nacional AutoÂnoma de MeÂxico, A. P. 70-515, C. P. 04510, MeÂxico, D. F. MeÂxico 3Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA ABSTRACT: Sceloporus bicanthalis is a viviparous lizard that inhabits high altitude temperate zone habitats in MeÂxico. Our histological observations indicate that adult males exhibit spermato- genesis and spermiogenesis throughout the year; no seasonal differences were found in testes mass, height of epididymal epithelial cells, and number of layers of spermatogonia, primary and secondary spermatocytes, and spermatids. Seminiferous tubules exhibited slight, but statistically signi®cant, seasonal variation in diameter. Continuous spermatogenesis and spermiogenesis of S. bicanthalis differ from the cyclical pattern exhibited by most species of lizards and from lizard species sympatric with S. bicanthalis. Continuous reproductive activity of males of S. bicanthalis, and maturation at a relatively small size, is associated with a female reproductive activity in which vitellogenic or pregnant females are present in the population during all months of the year. As a consequence, males can encounter potential mates as soon as they mature. Key words: Reproductive cycle; Sceloporus bicanthalis; Spermatogenesis; Viviparity REPRODUCTIVE activity of reptiles is ity of Sceloporus bicanthalis, a phrynoso- usually seasonal. In the temperate zone, matid lizard of high elevations of the cen- seasonal reproduction is associated with tral mountains of MeÂxico. This species is the alternation of warm and cold seasons viviparous as are most other lizards that (Duvall et al., 1982; Fitch, 1970; Sher- live at comparable elevations. Based on brooke, 1975). In the lowland tropics, variation in the volume of testes, Guillette most reptiles also exhibit seasonal repro- (1981a, 1982) reported that males of this ductive cycles, but, in this case, they are species exhibit a seasonal reproductive cy- associated with the alternation of wet and cle. In contrast, our histological analysis dry seasons (Howland et al., 1990; Vitt and shows that males are actually spermato- Morato de Carvalho, 1992). Similarly, in genic year round. high elevation subtropical areas of MeÂxico and Central America, most lizards also ex- MATERIALS AND METHODS hibit seasonal reproductive cycles (Guillet- We collected Sceloporus bicanthalis at te and MeÂndez-de la Cruz, 1993; MeÂndez- Parque Nacional Zoquiapan, State of MeÂx- de la Cruz et al., 1998; RamõÂrez-Bautista ico (988 379 390 W, 198 139 100 N), at 3200 et al., 1998). Aseasonal reproduction is, m. The study area has a relatively cool cli- thus, an uncommon reproductive pattern for reptiles, regardless of habitat. At high mate with low temperature variation dur- elevations in Costa Rica, however, males of ing the year, and most rain falls during Barisia monticola exhibit continual sper- summer (Fig. 1). Vegetation is dominated matogenesis and spermiogenesis and ap- by pines, and the understory consists of pear to be reproductive throughout the various species of bunch-grasses, including year (Vial and Stewart, 1985). Festuca and Muhlenbergia (Rzedowsky, Our study examines the testicular activ- 1981). Sceloporus bicanthalis is terrestrial and is associated with the bunch-grass mi- crohabitat; individuals use the grasses for 4 CORRESPONDENCE: e-mail, [email protected] perches and for shelter. Collections were 415 416 HERPETOLOGICA [Vol. 58, No. 4 TABLE 1.ÐMonthly sample sizes for males of Scelo- porus bicanthalis and individuals selected for histo- logical analysis. J 5 juvenile and Ad 5 adult males. Males selected for Sample size histological analysis Month Ad J Ad J April 4 0 3 0 May 4 2 3 0 June 4 0 3 0 July 4 6 2 0 August 5 0 4 0 September 4 3 3 0 FIG. 1.ÐMean temperature (solid circles) and October 4 1 3 0 rainfall (open circles) averaged over 3-mo intervals at November 3 0 3 0 the weather station (RõÂo FrõÂo) located closest (about December 2 6 2 1 15 km) to the Zoquiapan study site (GarcõÂa, 1973). January 5 0 3 0 February 5 0 2 0 March 4 1 2 1 made monthly (Table 1) but were analyzed seasonally: spring 1993 (April±June, n 5 14), summer 1993 (July±September, n 5 mass and SVL as the covariate for other 22), fall 1993 (October±December, n 5 measurements. In no case was the inter- 16), and winter 1994 (January±March, n 5 action term between the class variable and 15). Morphological measurements taken the covariate signi®cant at P , 0.05. from each animal were as follows: snout± vent length (SVL), body mass, and testic- RESULTS ular mass. The smallest sexually mature male was We performed conventional histological 35 mm SVL as judged by both gross mor- analyses (Estrada-Flores et al., 1990) of phology and histological