Genomes of Modern Dogs and Wolves Paint Complicated Picture of Domestication

Dogs and wolves evolved from a common ancestor between 11,000 and 34,000 years ago, before humans transitioned to agricultural societies, according to high-quality analysis of individual genomes of modern dogs and gray wolves from areas of the world thought to be centers of dog domestication.

The study, published in PLoS Genetics on January 16, 2014, also shows that dogs are more closely related to each other than any of the wolves, regardless of geographic origin. This suggests that part of the genetic overlap observed between some modern dogs and wolves is the result of interbreeding after dog domestication, not a direct line of descent from one group of wolves.

"Dog domestication is more complex than we originally thought," said John Novembre, associate professor in the Department of Human Genetics at the University of Chicago. "In this analysis we didn't see clear evidence in favor of a multi-regional model, or a single origin from one of the living wolves that we sampled. It makes the field of dog domestication very intriguing going forward."

Novembre is one of the senior authors of the study, along with Robert Wayne, professor in the Department of Ecology and Evolutionary Biology at the University of California, Los Angeles (UCLA).The study was the result of a large, international collaboration, whose lead analyst was first author Adam Freedman, a postdoctoral fellow.

The team led by Freedman, Novembre and Wayne generated the highest quality genome sequences to date from three gray wolves: one each from China, Croatia and Israel, representing three regions where dogs are believed to have originated. They also produced genomes for two dog breeds: a basenji, a breed which originates in central Africa, and a dingo from Australia, both areas that have been historically isolated from modern wolf populations. In addition to the wolves and dogs, they sequenced the genome of a golden jackal to serve as an "outgroup" representing earlier divergence.

Their analysis of the basenji and dingo genomes, plus a previously published boxer genome from Europe, showed that the dog breeds were most closely related to each other. Likewise, the three wolves from each geographic area were more closely related to each other than any of the dogs.

Novembre said this tells a different story than he and his colleagues anticipated. Instead of all three dogs being closely related to one of the wolf lineages, or each dog being related to closest its geographic counterpart (i.e. the basenji and Israeli wolf, or the dingo and Chinese wolf), they seem to have descended from an older, common ancestor.

"One possibility is there may have been other wolf lineages that these dogs are diverged from that then went extinct," he said. "So now when you ask which wolves are dogs most closely related to, it's none of these three because these are wolves that diverged in the recent past. It's something more ancient that isn't well represented by today's wolves."

Domestication apparently occurred with significant bottlenecks in the historical population sizes of both early dogs and wolves.Freedman and his colleagues were able to infer historical sizes of dog and wolf populations by analyzing genome-wide patterns of variation, and show that dogs suffered a 16-fold reduction in population size as they diverged from wolves. Wolves also experienced a sharp drop in population size soon after their divergence from dogs, implying that diversity among both animals' common ancestors was larger than represented by modern wolves.

The researchers also found differences across dog breeds and wolves in the number of amylase (AMY2B) genes that help digest starch.Recent studies have suggested that this gene was critical to domestication, allowing early dogs living near humans to adapt to an agricultural diet. Freedman and his colleagues surveyed genetic data from 12 additional dog breeds and saw that the Siberian husky, for example, had a relatively low copy number of this gene, as did the dingo. They also saw evidence of the expansion of this gene family in wolves, meaning that it isn't exclusive to dogs and may not have been a primary resultof domestication.

Novembre said this data reflects a more complicated history than the popular story thatearly farmers adopted a few docile, friendly wolves that later became our beloved, modern-day companions. Instead, the earliest dogs may have first lived among hunter-gatherer societies and adapted to agricultural life later.

Accounting for gene flow after domestication was a crucial step in the analyses. According to Freedman, "If you don't explicitly consider such exchanges, these admixture events get confounded with shared ancestry."  And, gene flow across canid species appears more pervasive than previously thought. "We also found evidence for genetic exchange between between wolves and jackals... The picture emerging from our analyses, is that these types of exchanges may play an important role in shaping the diversification of canid species."

"We're trying to get every thread of evidence we can to reconstruct the past," said Novembre. "We use genetics to reconstruct the history of population sizes, relationships among populations and the gene flow that occurred. So now we have a much more detailed picture than existed before, and it's a somewhat surprising picture."

The National Science Foundation and Life Technologies provided funding and reagents for this study. Additional authors include Rena Schweizer, Diego Ortega-Del Vecchyo, Eunjung Han, FarhadHormozdiari, Kevin Squire and Stanley Nelson from UCLA; IlanGronau, Adam Boyko and Adam Siepel from Cornell Univesity; Pedro Silva from University of Porto, Portugal; Marco Galaverni from Ozzanodell'Emilia, Italy; Zhenxin Fan from Sichuan University, China; Peter Marx from Budapest University, Hungary; Belen Lorente-Galdos, Oscar Ramirez and Tomas Marques-Bonet from Institut de Biologia Evolutiva (CSIC - Universitat Pompeu Fabra), Spain; Holly Beale, Heidi Parker and Elaine Ostrander from the National Institutes of Health; Can Alkan from Bilkent University, Turkey; Carles Vila from EstacionBiologia de Doñana, Spain; Eli Geffen from Tel Aviv University, Israel; JosipKusak from the University of Zagreb, Croatia; Clarence Lee, VasishtTadigotla and Timothy Harkins from Life Technologies; and Carlos Bustamante from Stanford University.

###