Oswaldo Hernández-Gallegos

Reproductive Cycle of the Lizard Sceloporus mucronatus with Comments on Intraspecific Geographic Variation

ABSTRACT. Sceloporus mucronatus is a viviparous lizard that inhabits high altitudes in central México. Lizards from Tecocomulco, Hidalgo, México, were collected monthly at 2500 m throughout one year. Macro- and microscopic evidence of gonads showed that both sexes reproduce synchronously during the fall. In males, after a short testicular quiescence in December, the recrudescence begins in winter (January) and continues through spring and summer (July), with maximum activity occurring from late summer to early fall (August–September). Regression takes place simultaneously with copulation during the fall (October–November). In females, vitellogenesis occurs during summer and fall (August–November), with ovulation in the fall (November–December). Gravid females were found throughout the winter, and parturition occurs during spring (May). Litter size was correlated with female snout-vent length. Female reproductive phenology of viviparous Sceloporus species seems to be highly conservative at different altitudes, but male reproductive phenology shifts between spring—summer (in populations higher than 2500 m) and summer—fall (in populations 2500 m or lower), as in the present study. The longer period of testicular recrudescence (January–July) in the studied population from Tecocomulco suggests plasticity in testicular activity.

Temporal germ cell development strategy during continuous spermatogenesis within the montane lizard, Sceloporus bicanthalis (Squamata; Phrynosomatidae)

Sceloporus bicanthalis is a viviparous lizard that lives at higher elevations in Mexico. Adult male S. bicanthalis were collected (n = 36) from the Nevado de Toluca, Mexico (elevation is 4200 m) during August to December, 2007 and January to July, 2008. Testes were extracted, fixed in Trumps, and dehydrated in a graded series of ethanol. Tissues were embedded, sectioned (2 μm), stained, and examined via a light microscope to determine the spermatogenic developmental strategy of S. bicanthalis. In all months examined, the testes were spermiogenically active; based on this, plus the presence of sperm in the lumina of seminiferous tubules, we inferred that S. bicanthalis had year-round or continuous spermatogenesis, unlike most reptiles that occupy a temperate or montane habitat. It was recently reported that seasonally breeding reptiles had a temporal germ cell development strategy similar to amphibians, where germ cells progress through spermatogenesis as a single population, which leads to a single spermiation event. This was much different than spatial development within the testis of other derived amniotes. We hypothesized that germ cell development was temporal in S. bicanthalis. Therefore, we wanted to determine whether reptiles that practice continuous spermatogenesis have a mammalian-like spatial germ cell development, which is different than the typical temperate reptile exhibiting a temporal development. In the present study, S. bicanthalis had a temporal development strategy, despite its continuous spermatogenic cycle, making them similar to tropical anoles.

Genetic Homogeneity between Populations of Aspidoscelis rodecki, a Parthenogenetic Lizard from the Yucatan Peninsula

Abstract We undertook skin-grafting between populations to determine whether Aspidoscelis rodecki originated from single, or multiple, parthenogenetically capable hybrids. We transplanted 292 skin grafts within and between the two most geographically distant populations, considering only grafts in animals surviving more than 45 days. Two hundred fifteen grafts were analyzed. Histocompatibility within (100%) and between (97.9%) populations suggests that A. rodecki was derived from a single, parthenogenetically capable, hybrid.

Reproductive Cycle of a High-Elevation, Oviparous Lizard (Sceloporus spinosus: Reptilia: Phrynosomatidae)

