Neuroendocrine correlates of juvenile amphibian behaviors across a latitudinal cline.

We assessed the macrogeographic and neuroendocrine correlates of behavioral variation exhibited by juveniles, an important life stage for dispersal, across the expansive range of the wood frog. By rearing animals from eggs in a common garden then using a novel environment test, we uniquely demonstrated differential expression of juvenile behaviors among 16 populations spanning 8° latitude. On the individual level, cluster analysis indicated three major behavior profiles and principal component analysis resolved four unique axes of behavior, including escape, foraging, food intake, feeding efficiency. We found that increased escape behavior was associated with lower adrenocorticotropic hormone (ACTH)-induced circulating corticosterone (CORT) levels, however, foraging and food intake behaviors were not associated with either resting or ACTH-induced CORT. At the population level, the expression of foraging behaviors increased with latitude while food intake behaviors declined with latitude, which raised several hypotheses of eco-evolutionary processes likely driving this variation. Given that these behaviors covary along the same ecological gradient as locally adapted developmental traits, genomic studies in this species could provide deep insights into how HPA/I activity is associated with the eco-evolutionary processes that structure intraspecific variation in morphology and behavior.

Ecological adaptation drives wood frog population divergence in life history traits.

Phenotypic variation among populations is thought to be generated from spatial heterogeneity in environments that exert selection pressures that overcome the effects of gene flow and genetic drift. Here, we tested for evidence of isolation by distance or by ecology (i.e., ecological adaptation) to generate variation in early life history traits and phenotypic plasticity among 13 wood frog populations spanning 1200 km and 7° latitude. We conducted a common garden experiment and related trait variation to an ecological gradient derived from an ecological niche model (ENM) validated to account for population density variation. Shorter larval periods, smaller body weight, and relative leg lengths were exhibited by populations with colder mean annual temperatures, greater precipitation, and less seasonality in precipitation and higher population density (high-suitability ENM values). After accounting for neutral genetic variation, the QST-FST analysis supported ecological selection as the key process generating population divergence. Further, the relationship between ecology and traits was dependent upon larval density. Specifically, high-suitability/high-density populations in the northern part of the range were better at coping with greater conspecific competition, evidenced by greater postmetamorphic survival and no difference in body weight when reared under stressful conditions of high larval density. Our results support that both climate and competition selection pressures drive clinal variation in larval and metamorphic traits in this species. Range-wide studies like this one are essential for accurate predictions of population's responses to ongoing ecological change.

Urbanization and Population Genetic Structure of the Panama City crayfish (Procambarus econfinae).

For species with geographically restricted distributions, the impacts of habitat loss and fragmentation on long-term persistence may be particularly pronounced. We examined the genetic structure of Panama City crayfish (PCC), Procambarus econfinae, whose historical distribution is limited to an area approximately 145 km2, largely within the limits of Panama City and eastern Bay County, FL. Currently, PCC occupy approximately 28% of its historical range, with suitable habitat composed of fragmented patches in the highly urbanized western portion of the range and managed plantations in the more contiguous eastern portion of the range. We used 1640 anonymous single-nucleotide polymorphisms to evaluate the effects of anthropogenic habitat modification on the genetic diversity and population structure of 161 PCC sampled from across its known distribution. First, we examined urban habitat patches in the west compared with less-developed habitat patches in the east. Second, we used approximate Bayesian computation to model inferences on the demographic history of eastern and western populations. We found anthropogenic habitat modifications explain the genetic structure of PCC range-wide. Clustering analyses revealed significant genetic structure between and within eastern and western regions. Estimates of divergence between east and west were consistent with urban growth in the mid-20th century. PCC have low genetic diversity and high levels of inbreeding and relatedness, indicating populations are small and isolated. Our results suggest that PCC have been strongly affected by habitat loss and fragmentation and management strategies, including legal protection, translocations, or reintroductions, may be necessary to ensure long-term persistence.

Geophysiology of Wood Frogs: Landscape Patterns of Prevalence of Disease and Circulating Hormone Concentrations across the Eastern Range.

