Contemporary and historical selection in Tasmanian devils (Sarcophilus harrisii) support novel, polygenic response to transmissible cancer

Abstract

Tasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. We used a targeted sequencing approach, RAD-capture, to identify genomic regions subject to rapid evolution in approximately 2,500 devils as DFTD spread across the species range. We found evidence for genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. We then searched for signatures of recurrent selection with a molecular evolution approach and found widespread evidence of historical positive selection in devils relative to other marsupials. We identified both contemporary and historical selection in 19 genes and enrichment for contemporary and historical selection independently in 22 gene sets. Nonetheless, the overlap between candidates for historical selection and for contemporary response to DFTD was lower than expected, supporting novelty in the evolutionary response of devils to DFTD. Our results can inform management actions to conserve adaptive capacity of devils by identifying high priority targets for genetic monitoring and maintenance of functional diversity in managed populations.

Contemporary and historical selection in Tasmanian devils ( Sarcophilus harrisii ) support novel, polygenic response to transmissible cancer

“…gov/bioproject/?term=PRJNA306495) and BioProject PRJNA634071 (http://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA634071). Code and tabular results are available at https://github.com/ Astahlke/contemporary_historical_sel_devils and on the Dryad Digital Repository: https://doi.org/10.5061/dryad.jq2bvq872 [92].…”

Utility and challenges of using whole‐genome resequencing to detect emerging insect and mite resistance in agroecosystems

“…Yet tracking changes within the same population before and after exposure to a novel selection pressure provides the most powerful evidence of response to selection. In natural systems, temporal genome scanning experiments have identified strong allele frequency shifts over the course of a few to dozens of generations (e.g., Bergland et al, 2014; Bi et al, 2013, 2019; Campbell‐Staton et al, 2017; Chaturvedi et al, 2021; Ergon et al, 2019; Mikheyev et al, 2015; Schiebelhut et al, 2018; Stahlke et al, 2021). Further study (e.g., QTL analysis, genome‐wide association studies [GWAS]) is required to causally link putative targets of selection to adaptive phenotypes (Jones et al, 2012; Price et al, 2018; Tiffin & Ross‐Ibarra, 2014).…”

“…Further study (e.g., QTL analysis, genome‐wide association studies [GWAS]) is required to causally link putative targets of selection to adaptive phenotypes (Jones et al, 2012; Price et al, 2018; Tiffin & Ross‐Ibarra, 2014). A small but growing number of studies have taken this extra step to establish or link published functional support to candidate targets of selection (Bergland et al, 2014; Campbell‐Staton et al, 2017; Chaturvedi et al, 2021; Mikheyev et al, 2015; Stahlke et al, 2021), documenting that strong adaptive temporal shifts in allele frequency at multiple genomic loci can be observed on short time scales. Although sampling intervals varied by study (range = ca.…”

“…Recent successful detection of genomic responses to selection in natural systems over the course of a few generations (Bergland et al, 2014; Campbell‐Staton et al, 2017; Chaturvedi et al, 2021; Mikheyev et al, 2015; Stahlke et al, 2021) as well as evidence that the strength and detectability of responses to selection do not necessarily differ between natural and agricultural systems suggests that genomic approaches hold promise for detection of resistance evolution. Indeed, several recent studies have used genome scanning of field‐collected pests to identify genes under selection by pesticides (Calla et al, 2021; Crossley et al, 2017; Gimenez et al, 2020; Kamdem et al, 2017; Pélissié et al, 2022; Taylor et al, 2021; Weedall et al, 2020).…”

“…When sampled geographically, such structure could hamper detection of resistance evolution by using temporal genome scanning. Careful sampling design, including use of paired treated and untreated plots in more geographic locations, as well as analytical approaches to accommodate population genetic structure (Stahlke et al, 2021) may be important if genomic monitoring is to be used for species with low rates of migration and gene flow (see below).…”