The evolutionary network of whiptail lizards reveals predictable outcomes of hybridization.

Hybridization between diverging lineages is associated with the generation and loss of species diversity, introgression, adaptation, and changes in reproductive mode, but it is unknown when and why it results in these divergent outcomes. We estimate a comprehensive evolutionary network for the largest group of unisexual vertebrates and use it to understand the evolutionary outcomes of hybridization. Our results show that rates of introgression between species decrease with time since divergence and suggest that species must attain a threshold of evolutionary divergence before hybridization results in transitions to unisexuality. Rates of hybridization also predict genome-wide patterns of genetic diversity in whiptail lizards. These results distinguish among models for hybridization that have not previously been tested and suggest that the evolutionary outcomes can be predictable.

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards.

Viviparity, an innovation enhancing maternal control over developing embryos, has evolved >150 times in vertebrates, and has been proposed as an adaptation to inhabit cold habitats. Yet, the behavioral, physiological, morphological, and life history features associated with live-bearing remain unclear. Here, we capitalize on repeated origins of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with this innovation. Using data from 125 species and phylogenetic approaches, we find that viviparous phrynosomatids repeatedly evolved a more cool-adjusted thermal physiology than their oviparous relatives. Through precise thermoregulatory behavior viviparous phrynosomatids are cool-adjusted even in warm environments, and oviparous phrynosomatids warm-adjusted even in cool environments. Convergent behavioral shifts in viviparous species reduce energetic demand during activity, which may help offset the costs of protracted gestation. Whereas dam and offspring body size are similar among both parity modes, annual fecundity repeatedly decreases in viviparous lineages. Thus, viviparity is associated with a lower energetic allocation into production. Together, our results indicate that oviparity and viviparity are on opposing ends of the fast-slow life history continuum in both warm and cool environments. In this sense, the 'cold climate hypothesis' fits into a broader range of energetic/life history trade-offs that influence transitions to viviparity.

Interactions between thermoregulatory behavior and physiological acclimatization in a wild lizard population.

Although the importance of thermoregulation and plasticity as compensatory mechanisms for climate change has long been recognized, they have largely been studied independently. Thus, we know comparatively little about how they interact to shape physiological variation in natural populations. Here, we test the hypothesis that behavioral thermoregulation and thermal acclimatization interact to shape physiological phenotypes in a natural population of the diurnal lizard, Sceloporus torquatus. Every month for one year we examined thermoregulatory effectiveness and changes in the population mean in three physiological parameters: cold tolerance (Ctmin), heat tolerance (Ctmax), and the preferred body temperature (Tpref), to indirectly assess thermal acclimatization in population means. We discovered that S. torquatus is an active thermoregulator throughout the year, with body temperature varying little despite strong seasonal temperature shifts. Although we did not observe a strong signal of acclimatization in Ctmax, we did find that Ctmin shifts in parallel with nighttime temperatures throughout the year. This likely occurs, at least in part, because thermoregulation is substantially less effective at buffering organisms from selection on lower physiological limits than upper physiological limits. Active thermoregulation is effective at limiting exposure to extreme temperatures during the day, but is less effective at night, potentially contributing to greater plasticity in Ctmin than Ctmax. Importantly, however, Tpref tracked seasonal changes in temperature, which is one the factors contributing to highly effective thermoregulation throughout the year. Thus, behavior and physiological plasticity do not always operate independently, which could impact how organisms can respond to rising temperatures.

Complex patterns of hybridization and introgression across evolutionary timescales in Mexican whiptail lizards (Aspidoscelis).

Identifying patterns of introgression across the tree of life is foundational to understanding general mechanisms that govern the impacts of gene flow on the speciation process. There are few vertebrate groups in which hybridization is associated with as large a diversity of outcomes as in North American whiptail lizards (Aspidoscelis). Of particular interest is that hybridization among divergent whiptail species has repeatedly led to the formation of unisexual (parthenogenetic) lineages. Understanding the hybrid origin of these unisexual lineages requires an accurate understanding of species boundaries among gonochoristic whiptails. Doing so has historically been an extremely challenging problem which, in part, may be a consequence of widespread hybridization and incomplete reproductive isolation among lineages. The lack of a robust phylogenetic framework and uncertainty in species boundaries precludes studies of general patterns and mechanisms of introgression among whiptail species. Here, we use genomic data to reconstruct a robust estimate of evolutionary history in the largest clade of whiptail lizards (A. sexlineatus species group) and use it to identify patterns of introgression. Our results indicate substantial introgressive hybridization and admixture has occurred among multiple lineages of whiptails across diverse evolutionary time scales, and illustrate their impact on phylogenetic inference. Thus, hybridization among whiptail species appears to have been a prominent feature throughout their evolutionary history, which could, in part, explain why parthenogenesis has evolved so many times in whiptails in comparison to other vertebrate groups.

Integrative species delimitation in practice: Revealing cryptic lineages within the short-nosed skink Plestiodon brevirostris (Squamata: Scincidae).