One of the major challenges for conservation physiologists is to determine how current or future environmental conditions relate to the health of animals at the population level. In this study, we measured prevalence of disease, mean condition of the body, and mean resting levels of corticosterone and testosterone in a total of 28 populations across the years 2011 and 2012, and correlated these measures of health to climatic suitability of habitat, using estimates from a model of the ecological niche of the wood frog's geographic range. Using the core-periphery hypothesis as a theoretical framework, we predicted a higher prevalence and intensity of infection of Batrachochytrium dendrobatidis (Bd) and ranaviruses, two major amphibian pathogens causing disease, and higher resting levels of circulating corticosterone, an indicator of allostatic load incurred from living in marginal habitats. We found that Bd infections were rare (2% of individuals tested), while infections with ranavirus were much more common: ranavirus-infected individuals were found in 92% of ponds tested over the 2 years. Contrary to our predictions, rates of infection with ranaviruses were positively correlated with quality of the habitat with the highest prevalence at the core of the range, and plasma corticosterone concentrations measured when frogs were at rest were not correlated with quality of the habitat, the prevalence of ranavirus, or the intensity of infection. Prevalence and mean viral titers of ranavirus infection were higher in 2012 than in 2011, which coincided with lower levels of circulating corticosterone and testosterone and an extremely early time of breeding due to relatively higher temperatures during the winter. In addition, the odds of having a ranavirus infection increased with decreased body condition, and if animals had an infection, viral titers were positively correlated to levels of circulating testosterone concentration. By resolving these patterns, experiments can be designed to test hypotheses about the mechanisms that produce them, such as whether transmission of the ranavirus and tolerance of the host are greater or whether virulence is lower in populations within core habitats. While there is debate about which metrics serve as the best bioindicators of population health, the findings of this study demonstrate the importance of long-term monitoring of multiple physiological parameters to better understand the dynamic relationship between the environment and the health of wildlife populations over space and time.

History matters more when explaining genetic diversity within the context of the core-periphery hypothesis.

The core-periphery hypothesis (CPH) predicts that populations located at the periphery of a species' range should have lower levels of genetic variation than those at the centre of the range. However, most of the research on the CPH focuses on geographic distance and not on ecological distance, or uses categorical definitions of core and periphery to explain the distribution of genetic diversity. We use current climate data and historical climate data from the last glacial maxima to develop quantitative estimates of contemporary and historical ecological suitability using ecological niche models. We analysed genetic diversity using 12 polymorphic microsatellites to estimate changes in heterozygosity, allelic richness and population differentiation in 31 populations of the wood frog (Lithobates sylvaticus) spanning the species' entire eastern clade (33(o) to 45(o) latitude) from Alabama, USA, to Nova Scotia, Canada. Our data support predictions based on the CPH. Populations showed significant differences in genetic diversity across the range, with lower levels of genetic variation at the geographic range edge and in areas with lower levels of historical and contemporary ecological suitability. However, history and geography (not current ecological suitability) best explain the patterns. This study highlights the importance of examining more than just geography when assessing the CPH, and the importance of historical ecological suitability in the maintenance of genetic diversity and population differentiation.

Preparing the "new" biologist of the future: student research at the interface of mathematics and biology.

We describe a unique Research Experience for Undergraduates and Research Experience for Veterinary students summer program at the National Institute for Mathematical and Biological Synthesis on the campus of the University of Tennessee, Knoxville. The program focused on interdisciplinary research at the interface of biology and mathematics. Participants were selected to work on projects with a biology mentor and a mathematics mentor in an environment that promoted collaboration outside of the students' respective disciplines. There were four research projects with teams of four participants and two faculty mentors. The participants consisted of a mixture of 10 undergraduates in biology- and mathematics-related disciplines, four veterinary students, and two high-school teachers. The activities included lectures on both the biological and mathematical backgrounds of the projects, tutorials for software, and sessions on ethics, graduate school, and possible career paths for individuals interested in biology and mathematics. The program was designed to give students the ability to actively participate in the scientific research process by working on a project, writing up their results in a final report, and presenting their work orally. We report on the results of our evaluation surveys of the participants.

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus.

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an 'asocial' phenotype with solitary female nests and a 'social' phenotype with multi-female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half-siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.