Fausto R. Méndez-de la Cruz

CONTINUOUS SPERMATOGENESIS IN THE LIZARD SCELOPORUS BICANTHALIS (SAURIA: PHRYNOSOMATIDAE) FROM HIGH ELEVATION HABITAT OF CENTRAL MEXICO

Sceloporus bicanthalis is a viviparous lizard that inhabits high altitude temperate zone habitats in México. Our histological observations indicate that adult males exhibit spermatogenesis 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 significant, 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. Resumen Sceloporus bicanthalis es una lagartija vivípara que habita en elevaciones altas de ambientes templados en México. De acuerdo al análisis histológico, los machos adultos presentan espermatogénesis y espermiogénesis continuas; no se encontraron diferencias estacionales en el peso testicular, altura del epitelio de los conductos del epidídimo, número de capas de espermatogonias, espermatocitos primarios y secundarios y espermátidas. En contraste, se encontró variación estacional en el diámetro de los túbulos seminíferos. El patrón reproductor continuo de S. bicanthalis es atípico cuando se compara con los ciclos reproductores de otras lagartijas, incluyendo especies simpátricas. Aparentemente, la actividad reproductora continua de los machos de S. bicanthalis y su madurez sexual temprana, están asociadas con la actividad reproductora de las hembras, en el cual la vitelogénesis o preñez se presentan durante todo el año. En consecuencia, los machos pueden aparearse una vez que alcanzan la madurez sexual.

Body Temperatures of Female Sceloporus grammicus: Thermal Stress or Impaired Mobility?

Females of some lizard species exhibit lower body temperatures (Tbs) when reproductive (gravid or pregnant) than when not reproductive. Two hypotheses have been invoked to explain this phenomenon. One, the thermal stress hypothesis, is that the thermal optimum for embryos is lower than that of the female, and females thus actively select relatively low Tbs. The other, the encumbrance hypothesis, is that females are encumbered by their clutch/litter and thus passively accept relatively low Tbs. We collected field data on the thermal biology of Sceloporus grammicus at a high elevation site in Mexico during two seasons. In March, when thermoregulation was facilitated by high ambient temperature, lizards had high Tbs overall, and reproductive females had significantly lower Tbs than males; these observations were in accord with the thermal stress hypothesis. In June/July, when thermoregulation was difficult as a result of low ambient temperatures, lizards had low Tbs overall, and reproductive females had considerably lower Tbs than nonreproductive females. Thus, when thermal opportunities were limited, reproductive females had more difficulty thermoregulating than did nonreproductive females. These observations were in accord with the encumbrance hypothesis. The encumbrance hypothesis was also supported by the observation that females grew more slowly when reproductive than when nonreproductive. Thus, we suggest that the thermal stress and the encumbrance hypotheses are not alternatives but are complementary explanations for the thermal behavior of female Sceloporus.

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.

Landscape Genetics of Leaf-Toed Geckos in the Tropical Dry Forest of Northern Mexico

Habitat fragmentation due to both natural and anthropogenic forces continues to threaten the evolution and maintenance of biological diversity. This is of particular concern in tropical regions that are experiencing elevated rates of habitat loss. Although less well-studied than tropical rain forests, tropical dry forests (TDF) contain an enormous diversity of species and continue to be threatened by anthropogenic activities including grazing and agriculture. However, little is known about the processes that shape genetic connectivity in species inhabiting TDF ecosystems. We adopt a landscape genetic approach to understanding functional connectivity for leaf-toed geckos (Phyllodactylus tuberculosus) at multiple sites near the northernmost limit of this ecosystem at Alamos, Sonora, Mexico. Traditional analyses of population genetics are combined with multivariate GIS-based landscape analyses to test hypotheses on the potential drivers of spatial genetic variation. Moderate levels of within-population diversity and substantial levels of population differentiation are revealed by F ST and D est. Analyses using structure suggest the occurrence of from 2 to 9 genetic clusters depending on the model used. Landscape genetic analysis suggests that forest cover, stream connectivity, undisturbed habitat, slope, and minimum temperature of the coldest period explain more genetic variation than do simple Euclidean distances. Additional landscape genetic studies throughout TDF habitat are required to understand species-specific responses to landscape and climate change and to identify common drivers. We urge researchers interested in using multivariate distance methods to test for, and report, significant correlations among predictor matrices that can impact results, particularly when adopting least-cost path approaches. Further investigation into the use of information theoretic approaches for model selection is also warranted.

Thermoregulation of two sympatric species of horned lizards in the Chihuahuan Desert and their local extinction risk.