analysis. Exter- testes from males exhibiting secondary nally, all individuals 35 mm in length or sexual characteristics (Table 1). An ocular more exhibited bright blue ventral color- micrometer was used to make the follow- ation and active femoral pores. Moreover, ing measurements on the left testis: mean all males 35 mm or more (n 5 33) had diameter of 25 representative seminiferous sperm in their seminiferous tubules and tubules and height of 25 epididymal epi- epididymal ducts. Adult males ranged in thelial cells. Germinal cells (spermatogo- size from 35±51 mm SVL (xÅ 5 42.6 mm, nia, primary and secondary spermatocytes, SE 5 0.61). Two males with SVL of 34 and spermatids) were classi®ed according mm had traces of blue coloration and were to size and position in the seminiferous tu- selected for histological analysis. They did bules. Relative abundance of germinal not, however, have sperm in the seminif- cells was estimated by counting the num- erous tubules and epididymis duct and, ber of layers in 25 tubules. The presence therefore, were considered immature. of spermatozoa in the seminiferous tu- Testis mass of adult males did not vary bules and epididymis ducts was used to seasonally (F3,43 5 0.8, P 5 0.51, ANCO- de®ne the minimum size of sexual matu- VA), although testis mass was related to rity. We averaged the measurements for body mass (F1,43 5 65.6, P , 0.0001). Anal- each individual; individuals were, thus, yses of histological data also indicated that represented only once in statistical analy- adult males of S. bicanthalis exhibit con- ses. tinuous testicular activity throughout the All statistical analyses were conducted year; no testicular recrudescence or re- with SAS software (SAS Institute, Inc., gression was observed. Mature sperm was Version 6.12, 1997). We used ANCOVA's found in the seminiferous tubules (Fig. 2) to compare seasonal means of morpholog- and epididymal ducts in all specimens in ical measurements. In these analyses, we all seasons. The height of epididymal epi- used body mass as the covariate for testis thelial cells and the number of layers of December 2002] HERPETOLOGICA 417 FIG. 2.ÐSeminiferous tubules of Sceloporus bicanthalis from Zoquiapan, State of MeÂxico: (a) spring, (b) summer, (c) fall, and (d) winter. Note the presence of spermatogonia (SG), primary spermatocytes (PS), secondary spermatocytes (SS), spermatids (SP), and spermatozoa (S) in all seasons. Scale bar 5 30 mm. 418 HERPETOLOGICA [Vol. 58, No. 4 sexual segment of the kidney, are known to increase in height and secretory activity in association with reproduction (Wilhoft, 1963). While we did not study the sexual segment of the kidney, the lack of seasonal variation in the size of the cells in the ep- ithelial lining of the epididymis duct indi- cates that reproduction by males was pos- sible year round. The bright blue ventral coloration and active femoral pores throughout the year further suggest con- tinual reproductive activity; these features presumably re¯ect high androgen levels throughout the year (Cooper, 1995; Hews and Moore, 1995). Our conclusion about the reproductive cycle of males of S. bicanthalis differs from that of Guillette (1981a, 1982). A possible reason for this difference is that observations by Guillette and by us were made on different populations and for dif- ferent years. Geographic variation in re- productive cycles is known for several spe- cies (MeÂndez-de la Cruz et al., 1994; Vil- lagraÂn-Santa Cruz et al., 1994). More like- ly explanations, however, relate to methodology. Guillette9s study is based on FIG. 3.ÐMorphological measurements of testis estimates of testis volume whereas our mass and histological structures expressed as means conclusions are based on histological anal- and their standard errors. When standard error bars are not shown, they were too small to be distin- ysis. The problem with the use of testis guished from the means. Values with different super- size to assess reproductive status is that scripts are signi®cantly different (P , 0.05). variation in testis size may re¯ect the de- gree of hydration (Vitt, 1986) or variation in intensity of sperm production (GarcõÂa- spermatogonia, primary and secondary Collazo et al., 1993). Moreover, Guillette spermatocytes, and spermatids did not did not correct estimates of testis size for vary seasonally or as a function of SVL (P the size of the lizard, and testis size is values 0.11±0.95 for overall models). The strongly correlated with body size in our only feature that varied seasonally was the investigation. diameter of seminiferous tubules (F3,28 5 Our results call into question male re- 4.0, P 5 0.018, ANCOVA) (Fig.
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