Domesticated dogs, genomes, and malaria

Plasmodium falciparum is a unicelluar protozoan parasite of humans and the deadliest species of Plasmodium. It is transmitted through the bite of a female Anopheles mosquito and responsible for Therefore it is regarded as the deadliest parasite in humans, causing at least one million deaths every year. The species evolved about 10,000 years ago from the malarial parasite found in gorillas. A World Health Organization report in 2015, suggested there were 214 million cases of malaria worldwide.

Dogs spread across the globe with humans and have had to adapt to the same environmental conditions as humans. A Chinese research team led by Zhang has successfully identified genes selected in African dogs and functionally verified the action of one of these as the first evidence of dog adaptation to malaria.

“Recently, we have shown the first evidence that dogs can undergo similar adaptations as humans, using the same genes to live in the high altitudes of Tibet,” said professor Ya-Ping Zhang.

“Dogs have survived in tropical environments for thousands of years alongside humans,” said Zhang. “In this study, we have identified genes associated with insulin secretion and sensitivity, immunity, angiogenesis and ultraviolet protection showed adaptive selection.”

Yan-Hu Liu et al. (2017) sequenced the genomes of 19 dogs from Nigeria. For this new data set, they identified a set of candidate genes for natural selection in African village dogs and also carried out functional studies to confirm that one of these, ADGRE1, might be responsible for providing host immunity to Plasmodium infection—a target of selection associated with malaria.

“Our study suggests ADGRE1 also contributes to defense against Plasmodium infection in dogs, and thus, convergent evolution in this gene between humans and dogs,” said Guo-Dong Wang. “This is a novel finding since in earlier studies the most apparent cases of convergent evolution between humans and dogs were in genes for digestion and metabolism, neurological process, and cancer.”

The authors went on to show in cell culture experiments in the lab that the derived variant of ADGRE1 is linked to increased phagocytosis in cells infected with Plasmodium parasites, making it very likely that the ADGRE1 confers protection against Plasmodium infection by stimulating the immune response against the parasite.

In addition, they investigated the Nigerian dogs’ demographic history in relation to other dogs, including Eurasian gray wolves and African golden wolves. They found that the Nigerian dog population diverged from Eurasian dog populations around 14,000 years ago. After this divergence, the population fell on hard times, and experienced a severe bottleneck (leading to a reduced genetic diversity within the Nigerian dog population) and also gene flow from African golden wolves after the divergence.

Finally, they explored signals of selection in the Nigerian dog samples, and identified a number of candidate genes that are also linked to dietary and environmental factors.

As the authors note, since ADGRE1 has also been implicated in an adaptive response to Plasmodium in humans, it makes for a nice genetic tale of dogs utilizing similar tricks from living alongside their human companions to adapt to new environments.

References

Caspermeyer J. 2017. Scientists Find Evidence Our Best Friends, Dogs, Similarly Adapted to Malaria in Africa, Molecular Biology and Evolution,  msx289, https://doi.org/10.1093/molbev/msx289

Liu Y-H, Wang L, Xu T, Guo X, Li Y, Yin T-T, Yang H-C, Yang H, Adeola AC, Sanke OJ, et al. 2017. Whole-genome sequencing of African dogs provides insights into adaptations against tropical parasites. Molecular Biology and Evolution.

 Advance Access published October 10, 2017, doi: 10.1093/molbev/msx258

Wolf parasites in domestic dogs

Grey wolves, like all wild animals, are hosts to a variety of parasites. The presence of grey wolves in German forests has little influence on the parasite burden of hunting dogs. This reassuring conclusion is the result of a new study at the Berlin-based Leibniz Institute for Zoo and Wildlife Research (IZW). The study examined the feces of 78 hunting dogs over several months in an area without wolves and in one that had been recolonized. The results have been published in the open access scientific journal International Journal for Parasitology: Parasites and Wildlife.