Thermoregulatory studies of ectothermic organisms are an important tool for ecological physiology, evolutionary ecology and behavior, and recently have become central for evaluating and predicting global climate change impacts. Here, we present a novel combination of field, laboratory, and modeling approaches to examine body temperature regulation, habitat thermal quality, and hours of thermal restriction on the activity of two sympatric, aridlands horned lizards (Phrynosoma cornutum and Phrynosoma modestum) at three contrasting Chihuahuan Desert sites in Mexico. Using these physiological data, we estimate local extinction risk under predicted climate change within their current geographical distribution. We followed the Hertz et al. (1993, Am. Nat., 142, 796-818) protocol for evaluating thermoregulation and the Sinervo et al. (2010, Science, 328, 894-899) eco-physiological model of extinction under climatic warming. Thermoregulatory indices suggest that both species thermoregulate effectively despite living in habitats of low thermal quality, although high environmental temperatures restrict the activity period of both species. Based on our measurements, if air temperature rises as predicted by climate models, the extinction model projects that P. cornutum will become locally extinct at 6% of sites by 2050 and 18% by 2080 and P. modestum will become extinct at 32% of sites by 2050 and 60% by 2080. The method we apply, using widely available or readily acquired thermal data, along with the modeling, appeared to identify several unique ecological traits that seemingly exacerbate climate sensitivity of P. modestum.

Reproductive Activity of Three Sympatric Viviparous Lizards at Omiltemi, Guerrero, Sierra Madre del Sur, Mexico

Abstract We studied the reproductive characteristics of sympatric populations of Sceloporus formosus scitulus, Sceloporus omiltemanus (Phrynosomatidae), and Mesaspis gadovii (Anguidae) at the Omiltemi forest reserve (Guerrero, Mexico). Males are larger and reach larger body sizes at reproductive maturity and are more colorful than females in both Sceloporus, whereas males are smaller than females and reach sexual maturity at similar body sizes in M. gadovii. These species are single brooded and follow a common pattern of annual reproductive activity. The reproductive activity of females and males of the three species is seasonal; vitellogenesis is initiated in late summer and continues in autumn/rainy season, gestation occurs throughout the winter/dry season, and parturition occurs in early spring. All three species have intersexual synchrony in reproductive activity. In spite of similar reproductive schedules, some subtle features related to the length of each of the reproductive stages could be observed. Sceloporus formosus scitulus has a more extended reproductive season, and large females start vitellogenesis earlier than do small ones. Males have a prolonged reproductive activity and a short nonreproductive season. In contrast, the reproductive cycle of the other two species is defined by shorter reproductive season and less intrasexual asynchrony for both sexes than found in S. f. scitulus. The seasonal pattern of reproduction shared by these three species is characteristic of other viviparous lizards at high elevations in tropical and subtropical latitudes of Central and South America, being convergent for different lizard families. This convergence in reproductive patterns suggests a common evolutionary response to environmental factors associated with montane habitats, whereas specific differences observed within species are attributed to the particular evolutionary history of each taxon.

Estimating the temporal and spatial extent of gene flow among sympatric lizard populations (genus Sceloporus) in the southern Mexican highlands

Interspecific gene flow is pervasive throughout the tree of life. Although detecting gene flow between populations has been facilitated by new analytical approaches, determining the timing and geography of hybridization has remained difficult, particularly for historical gene flow. A geographically explicit phylogenetic approach is needed to determine the overlap of ancestral populations. In this study, we performed population genetic analyses, species delimitation, simulations and a recently developed approach of species tree diffusion to infer the phylogeographic history, timing and geographic extent of gene flow in lizards of the Sceloporus spinosus group. The two species in this group, S. spinosus and S. horridus, are distributed in eastern and western portions of Mexico, respectively, but populations of these species are sympatric in the southern Mexican highlands. We generated data consisting of three mitochondrial genes and eight nuclear loci for 148 and 68 individuals, respectively. We delimited six lineages in this group, but found strong evidence of mito‐nuclear discordance in sympatric populations of S. spinosus and S. horridus owing to mitochondrial introgression. We used coalescent simulations to differentiate ancestral gene flow from secondary contact, but found mixed support for these two models. Bayesian phylogeography indicated more than 60% range overlap between ancestral S. spinosus and S. horridus populations since the time of their divergence. Isolation–migration analyses, however, revealed near‐zero levels of gene flow between these ancestral populations. Interpreting results from both simulations and empirical data indicate that despite a long history of sympatry among these two species, gene flow in this group has only recently occurred.

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.

Genetic Variation and Origin of Parthenogenesis in the Aspidoscelis cozumela Complex: Evidence from Mitochondrial Genes

Parthenogenesis is a form of clonal reproduction. Eggs develop in the absence of sperm and offspring are genetically identical to their mother. Although common in invertebrates, it occurs in only a few species of squamate reptiles. Parthenogenetic reptiles have their origin in interspecific hybridization, and their populations are exclusively female. Because of its high mutation rate and maternal inheritance, mitochondrial DNA sequence data can evaluate the origin and evolution of all-female vertebrates. Partial sequences from two mitochondrial genes, Cytb and ND4, were analyzed to investigate questions about the origin of parthenogenesis in the Aspidoscelis cozumela complex, which includes A. cozumela, A. maslini and A. rodecki. Low levels of divergence were detected among parthenogenetic species, and between them and A. angusticeps, confirming it as the maternal species of the parthenoforms. A gene tree was constructed using sequences from three populations of A. angusticeps and nine of its unisexual daughter species. The phylogeny suggests that two independent hybridization events between A. angusticeps and A. deppii formed three unisexual species. One hybridization resulted in A. rodecki and the other formed A. maslini and A. cozumela. Although A. cozumela has the haplotype characteristic of A. maslini from Puerto Morelos, it is considered to be a different species based on karyological and morphological characteristics and its geographical isolation.