The History of Farm Foxes Undermines the Animal Domestication Syndrome

Abstract

The Russian Farm-Fox Experiment is the best known experimental study in animal domestication. By subjecting a population of foxes to selection for tameness alone, Dimitry Belyaev generated foxes that possessed a suite of characteristics that mimicked those found across domesticated species. This 'domestication syndrome' has been a central focus of research into the biological pathways modified during domestication. Here, we chart the origins of Belyaev's foxes in eastern Canada and critically assess the appearance of domestication syndrome traits across animal domesticates. Our results suggest that both the conclusions of the Farm-Fox Experiment and the ubiquity of domestication syndrome have been overstated. To understand the process of domestication requires a more comprehensive approach focused on essential adaptations to human-modified environments. The Origins of Domestication SyndromeThe domestication syndrome describes a suite of behavioral and morphological characteristics consistently observed in domesticated populations. It was first described in animals (although not named as such) by Charles Darwin [1]. The term itself, coined by botanists in the early 1900s [2,3], was applied to animals in the 1980s [3]. Usage has risen dramatically since the mid-1990s, by more than 20-fold (see the supplemental information online) [4].The concept of a domestication syndrome is appealing. The grouping of a collection of traits allows easier identification and facilitates the definition of domesticated taxa. It also inspires a search for causal mechanisms, whether genetic or environmental, responsible for their collective appearance. Characteristics attributed to domestication syndrome vary, but include tamability (see Glossary), loss of reproductive seasonality, and changes in coat color, ear form, tail form, and craniofacial morphology (Figure 1) [1,[5][6][7][8][9][10][11][12][13].

Morphology does not covary with predicted behavioral correlations of the domestication syndrome in dogs

“…However, the ability of phenotypes in extant domesticates to provide insights about altered selection pressures during initial domestication is complicated by postdomestication selection events, that is, improvement traits (Olsen and Wendel 2013; Larson and Fuller 2014, Lord et al. 2019). Initial stages of domestication likely acted upon existing variation at multiple loci across the genome (Larson and Fuller 2014), but the breed‐specific morphology and behavior expressed in present day dog breeds were likely selected for postdomestication during breed formation.…”

“…If the latter is true, which seems likely for dogs, we must reevaluate our expectations of the DS and thereby also our assessment of DS traits in present day domesticates, as they have limited bearing of the initial selection pressures applied during domestication (Lord et al. 2019). Including contemporary populations of primitive canids, such as dingoes ( Canis dingo ), in future research efforts could provide further insight into the consequences of domestication, as they likely reflect the altered selection pressures during early stages domestication (Smith et al.…”

“…However, traits of the DS are not fully consistent with such hypotheses and recently support for the existence of a DS in animals has been called into question (Lord et al. 2019). First, DS traits are not evenly distributed among domesticated animals (Sánchez‐Villagra et al.…”

“…2014), it is currently not well resolved if present day dog traits are original domestication traits, that is, traits evolved as a consequence of altered selection pressures during the initial stages of domestication, or so‐called improvement traits that have been secondarily enhanced postdomestication during breed formation (sensu Olsen and Wendel 2013, Larson and Fuller 2014; Lord et al. 2019).…”

Genomics and Transcriptomics of Behaviour and Plumage Colouration

“…There is one particular aspect of domestication that has intrigued scientist for ages, most domestic animals resemble one another and seem to share key characteristics, such as coat colour, increased tameness and altered cranial morphology to name a few. This is known as the domestication syndrome, and it has also divided the opinion of researchers for just as long, see for instance (Lord, Larson, Coppinger, & Karlsson, 2020). I would like to take this opportunity to share my views on the matter.…”