Integrative taxonomy has been generally considered as a goal in systematics for more than a decade. Here, we employed environmental, molecular, and morphological data to evaluate the species boundaries within the short-nosed skink Plestiodon brevirostris from south-central Mexico, one member of the morphologically conservative P. brevirostris group. Our molecular dataset includes one mitochondrial and two nuclear loci. The mitochondrial fragment includes the full length of the gene coding for the NADH dehydrogenase subunit 1 protein, a segment of the gene coding for 16S ribosomal RNA, and flanking tRNAs. The nuclear dataset includes fragments of the genes coding for the megakaryoblastic leukemia 1 and RNA fingerprint 35 proteins. We employed phylogenetic reconstruction, analyses of population structure and morphological variation, and species delimitation methods (including the integration of the three kinds of data in a unified probabilistic framework) to evaluate species limits. Our results suggest that P. brevirostris represents four distinct species. The information provided by each kind of data allowed us to discern between alternative explanations for the observed patterns of geographic structure. Two of the newly recognized lineages are poorly differentiated morphologically but apparently differ in environmental preferences and are allopatric. Additionally, one lineage is microendemic and parapatric with respect to another one. Moreover, our phylogenetic analyses suggest that other taxa within the P. brevirostris group may represent species complexes. We discuss our results in the context of integrative species delimitation.

Implicaciones de la precipitación sobre la evolución del tamaño corporal y distancia interaxilar en el complejo Aspidoscelis gularis (Squamata: Teiidae) / Rainfall implications on body size evolution of Aspidoscelis gularis (Squamata: Teiidae)

ResumenLas historias de vida son atributos altamente variables que maximizan la adecuación de los organismos. Se ha documentado la relación del peso y el tamaño corporal sobre estos atributos, los cuales además estan influidos por variaciones ambientales y la heterogeneidad del hábitat. El tamaño y forma corporal son considerados atributos de historia de vida, los cuales estan principalmente asociados a la precipitación que promueve la cantidad de recursos disponibles en el ambiente. En el género Aspidoscelis el tamaño y masa relativa de la nidada estan asociados principalmente a la latitud y altitud. En Aspidoscelis gularis la precipitación de invierno favorece dos temporadas reproductoras, lo que determina que el tamaño de nidada sea variable en cada puesta. Las muestras fueron tomadas de mayo-julio 2013 y mayo-septiembre 2015. Se obtuvieron un total de 65 individuos de los cuales se tomaron medidas de longitud del cuerpo y distancia interaxilar, así como muestras de tejido hepático para la extracción de ADN y obtener las relaciones filogenéticas con respecto a un análisis de Inferencia Bayesiana para posteriormente aplicar los Métodos Comparados Filogenéticos como señal filogenética, contrastes filogenéticamente independientes y la reconstrucción del carácter ancestral. Por lo tanto, nuestros resultados muestran que en el tamaño y forma del cuerpo existe poca señal filogenética, en tanto que los contrastes filogenéticamente independientes y la reconstrucción del carácter ancestral sugieren que los tamaños corporales pequeños están asociadas a localidades con mayor cantidad de precipitación, lo que puede estar relacionado con un establecimiento de la madurez sexual temprana lo cual es el reflejo de la talla máxima de los adultos. Además, de acuerdo a un ANOVA y un ANCOVA hubo diferencias estadísticamente significativas en el tamaño y forma corporal respectivamente, lo que promueve un sistema para la competencia sexual para machos y un sistema para la fecundidad en hembras. Estos resultados son importantes para determinar el efecto de la precipitación sobre algunas características de historia de vida, lo que indica que las lagartijas del complejo sureste del complejo A. gularis son capaces de enfrentar diferentes presiones de selección, impuestas por el ambiente.

AbstractLife history traits are highly variable attributes that maximize organisms's fitness. The relationship of weight and body size with environmental changes and habitat heterogeneity has been documented in previous reports; and size and body shapes are both considered life history attributes that are associated with rainfall, that boost available resources in the environment. While in Aspidoscelis genus, clutch size and relative mass are mainly associated with latitude and altitude, in Aspidoscelis gularis, winter rainfall favors two reproductive seasons, which may determine season variable clutch size. With the aim to study this, samplings were undertaken from May-July 2013, and May-September 2015. A total of 65 individuals lizards of the Southeast clade were obtained, and body length and interaxilar distance measurements were taken; furthermore, hepatic tissue samples were taken for DNA extraction, which allowed us to analyze phylogenetic relationships through a Bayesian Inference analysis, and subsequently, to apply Phylogenetic Comparative Methods (like phylogenetic signal, phylogenetically independent contrasts and reconstruction of ancestral character). Our results showed that there is a low phylogenetic signal regarding body size and shape, while the phylogenetically independent contrasts and reconstruction of ancestral characters suggest that small body sizes are associated to locations with highest rainfall. This can be associated to an establishment of an early sexual maturity, which reflects the maximum size of adults. Furthermore, according to an ANOVA and ANCOVA, there were statistically significant differences in body size and shape respectively, which promote a system for sexual competition for males and a system for fertility in females. These results were important to determine the effect of rainfall on some life history traits, pointing out that lizards of the Southeast clade, belonging to the A. gularis complex were able to face different selection pressures, determined by the environment.

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.