Abstract We studied the reproductive cycle of Sceloporus spinosus from Laguna La Preciosa, Puebla, Mexico, elevation 2,400 m. There was no sexual dimorphism in snout–vent length (males, 87.5 mm; females, 88.8 mm). Gonadal mass varied monthly and was related to snout–vent length; both sexes had a synchronous reproductive cycle that peaked in late winter and early spring. In males, recrudescence occurred November–January with abundant primary and secondary spermatocytes. Maximum testicular mass was in February when seminiferous tubules showed spermiogenesis and spermatozoa were in the lumen and epididymis. Regression was evident in April, when testicular mass decreased, and it continued in May, although spermatozoa were in seminiferous tubules and lumen of epididymal ducts. In July–September, testicular mass was less, and only spermatogonias, Sertoli cells, and remains of sperm were in seminiferous tubules. In females, vitellogenesis began in late autumn, maximum deposition of yolk was in March, and ovulation was in April. Oviductal eggs were present in April–June and oviposition was in June–July. In August–September, only previtellogenic and atretic follicles were present; hatchlings were present in September. Size of clutch was 6–17 eggs and correlated with snout–vent length. One clutch is produced per reproductive season. Reproductive activity in both sexes was distinct from spring-summer activity in tropical sceloporines from high elevations, but was similar to other lizards in northern temperate areas. Resumen Estudiamos el ciclo reproductor de Sceloporus spinosus de la laguna La Preciosa, Puebla, México, a una elevación de 2,400 m. No hubo dimorfismo sexual en la longitud hocico cloaca de machos (87.5 mm) y hembras (88.8 mm). La masa gonadal varió mensualmente y se correlacionó con la longitud hocico cloaca; ambos sexos tuvieron un ciclo reproductor sincrónico con una máxima actividad a fines del invierno y principios de la primavera. En los machos, la recrudescencia ocurrió de noviembre a enero con abundantes espermatocitos primarios y secundarios. La máxima masa testicular fue en febrero cuando los túbulos seminíferos mostraron espermiogénesis y espermatozoides se encontraron en la luz y en los conductos del epidídimo. La regresión fue evidente en abril, cuando decreció la masa testicular y se continuó en mayo, aunque espermatozoides estuvieron presentes en la luz de los túbulos seminíferos y en los conductos del epidídimo. De julio a septiembre la masa testicular se redujo y sólo espermatogonias, células de Sertoli y restos de espermatozoides permanecieron en los túbulos seminíferos. En las hembras la vitelogénesis inició a fines del otoño, el máximo depósito de vitelo fue en marzo y la ovulación en abril. Los huevos en el oviducto estuvieron presentes de abril a junio y la ovoposición fue en junio-julio. De agosto a septiembre sólo folículos previtelogénicos y atrésicos estuvieron presentes; los recién eclosionados aparecieron en septiembre. El tamaño de la puesta fue de 6 a 17 huevos y se correlacionó con la longitud hocico cloaca. Sólo una puesta es producida por estación reproductora. La actividad reproductora en ambos sexos fue diferente de la actividad de primavera–verano de sceloporinos tropicales de elevaciones altas, pero fue similar a la de otros lacertilios de áreas templadas norteñas.

DEMOGRAPHY OF A SEMELPAROUS, HIGH-ELEVATION POPULATION OF SCELOPORUS BICANTHALIS (LACERTILIA: PHRYNOSOMATIDAE) FROM THE NEVADO DE TOLUCA VOLCANO, MEXICO

Abstract We studied demography of a population of viviparous lizard, Sceloporus bicanthalis, from Nevado de Toluca Volcano, Mexico, using mark-recapture methods. Age structure of this population varied seasonally due to an increase in number of juveniles over summer, although neonates were observed in every month. Estimated average density was 304 individuals/ha. Snout-vent length at sexual maturity in viviparous S. bicanthalis was 31 mm in males and 32 mm in females. Males survived longer than females, with an expected lifespan of 15 months, compared to 8 months for females. Net reproductive rate of this population was 1, suggesting it was at equilibrium, while generation time was 7 months. This high-elevation population has a semelparous life cycle.

Ontogenic development of spermatids during spermiogenesis in the high altitude bunchgrass lizard (Sceloporus bicanthalis)

The body of ultrastructural data on spermatid characters during spermiogenesis continues to grow in reptiles, but is still relatively limited within the squamates. This study focuses on the ontogenic events of spermiogenesis within a viviparous and continually spermatogenic lizard, from high altitude in Mexico. Between the months of June and August, testicular tissues were collected from eight spermatogenically active bunchgrass lizards (Sceloporus bicanthalis) from Nevado de Toluca, México. The testicular tissues were processed for transmission electron microscopy and analyzed to access the ultrastructural differences between spermatid generations during spermiogenesis. Interestingly, few differences exist between S. bicanthalis spermiogenesis when compared with what has been described for other saurian squamates. Degrading and coiling membrane structures similar to myelin figures were visible within the developing acrosome that are likely remnants from Golgi body vesicles. During spermiogenesis, an electron lucent area between the subacrosomal space and the acrosomal medulla was observed, which has been observed in other squamates but not accurately described. Thus, we elect to term this region the acrosomal lucent ridge. This study furthers the existing knowledge of spermatid development in squamates, which could be useful in future work on the reproductive systems in high altitude viviparous lizard species.

The ultrastructure of spermatid development during spermiogenesis within the rosebelly lizard, Sceloporus variabilis (Reptilia, Squamata, Phrynosomatidae).

