Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication

Abstract

Little is known about the genetic changes that distinguish domestic cat populations from their wild progenitors. Here we describe a high-quality domestic cat reference genome assembly and comparative inferences made with other cat breeds, wildcats, and other mammals. Based upon these comparisons, we identified positively selected genes enriched for genes involved in lipid metabolism that underpin adaptations to a hypercarnivorous diet. We also found positive selection signals within genes underlying sensory processes, especially those affecting vision and hearing in the carnivore lineage. We observed an evolutionary tradeoff between functional olfactory and vomeronasal receptor gene repertoires in the cat and dog genomes, with an expansion of the feline chemosensory system for detecting pheromones at the expense of odorant detection. Genomic regions harboring signatures of natural selection that distinguish domestic cats from their wild congeners are enriched in neural crest-related genes associated with behavior and reward in mouse models, as predicted by the domestication syndrome hypothesis. Our description of a previously unidentified allele for the gloving pigmentation pattern found in the Birman breed supports the hypothesis that cat breeds experienced strong selection on specific mutations drawn from random bred populations. Collectively, these findings provide insight into how the process of domestication altered the ancestral wildcat genome and build a resource for future disease mapping and phylogenomic studies across all members of the Felidae.Felis catus | domestication | genome T he domestic cat (Felis silvestris catus) is a popular pet species, with as many as 600 million individuals worldwide (1). Cats and other members of Carnivora last shared a common ancestor with humans ∼92 million years ago (2, 3). The cat family Felidae includes ∼38 species that are widely distributed across the world, inhabiting diverse ecological niches that have resulted in divergent morphological and behavioral adaptations (4). The earliest archaeological evidence for human coexistence with cats dates to ∼9.5 kya in Cyprus and ∼5 kya in central China (5, 6), during periods when human populations adopted more agricultural lifestyles. Given their sustained beneficial role surrounding vermin control since the human transition to agriculture, any selective forces acting on cats may have been minimal subsequent to their domestication. Unlike many other domesticated mammals bred for food, herding, hunting, or security, most of the 30-40 cat breeds originated recently, within the past 150 y, largely due to selection for aesthetic rather than functional traits.Previous studies have assessed breed differentiation (6, 7), phylogenetic origins of the domestic cat (8), and the extent of recent introgression between domestic cats and wildcats (9, 10). However, little is known regarding the impact of the domestication process within the genomes of modern cats and how this compares with genetic changes accompanying selection identified...

European wildcat populations are subdivided into five main biogeographic groups: consequences of Pleistocene climate changes or recent anthropogenic fragmentation?

“…2015) or variation at domestication genes identified through entire genome analyses (Montague et al. 2014; Tamazian et al. 2014) can potentially improve the detection of admixture ancestry.…”

“…Thus, we offer the time frames described in this study as a working hypothesis that could be tested when cat populations will be genotyped with larger panels of informative autosomal markers derived from entire genome sequences (Montague et al. 2014; Tamazian et al. 2014).…”

Development and application of CatFACS: Are human cat adopters influenced by cat facial expressions?

“…Caeiro) Cats have associated with humans for around 10,000 years (Hu et al, 2014). During this time, they have been subject to some degree of evolutionary selection processes, both natural and artificial (Yamaguchi et al, 2004;Driscoll et al, 2009a,b;Faure and Kitchener, 2009;Montague et al, 2014), that have resulted in the domestic species known to us today. Domestication is known to influence the morphology, behaviour and cognitive abilities of a species (Price, 1984;Driscoll et al, 2009a;Montague et al, 2014), but in the case of the domestic cat, researchers are only just starting to understand these modifications.…”

Effect of cognitive enrichment on behavior, mucosal immunity and upper respiratory disease of shelter cats rated as frustrated on arrival

“…Despite at least 4000 years of domestication (Serpell 2000) and even when socialized and fed by humans, some domestic cats have retained the drive to hunt and roam (Montague et al, 2014) and when living outdoors have a range which exceeds 1.7 km (Bradshaw, 1992). Although some cats adapt well to confinement to the home (Jongman, 2007), it is also clear that domestic cats can experience frustration in confinement, particularly in cages in animal shelters and laboratories.…”