Christian L. Cox

Matched regulation of gastrointestinal performance in the Burmese python,Python molurus

SUMMARY In Burmese pythons fasting and feeding cause dramatic regulation of gastric acid production and intestinal nutrient uptake. Predictably, other components of their gastrointestinal tract are similarly regulated with each meal. We therefore assessed the matched regulation of gastrointestinal performance by comparing the postprandial activities and capacities of gastric (pepsin), pancreatic (amylase and trypsin) and intestinal (aminopeptidase-N and maltase) enzymes, and intestinal nutrient uptake. Tissue samples were collected from pythons fasted and at 0.25, 0.5, 1, 2, 3, 4, 6, 10 and 15 days following their consumption of rodent meals equaling 25% of snake body mass. With feeding, pythons experience no significant change in stomach mass, whereas both the pancreas and small intestine doubled in mass. Feeding also triggered a depletion of gastric mucosal pepsinogen, a respective 5.7- and 20-fold increase in the peak activities of pancreatic trypsin and amylase, and a respective 2.3- and 5.5-fold increase in the peak activities of intestinal maltase and aminopeptidase-N. Enzyme activities peaked between 2 and 4 days postfeeding and returned to fasting levels by day 10. Independent of digestive stage, python intestine exhibited a proximal to distal decline in enzyme activity. For both sugars and proteins, intestinal capacities for enzyme activity were significantly correlated with nutrient uptake capacities. The concomitant postprandial upregulation of tissue morphology, intestinal nutrient transport rates and enzyme activities illustrate, for the python, the matched regulation of their gastrointestinal performance with each meal.

The fitness consequences of the autotomous blue tail in lizards: an empirical test of predator response using clay models.

Numerous vertebrates employ one or more autotomous body parts as an anti-predation mechanism. Many lizards possess an autotomous tail that is brightly colored blue, which has been suggested to either serve as a decoy mechanism to divert predator attention to the autotomous body part, as an interspecific signal, or as an aposematic signal to predators that it is distasteful or dangerous. While theoretical studies suggest that a conspicuous autotomous body part that increases the probability of escape while not increasing the rate of detection will be favorable over a completely cryptic form, there is little empirical evidence supporting the adaptive benefit of an autotomous blue tail. We used in situ clay models of a scincid lizard to test the fitness consequences of blue coloration. Lizard models with a dark base color and blue decoy coloration experienced no measurable difference in avian predation relative to an all-dark model, which suggests that blue coloration neither serves as an aposematic signal nor increases the conspicuousness of the lizard model. Despite statistically similar attack rates, avian attacks on models with blue coloration were indeed focused on body sections that were colored blue. Our results suggest that the blue tail in lizards serves as an effective decoy, and that avian predation has possibly played a role in the evolution of the blue tail.

Spatial and Temporal Drivers of Phenotypic Diversity in Polymorphic Snakes

Color polymorphism in natural populations presents an ideal opportunity to study the evolutionary drivers of phenotypic diversity. Systems with striking spatial, temporal, and qualitative variation in color can be leveraged to study the mechanisms promoting the distribution of different types of variation in nature. We used the highly polymorphic ground snake (Sonora semiannulata), a putative coral snake mimic with both cryptic and conspicuous morphs, to compare patterns of neutral genetic variation and variation over space and time in color polymorphism to investigate the mechanistic drivers of phenotypic variation across scales. We found that strong selection promotes color polymorphism across spatial and temporal scales, with morph frequencies differing markedly between juvenile and adult age classes within a single population, oscillating over time within multiple populations, and varying drastically over the landscape despite minimal population genetic structure. However, we found no evidence that conspicuousness of morphs was related to which color pattern was favored by selection or to any geographic factors, including sympatry with coral snakes. We suggest that complex patterns of phenotypic variation in polymorphic systems may be a fundamental outcome of the conspicuousness of morphs and that explicit tests of temporal and geographic variation are critical to the interpretation of conspicuousness and mimicry.

Analyzing the relationship between sequence divergence and nodal support using Bayesian phylogenetic analyses.

Determining the appropriate gene for phylogeny reconstruction can be a difficult process. Rapidly evolving genes tend to resolve recent relationships, but suffer from alignment issues and increased homoplasy among distantly related species. Conversely, slowly evolving genes generally perform best for deeper relationships, but lack sufficient variation to resolve recent relationships. We determine the relationship between sequence divergence and Bayesian phylogenetic reconstruction ability using both natural and simulated datasets. The natural data are based on 28 well-supported relationships within the subphylum Vertebrata. Sequences of 12 genes were acquired and Bayesian analyses were used to determine phylogenetic support for correct relationships. Simulated datasets were designed to determine whether an optimal range of sequence divergence exists across extreme phylogenetic conditions. Across all genes we found that an optimal range of divergence for resolving the correct relationships does exist, although this level of divergence expectedly depends on the distance metric. Simulated datasets show that an optimal range of sequence divergence exists across diverse topologies and models of evolution. We determine that a simple to measure property of genetic sequences (genetic distance) is related to phylogenic reconstruction ability in Bayesian analyses. This information should be useful for selecting the most informative gene to resolve any relationships, especially those that are difficult to resolve, as well as minimizing both cost and confounding information during project design.

