In an era of unprecedented global change, exploring patterns of gene expression among wild populations across their geographic range is crucial for characterizing adaptive potential. RNA-sequencing studies have successfully characterized gene expression differences among populations experiencing divergent environmental conditions in a wide variety of taxa. However, few of these studies have identified transcriptomic signatures to multivariate, environmental stimuli among populations in their natural environments. Herein, we aim to identify environmental and sex-driven patterns of gene expression in the Tasmanian devil (Sarcophilus harrisii), a critically endangered species that occupies a heterogeneous environment. We performed RNA-sequencing on ear tissue biopsies from adult male and female devils from three populations at the extremes of their geographic range. There were no transcriptome-wide patterns of differential gene expression that would be suggestive of significant, environmentally-driven transcriptomic responses. The general lack of transcriptome-wide variation in gene expression levels across the devil's geographic range is consistent with previous studies that documented low levels of genetic variation in the species. However, genes previously implicated in local adaptation to abiotic environment in devils were enriched for differentially expressed genes. Additionally, three modules of co-expressed genes were significantly associated with either population of origin or sex.

Identifying the genetic architecture of complex phenotypes is a central goal of modern biology, particularly for disease-related traits. Genome-wide association methods are a classical approach for identifying the genomic basis of variation in disease phenotypes, but such analyses are particularly challenging in natural populations due to sample size difficulties. Extensive mark-recapture data, strong linkage disequilibrium and a lethal transmissible cancer make the Tasmanian devil (Sarcophilus harrisii) an ideal model for such an association study. We used a RAD-capture approach to genotype 624 devils at ~16,000 loci and then used association analyses to assess the heritability of three cancer-related phenotypes: infection case-control (where cases were infected devils and controls were devils that were never infected), age of first infection and survival following infection. The SNP array explained much of the phenotypic variance for female survival (>80%) and female case-control (>61%). We found that a few large-effect SNPs explained much of the variance for female survival (~5 SNPs explained >61% of the total variance), whereas more SNPs (~56) of smaller effect explained less of the variance for female case-control (~23% of the total variance). By contrast, these same SNPs did not account for a significant proportion of phenotypic variance in males, suggesting that the genetic bases of these traits and/or selection differ across sexes. Loci involved with cell adhesion and cell-cycle regulation underlay trait variation, suggesting that the devil immune system is rapidly evolving to recognize and potentially suppress cancer growth through these pathways. Overall, our study provided necessary data for genomics-based conservation and management in Tasmanian devils.