Genomic analysis of dingoes identifies genomic regions under reversible selection during domestication and feralization

Abstract

Dingoes (Canis dingo) are wild canids living in Australia. They have lived isolated from both the wild and the domestic ancestor and are a unique model for studying feralization, the process in which a domestic species escapes human control, adapts to the wild, and diverges from the domestic ancestor into a genetically distinct population.Here, we sequenced the genomes of 10 dingoes and 2 New Guinea Singing Dogs, to study the origins and feralization process of the dingo. Phylogenetic and demographic analyses show that dingoes originate from domestic dogs in southern East Asia, which migrated via Island Southeast Asia to reach Australia 4300-5000 years ago, and subsequently diverged into a genetically distinct population. Selection analysis identified 99 positively selected genes enriched in starch and fat metabolism pathways, indicating a diet change during feralization of dingoes. Interestingly, we found that 14 genes have shifted allele frequencies compared to dogs but not compared to wolves.This suggests that the selection affecting these genes during domestication of the wolf was reversed in the feralization process. One of these genes, ARHGEF7, may promote the formation of neural spine and synapses in hippocampal neurons. Functional assays showed that an A to G mutation in ARHGEF7, located in a transcription factor-binding site, decreases the endogenous expression. This suggests that ARHGEF7 may have been under selection for behavioral adaptations related to the transitions in environment both from wild to domestic and from domestic back to wild.Our results indicate that adaptation to domestication and feralization primarily affected different genomic regions, but that some genes, related to neurodevelopment, metabolism and reproduction, may have been reversibly affected in the two processes.

Taxonomic status of the Australian dingo: the case for Canis dingo Meyer, 1793

“…Instead, dingoes likely came as an earlier radiation of dogs, presumably associated with human hunter-gatherers, reaching Australia on one or more occasions (and possibly even without human intervention). This is consistent with Y-chromosome modelling that indicates dingoes are an older radiation than dogs found on the islands of Southeast Asia (Sacks et al 2013;Zhang et al (2018).…”

“…Today, based on the recent exceptional advances in DNA technology, sequencing of the entire nuclear genome and analysis using genome-wide high density SNP panels offer powerful tools for distinguishing dingoes from other canids (vonHoldt et al 2010;Freedman et al 2014;Cairns 2015). These analyses show that dingoes are a highly divergent, ancient dog lineage (vonHoldt et al 2010;Freedman et al 2014;Cairns & Wilton 2016;, Zhang et al 2018. For example, principal component analysis based on whole-genome SNPs distinguishes dingoes from other canid populations: village dogs and modern breed dogs, as well as wolves (Fig.…”

“…This is in agreement with morphological analyses based on measurements taken of dingo, wolf, and dog skulls (Gollan 1982). Although descended from a dog-like ancestor, according to a variety of genetic markers dingoes are genetically distinct from modern dogs, including Asian village dogs, and share some genetic signatures with Asian wolves (Savolainen et al 2004;vonHoldt et al 2010;Sacks et al 2013;Freedman et al 2014;Cairns & Wilton 2016;, Zhang et al 2018. Mitochondrial and Y-chromosome data indicate that dingoes are closely related to Southeast Asian dogs (Savolainen et al 2004;Oskarsson et al 2011;Ardalan et al 2012;Sacks et al 2013).…”

“…Still, the early genetic research found that the reference dingo and domestic dog populations are genetically distinct, and suggested that introgression of dog genes in the reference dingo population was low (Wilton et al 1999;Wilton 2001, Zhang et al 2018. Advances in technology have improved the original method by applying Bayesian clustering, reducing the reliance on a small, pre-defined dingo or domestic dog reference sample (Stephens 2011;Stephens et al 2015).…”

“…Indeed, it is also uncertain what the wild ancestor of the dingo was, because dingoes do not sit within any extant wolf clade. Dingoes do bear a resemblance to village dogs in Asia, but can be easily distinguished by their DNA (Savolainen et al 2004;Oskarsson et al 2011;Sacks et al 2013;Cairns & Wilton 2016, Zhang et al 2018, as well as their morphology (e.g., larger size and cranial measurements; Corbett 1985), behaviour and lifestyle, consistent with limited domestication. In the following sections, we explore other independent lines of evidence that suggest the dingo and its ancestors were never truly domesticated.…”