Rapid range expansion in the Great Plains narrow-mouthed toad (Gastrophryne olivacea) and a revised taxonomy for North American microhylids

We investigated genetic variation within the Great Plains narrow-mouthed toad, Gastrophryne olivacea, across its geographic range in the United States and Mexico. An analysis of mitochondrial DNA (mtDNA) from 105 frogs revealed remarkably low levels of genetic diversity in individuals inhabiting the central United States and northern Mexico. We found that this widespread matrilineal lineage is divergent (ca. 2% in mtDNA) from haplotypes that originate from the western United States and western coast of Mexico. Using a dataset that included all five species of Gastrophryne and both species of the closely related genus Hypopachus, we investigated the phylogenetic placement of G. olivacea. This analysis recovered strong support that G. olivacea, the tropically distributed G. elegans, and the temperately distributed G. carolinensis constitute a monophyletic assemblage. However, the placement of G. pictiventris and G. usta render Gastrophryne paraphyletic with respect to Hypopachus. To complement our mitochondrial analysis, we examined a small fragment of nuclear DNA and recovered consistent patterns. In light of our findings we recommend (1) the resurrection of the nomen G. mazatlanensisTaylor (1943) for the disjunct western clade of G. olivacea and (2) the tentative placement of G. pictiventris and G. usta in Hypopachus. To explore possible scenarios leading to low levels of genetic diversity in G. olivacea, we used mismatch distributions and Bayesian Skyline plots to examine historic population expansion and demography. Collectively these analyses suggest that G. olivacea rapidly expanded in effective population size and geographic range during the late Pleistocene or early Holocene. This hypothesis is consistent with fossil data from northern localities and contemporary observations that suggest ongoing northern expansion. Given our findings, we suspect that the rapid range expansion of G. olivacea may have been facilitated by ecological associations with open habitats and seasonal water bodies.

Integrated Postprandial Responses of the Diamondback Water Snake, Nerodia rhombifer

Among snakes, the magnitude to which intestinal performance is regulated with feeding and fasting is adaptively linked to their natural feeding frequency. For infrequently feeding boas and pythons, gastrointestinal form and function are widely regulated with each feeding bout. In contrast, snakes that naturally feed more frequently modestly regulate intestinal function with each meal. To further explore the postprandial responses of a frequently feeding snake and assess whether such responses are matched in magnitude, we examined the postprandial metabolic, morphologic, and functional responses of the diamondback water snake (Nerodia rhombifer) following the consumption of catfish meals equaling 25% of their body mass. After feeding, N. rhombifer experienced 5.4‐fold increases in metabolic rate and a specific dynamic action of 101 kJ that equaled 25.3% of the ingested energy. Nerodia rhombifer that were fed did not undergo any change in stomach tissue mass but did experience a rapid drop in gastric pH and a decline in tissue stores of pepsinogen. Feeding triggered an increase in pancreatic mass and a temporary loss of trypsin activity. The small intestine of N. rhombifer responded to feeding with a 70% increase in mass and a 27% increase in enterocyte length but no change in microvillus length. Intestinal nutrient uptake rates did not increase with feeding, whereas intestinal aminopeptidase‐N activity increased by fivefold. The postprandial increases in metabolism and gastrointestinal morphology and function of N. rhombifer are of a lower magnitude than is characteristic of infrequently feeding snakes and are more similar to the responses observed for other frequently feeding species. In support of an adaptive interplay between feeding habits and digestive physiology, this study demonstrates that the regulation of gastrointestinal structure and function for the frequently feeding N. rhombifer is generally modest and matched in magnitude.

Female anoles retain responsiveness to testosterone despite the evolution of androgen‐mediated sexual dimorphism

Summary 1. The evolution of sexual dimorphism presents a challenge because males and females must express two phenotypes from the same underlying genome. In vertebrates, one solution to this challenge is to link the expression of shared traits to sex steroids. However, even ‘male-biased’ steroids such as testosterone (T) circulate at biologically significant levels in females, raising the question of whether sexual dimorphism evolves not only through the coupling of trait expression to T in males, but also through the decoupling of trait expression from T in females. 2. We tested these alternatives by asking whether male and female brown anoles (Anolis sagrei) respond to exogenous T in similar fashion with respect to a suite of sexually dimorphic traits: growth, skeletal morphology, resting metabolism, fat storage, dewlap size and dewlap colour. 3. First, we established the ontogeny of sexual dimorphism in a colony raised in a laboratory common garden. Next, we treated juveniles of each sex with either T implants or empty implants at 5–8 months of age, when sexual dimorphism first began to develop for most traits. 4. T stimulated growth in both sexes and largely abolished natural sex differences in growth. This effect was associated with the stimulation of resting metabolism and the diversion of energy from fat and liver stores in both sexes. T also enlarged the dewlap in both sexes, though females never developed dewlaps equal in size to those of males. Finally, T altered the brightness and saturation of the dewlap in both sexes, inducing coloration similar to that of adult males. 5. Female brown anoles retain many of the same tissue-specific responses to T that occur in males, suggesting that the evolution of androgen-mediated sexual dimorphism has been achieved largely through the coupling of trait expression to sex differences in circulating T, without an associated decoupling of trait expression from T in females.

Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles.

Aridity is an important determinant of species distributions, shaping both ecological and evolutionary diversity. Lizards and snakes are often abundant in deserts, suggesting a high potential for adaptation or acclimation to arid habitats. However, phylogenetic evidence indicates that squamate diversity in deserts may be more strongly tied to speciation within arid habitats than to convergent evolution following repeated colonization from mesic habitats. To assess the frequency of evolutionary transitions in habitat aridity while simultaneously testing for associated changes in water‐balance physiology, we analyzed estimates of total evaporative water loss (EWL) for 120 squamate species inhabiting arid, semiarid, or mesic habitats. Phylogenetic reconstructions revealed that evolutionary transitions to and from semiarid habitats were much more common than those between arid and mesic extremes. Species from mesic habitats exhibited significantly higher EWL than those from arid habitats, while species from semiarid habitats had intermediate EWL. Phylogenetic comparative methods confirmed this association between habitat aridity and EWL despite phylogenetic signal in each. Thus, the historical colonization of arid habitats by squamates is repeatedly associated with adaptive changes in EWL. This physiological convergence, which may reflect both phenotypic plasticity and genetic adaptation, has likely contributed to the success of squamates in arid environments.

Non-linear scaling of oxygen consumption and heart rate in a very large cockroach species (Gromphadorhina portentosa): correlated changes with body size and temperature

SUMMARY Although well documented in vertebrates, correlated changes between metabolic rate and cardiovascular function of insects have rarely been described. Using the very large cockroach species Gromphadorhina portentosa, we examined oxygen consumption and heart rate across a range of body sizes and temperatures. Metabolic rate scaled positively and heart rate negatively with body size, but neither scaled linearly. The response of these two variables to temperature was similar. This correlated response to endogenous (body mass) and exogenous (temperature) variables is likely explained by a mutual dependence on similar metabolic substrate use and/or coupled regulatory pathways. The intraspecific scaling for oxygen consumption rate showed an apparent plateauing at body masses greater than about 3 g. An examination of cuticle mass across all instars revealed isometric scaling with no evidence of an ontogenetic shift towards proportionally larger cuticles. Published oxygen consumption rates of other Blattodea species were also examined and, as in our intraspecific examination of G. portentosa, the scaling relationship was found to be non-linear with a decreasing slope at larger body masses. The decreasing slope at very large body masses in both intraspecific and interspecific comparisons may have important implications for future investigations of the relationship between oxygen transport and maximum body size in insects.

Molecular systematics of the genus Sonora (Squamata: Colubridae) in central and western Mexico

Mexico possesses high levels of endemic biodiversity, especially for squamate reptiles. However, the evolutionary relationships among many reptiles in this region are not well known. The closely related genera of Sonora Baird and Girard 1853 and Procinura Cope 1879 are coralsnake mimics found from the central and western United States to southwestern Mexico and Baja California. Although species delimitation in this group has historically relied upon colour pattern and other morphological characters, many populations of these species display colour pattern polymorphism, which may confound taxonomy. We used molecular phylogenetics to assess the evolutionary relationships and delimit species within Sonora, focusing on the phylogenetic position of Procinura and the validity of S. mutabilis and aequalis. We sequenced two mitochondrial (ND4 and cytb) and two nuclear (c-mos and RAG-1) genes for the single species of Procinura and each of the four species of Sonora. We analysed these sequences using maximum parsimony, maximum likelihood and Bayesian phylogenetic analyses on separately concatenated mitochondrial and nuclear datasets. Additionally, we used Bayesian coalescent methods to build a species tree (Bayesian species tree analysis) and delimit species boundaries (Bayesian species delimitation). All methods indicated that Procinura is deeply nested within Sonora, and most individual species are well supported. However, we found that one taxon (S. aequalis) is paraphyletic with regard to another (S. mutabilis). We recommend that the genus Procinura be synonymised with Sonora and that S. aequalis be synonymised with S. mutabilis. Additionally, the phylogenetic patterns that we document are broadly congruent with a Miocene or Pliocene divergence between S. michoacanensis and S. mutabilis along the Trans-Mexican Volcanic Belt. Finally, our data are consistent with the early evolution of coralsnake mimicry and colour pattern polymorphism within the genus Sonora.