Evaluating the roles of directed breeding and gene flow in animal domestication

Abstract

For the last 150 y scholars have focused upon the roles of intentional breeding and genetic isolation as fundamental to understanding the process of animal domestication. This analysis of ethnoarchaeological, archaeological, and genetic data suggests that long-term gene flow between wild and domestic stocks was much more common than previously assumed, and that selective breeding of females was largely absent during the early phases of animal domestication. These findings challenge assumptions about severe genetic bottlenecks during domestication, expectations regarding monophyletic origins, and interpretations of multiple domestications. The findings also raise new questions regarding ways in which behavioral and phenotypic domestication traits were developed and maintained.reproductive isolation | selected breeding | zooarchaeology | donkey | pig Domestication resulted in diverse phenotypic and behavioral changes to wild animals, including decreased flight responses, increased sociality, earlier reproduction, and modification of endocrine and metabolic systems (1-4). Darwin's (5) seminal research, heavily influenced by European animal breeding practices during the 19th century, led subsequent scholars studying animal domestication to prioritize the central roles of human intentionality, directed or controlled breeding of individuals, and genetic isolation of captive herds from wild relatives (6). This anthropocentric legacy is evident in various widely used definitions of domestication that emphasize isolation of captive animals from wild species and total human control over breeding and animal care (6-8). However, a growing body of archaeological, genetic, and ethnohistorical evidence discussed here shows that neither reproductive isolation nor intentional breeding of individuals was as significant as traditionally thought. Our findings indicate long-term gene flow between managed and wild animal populations, and little control of breeding of domestic females. These findings challenge assumptions about severe genetic bottlenecks during domestication and interpretations of genetic variability in terms of multiple instances of domestication. The findings also raise questions about ways in which behavioral and phenotypic domestication traits were maintained.Research into dog and pig domestication over the last several decades has drawn attention to the roles of nonhuman drivers in the domestication process (9, 10)

High domestic pig contribution to the local gene pool of free-living European wild boar: a case study in Poland

“…Alternatively, hybrid origin could result from historic crosses between WB and DS in semi-wild condition, followed by genetic drift . Until the modern era, the seasonal practice of releasing DS in the forest provided plenty of opportunities of crossbreeding with WB (White 2011;Marshall et al 2014). Although, recessive or semi-dominant MC1R alleles may be masked by dominant genes, the coat color is a remarkable trait which is likely to undergo strong selective pressure in the wild.…”

Current perspectives and the future of domestication studies

“…Importantly, the wild progenitor species of domesticated taxa must have possessed the potential to live in the context of human ecologies, and to express traits that were favorable for human use, harvesting, and edibility. Finally, the presence of gene flow between populations of domestic and wild plants and animals [and members of the same or closely related but geographically and genetically differentiated domesticated species (12)] often results in modern populations that appear as if they arose outside the regions where the initial domestication process took place (13). As a result, it is crucial that researchers carefully evaluate whether multiple domestications of a single species occurred (13,14), making sure to reserve the term "domestication" solely for the initial independent process, and to avoid using the term to refer to subsequent admixture that often incorporated genetic and morphological characteristics of wild populations that were never independently domesticated (12,13).…”

“…Marshall et al (12) make a compelling case that intentional breeding of females was largely absent during the early stages of domestication for a wide range of species. This theory, along with what probably was considerable gene flow between wild and early managed animals (13), poses challenges to a number of commonly held assumptions about early domestication in some species relating to interpretations of genetic bottlenecks and molecular sequences more generally, the number of times a species was domesticated, and how various domestication traits emerged and were maintained in the long term.…”

“…In another vein, Blumler's analysis (103), suggesting that the Near East was unusually well endowed with large seeded grasses preadapted to domestication, might explain the early and diverse domestication of plants in that region. In addition, Marshall et al (12) make the point that epigenetic mechanisms should also be investigated in animal genetic responses during the domestication process.…”

The eco-evolutionary impacts of domestication and agricultural practices on wild species

“…To reduce the effectiveness of reproduction, domestic and wild species should be spatially or temporally separated during periods of reproduction. In reality, however, establishing reproductive barriers is difficult for both livestock and crops, unless they are physically separated before they mature [45]. Reducing genetic differences between domesticated and wild populations may also be possible to help conserve wild, threatened species.…”