Several recent studies have mapped out the characters of spermiogenesis within several species of squamates. Many of these data have shown both conserved and possibly apomorphic morphological traits that could be important in future phylogenetic analysis within Reptilia. There, however, has not been a recent study that compares spermiogenesis and its similarities or differences between two species of reptile that reside in the same genus. Thus, the present analysis details the changes to spermiogenesis in Sceloporus variabilis and then compares spermatid morphologies to that of Sceloporus bicanthalis. Many of the morphological changes that the spermatids undergo in these two species are similar or conserved, which is similar to what has been reported in other squamates. There are six main character differences that can be observed during the development of the spermatids between these two sceloporid lizards. They include the presence (S. variabilis) or absence (S. bicanthalis) of a mitochondrial/endoplasmic reticulum complex near the Golgi apparatus during acrosome development, a shallow (S. variabilis) or deep (S. bicanthalis) nuclear indentation that accommodates the acrosomal vesicle, filamentous (S. variabilis) or granular (S. bicanthalis) chromatin condensation, no spiraling (S. variabilis) or spiraling (S. bicanthalis) of chromatin during condensation, absence (S. variabilis) or presence (S. bicanthalis) of the longitudinal manchette microtubules, and the lack of (S. variabilis) or presence (S. bicanthalis) of nuclear lacunae. This is the first study that compares spermiogenic ultrastructural characters between species within the same genus. The significance of the six character differences between two distantly related species within Sceloporus is still unknown, but these data do suggest that spermiogenesis might be a good model to study the hypothesis that spermatid ontogeny is species specific. J. Morphol. 275:258–268, 2014.

Larval stages of trematodes in gastropods from Lake Chicnahuapan, State of Mexico, Mexico

During the period from January to December (2007), 1,095 freshwater molluscs of four species were captured (Lymnaea stagnalis, Stagnicola elodes, Physella cubensis and Physa acuta) in Lake Chicnahuapan, State of Mexico, Mexico. Two hundred seventy-two (24.84% prevalence) of these molluscs were parasitised by 11 trematode species (from which two were not identified at the species level) having six cercariae species and five metacercariae species represented in five families. The cercariae Telorchis corti (Plagiorchiidae) and the metacercariae Cotylurus cornutus (Strigeidae) were the species with the highest prevalence among the examined snails. The highest percentage of infection was observed in L. stagnalis (27.45% of prevalence, n = 572) and P. cubensis (23.96%, n = 455). Twenty-one of the examined snails had multiple infections with up to three trematode species.

Spermiogenesis in the imbricate alligator lizard, Barisia imbricata (Reptilia, Squamata, Anguidae)

Although the events of spermiogenesis are commonly studied in amniotes, the amount of research available for Squamata is lacking. Many studies have described the morphological characteristics of mature spermatozoa in squamates, but few detail the ultrastructural changes that occur during spermiogenesis. This studys purpose is to gain a better understanding of the subcellular events of spermatid development within the Imbricate Alligator Lizard, Barisia imbricata. The morphological data presented here represent the first complete ultrastructural study of spermiogenesis within the family Anguidae. Samples of testes from four specimens collected on the northwest side of the Nevado de Toluca, México, were prepared using standard techniques for transmission electron microscopy. Many of the ultrastructural changes occurring during spermiogenesis within B. imbricata are similar to that of other squamates (i.e., early acrosome formation, chromatin condensation, flagella formation, annulus present, and a prominent manchette). However, there are a few unique characteristics within B. imbricata spermatids that to date have not been described during spermiogenesis in other squamates. For example, penetration of the acrosomal granule into the subacrosomal space to form the basal plate of the perforatorium during round spermatid development, the clover‐shaped morphology of the developing nuclear fossa of the flagellum, and the bulbous shape to the perforatorium are all unique to the Imbricate Alligator Lizard. These anatomical character differences may be valuable nontraditional data that along with more traditional matrices (such as DNA sequences and gross morphological data) may help elucidate phylogenetic relationships, which are historically considered controversial within Squamata. J. Morphol., 2013.

Sperm storage in the viviparous lizard Sceloporus bicanthalis (Squamata: Phrynosomatidae), a species with continuous spermatogenesis

Sceloporus bicanthalis inhabits the Nevado de Toluca, México, and the males exhibit continuous spermatogenesis with mature sperm available year round. Females were collected monthly to evaluate the morphology of the oviducts and the presence of sperm storage. Histological examination revealed that the oviductal structure in this lizard is similar to that described for other lacertilian species: anterior infundibulum, glandular uterus, and a posterior non-glandular uterus. The oviduct wall consists of a superficial visceral pleuroperitoneum, a middle layer of smooth muscle with outer longitudinal and inner circular fibers, and a deep mucosa or lamina propria deeply lined by an epithelium containing ciliated and non-ciliated secretory cells. Spermatozoa are stored at the base of the mucosal folds, in crypts and in sperm storage tubules at the transition between the glandular uterus and non-glandular uterus, as well as in the anterior non-glandular uterus of previtellogenic, vitellogenic, pregnant, and postpartum females. The sperm in the oviductal cavity or in retention sites is in contact with secretory products derived from non-ciliated epithelial cells. Spermatozoa usually assume an orderly distribution with their heads aligned and oriented toward the base of the folds or crypts. This study shows that females of S. bicanthalis exhibit prolonged sperm storage that corresponds with the continuous reproductive strategy employed by males.