Survival by genotype: patterns at Mc1r are not black and white at the White Sands ecotone.

Measuring links among genotype, phenotype and survival in the wild has long been a focus of studies of adaptation. We conducted a 4-year capture-recapture study to measure survival by genotype and phenotype in the Southwestern Fence Lizard (Sceloporus cowlesi) at the White Sands ecotone (transition area between white sands and dark soil habitats). We report several unanticipated findings. First, in contrast with previous work showing that cryptic blanched coloration in S. cowlesi from the heart of the dunes is associated with mutations in the melanocortin-1 receptor gene (Mc1r), ecotonal S. cowlesi showed minimal association between colour phenotype and Mc1r genotype. Second, the frequency of the derived Mc1r allele in ecotonal S. cowlesi appeared to decrease over time. Third, our capture-recapture data revealed a lower survival rate for S. cowlesi individuals with the derived Mc1r allele. Thus, our results suggest that selection at the ecotone may have favoured the wild-type allele in recent years. Even in a system where a genotype-phenotype association appeared to be black and white, our study suggests that additional factors - including phenotypic plasticity, epistasis, pleiotropy and gene flow - may play important roles at the White Sands ecotone. Our study highlights the importance of linking molecular, genomic and organismal approaches for understanding adaptation in the wild. Furthermore, our findings indicate that dynamics of natural selection can be particularly complex in transitional habitats like ecotones and emphasize the need for future research that examines the patterns of ongoing selection in other ecological 'grey' zones.

Comparative study of host response to chytridiomycosis in a susceptible and a resistant toad species.

In the past century, recently emerged infectious diseases have become major drivers of species decline and extinction. The fungal disease chytridiomycosis has devastated many amphibian populations and exacerbated the amphibian conservation crisis. Biologists are beginning to understand what host traits contribute to disease susceptibility, but more work is needed to determine why some species succumb to chytridiomycosis while others do not. We conducted an integrative laboratory experiment to examine how two toad species respond to infection with the pathogen Batrachochytrium dendrobatidis in a controlled environment. We selected two toad species thought to differ in susceptibility - Bufo marinus (an invasive and putatively resistant species) and Bufo boreas (an endangered and putatively susceptible species). We measured infection intensity, body weight, histological changes and genomewide gene expression using a custom assay developed from transcriptome sequencing. Our results confirmed that the two species differ in susceptibility with the more susceptible species, B. boreas, showing higher infection intensities, loss in body weight, more dramatic histological changes and larger perturbations in gene expression. We found key differences in skin expression responses in multiple pathways including upregulation of skin integrity-related genes in the resistant B. marinus. Together, our results show intrinsic differences in host response between related species, which are likely to be important in explaining variation in response to a deadly emerging pathogen in wild populations. Our study also underscores the importance of understanding differences among host species to better predict disease outcomes and reveal generalities about host response to emerging infectious diseases of wildlife.

Crossing the threshold: gene flow, dominance and the critical level of standing genetic variation required for adaptation to novel environments.

Genetic architecture plays an important role in the process of adaptation to novel environments. One example is the role of allelic dominance, where advantageous recessive mutations have a lower probability of fixation than advantageous dominant mutations. This classic observation, termed 'Haldane's sieve', has been well explored theoretically for single isolated populations adapting to new selective regimes. However, the role of dominance is less well understood for peripheral populations adapting to novel environments in the face of recurrent and maladaptive gene flow. Here, we use a combination of analytical approximations and individual-based simulations to explore how dominance influences the likelihood of adaptation to novel peripheral environments. We demonstrate that in the face of recurrent maladaptive gene flow, recessive alleles can fuel adaptation only when their frequency exceeds a critical threshold within the ancestral range.

Male territoriality and 'sex confusion' in recently adapted lizards at White Sands.

The evolution of intersexual interactions, like mate choice, during ecological speciation has received widespread attention. However, changes in intrasexual interactions, like male territoriality, during ecological divergence are largely unexamined. We conducted field experiments with adaptively diverged populations of the eastern fence lizard (Sceloporus undulatus) to determine whether territorial males behaved differently towards ecologically similar vs. dissimilar intruders. We performed trials with light-coloured males from White Sands, New Mexico and dark-coloured males from the surrounding desert. We found that intruders from White Sands elicited more aggression than intruders from dark-soil habitat. We also documented a case of 'sex confusion' where white-sand males courted dark-soil intruders. We found population differences in signalling patch size that can explain both aggression bias and sex misidentification. We argue that direct selection (for population recognition or optimal signal transmission) and indirect selection (by-products of ecological adaptation) should influence both intersexual and intrasexual interactions during ecological speciation.

Insights From Genomics Into Spatial and Temporal Variation in Batrachochytrium dendrobatidis.

Advances in genetics and genomics have provided new tools for the study of emerging infectious diseases. Researchers can now move quickly from simple hypotheses to complex explanations for pathogen origin, spread, and mechanisms of virulence. Here we focus on the application of genomics to understanding the biology of the fungal pathogen Batrachochytrium dendrobatidis (Bd), a novel and deadly pathogen of amphibians. We provide a brief history of the system, then focus on key insights into Bd variation garnered from genomics approaches, and finally, highlight new frontiers for future discoveries. Genomic tools have revealed unexpected complexity and variation in the Bd system suggesting that the history and biology of emerging pathogens may not be as simple as they initially seem.

Ecological release in White Sands lizards.

Ecological opportunity is any change that allows populations to escape selection from competition and predation. After encountering ecological opportunity, populations may experience ecological release: enlarged population size, broadened resource use, and/or increased morphological variation. We identified ecological opportunity and tested for ecological release in three lizard colonists of White Sands, New Mexico (Sceloporus undulatus, Holbrookia maculata, and Aspidoscelis inornata). First, we provide evidence for ecological opportunity by demonstrating reduced species richness and abundance of potential competitors and predators at White Sands relative to nearby dark soils habitats. Second, we characterize ecological release at White Sands by demonstrating density compensation in the three White Sands lizard species and expanded resource use in White Sands S. undulatus. Contrary to predictions from ecological release models, we observed directional trait change but not increased trait variation in S. undulatus. Our results suggest that ecological opportunity and ecological release can be identified in natural populations, especially those that have recently colonized isolated ecosystems.

Aging, mating, and the evolution of mtDNA heteroplasmy in Drosophila melanogaster.

Heteroplasmy, the presence of more than one type of mtDNA within cells, is common in animals and has been associated with aging and disease in humans. Changes in the frequencies of mtDNA variants between cell and animal generations thus bears on the evolution of mtDNA and the progression of diverse pathologies. We have used densitometry of Southern blots of individual heteroplasmic Drosophila melanogaster to study the effects of age, increased egg production after mating, and temperature on evolution of heteroplasmy within and between generations. The frequency of the longer mtDNA variant consistently increased between early and late cohorts of F1 offspring derived from 18 independent heteroplasmic mothers as they aged. Neither temperature (flies maintained at 25 degrees C and 18 degrees C) nor the holding of flies as virgins for 10 days before mating had significant effects on transmission patterns. However, at the ends of their lives, flies that had laid eggs at 25 degrees C had a greater frequency of the long mtDNA than did their siblings who had laid eggs at 18 degrees C. The evolution of heteroplasmy within a generation was studied in samples of siblings that either were mated or held as virgins, and then scored for mtDNA haplotype frequencies at two different ages (day 2 and day 14). Mated flies showed a significantly greater increase in the frequency of the long mtDNA variant with age than did the unmated flies. This system provides a model for the joint analysis of generational and chronological age in the transmission dynamics of a molecular polymorphism.