Since the early 1990s grey wolves are expanding their range in central Europe. This recolonization gives rise to many questions about this apex predator and its influence on the environment and the life cycles of its parasites, prey, and potential competitors. Scientists at the Leibniz-IZW have now uncovered that the presence of wolves has little impact on the parasite burden of domestic dogs used for hunting prey of wolves. The scientists compared hunting dogs based in Eastern Germany, where wolves have re-established themselves since early 2000, with hunting dogs in North of Germany, where -- at the time of the study -- there were no resident wolf packs.

Grey wolves in the Bavarian forest.Photo Credit: © gallas / Fotolia

"Hunting dogs, unlike companion dogs, are especially well suited for this comparison as they, just like the wolf, rummage through forests and have access to game meat.," Ines Lesniak, a scientist at Leibniz-IZW, explains. "The study focused on the parasites of the internal organs, so-called endoparasites, which can be identified in the feces of the host." In a previous study, the spectrum of endoparasites present in German grey wolves was described. As previously, the researchers used genetic techniques to determine the presence of parasitic worms and protozoan intestinal parasites belonging to the Sarcocystis genus in hunting dogs. Both the rate of infection and the species richness of worms and Sarcocystis species found in the dogs did not differ between the study areas with and without wolves. The parasite spectrum of hunting dogs and wolves overlapped considerably, indicating that dogs might have replaced the wolf during its absence as an alternate and suitable definite host in the life cycles of some parasites. A single Sarcocystis species (Sarcocystis grueneri), previously identified as a "wolf specialist," was discovered more frequently in hunting dogs in wolf areas than in hunting dogs in areas without wolves. Like many tapeworms, these protozoans have a life cycle in which carnivores, like dogs or wolves, function as definite host and their prey, such as roe deer and red deer, act as intermediate hosts.

"Unlike wild animals, hunting dogs are regularly dewormed, including the individual hunting dogs which participated in our study," Lesniak emphasizes. "However, these medical treatments do not affect protozoan parasites such as Sarcocystis." The scientists suspect that the high infection probability of hunting dogs -- over 60 percent in both study areas -- is caused by the routine feeding of game meat or offal. "It's in the owner's hands," Lesniak says. "Many study participants already act very responsibly by deworming their dogs on a regular basis; in the best cases several times a year." The official recommendation of the European Scientific Council for Companion Animal Parasites (ESCCAP) is that there should be a monthly treatment of risk groups such as hunting dogs. Such a regular treatment prevents parasitic worms from reproduction in the host and subsequent egg development, which thereby improves the health and wellbeing of the hunting dog. "Dog owners can also reduce the parasite burden of their dogs by the careful feeding of meat leftovers. Cooking the meat is a simple precautionary measure that inactivates all parasites -- from protozoans to tapeworm cysts -- as well as other pathogens that might be present in the meat." The Leibniz-IZW considers wolves to play a minor role regarding the excretion and distribution of parasites. "The number of wolves in Germany is extremely low compared to other carnivores such as red foxes or raccoon dogs, which can also serve as hosts for these parasites, and it is also low in comparison to the number of hunting dogs," comments the senior author of the study, Dr. Oliver Krone.

German dog owners can rejoice: None of the parasite species found in hunting dogs are an unreasonable health risk to humans, irrespective of whether the dogs live in an area where wolves are present or not present. The regular treatment with anthelmintics and feeding of cooked leftovers are simple but effective measures to maintain the health of hunting dogs. The Leibniz-IZW study illustrates that concerns regarding pathogens related to the return of wolves are currently unjustified.


Citations
Ines Lesniak, Mathias Franz, Ilja Heckmann, Alex D. Greenwood, Heribert Hofer, Oliver Krone. Surrogate hosts: Hunting dogs and recolonizing grey wolves share their endoparasites. International Journal for Parasitology: Parasites and Wildlife, 2017; 6 (3): 278 DOI: 10.1016/j.ijppaw.2017.09.001

Ines Lesniak, Ilja Heckmann, Emanuel Heitlinger, Claudia A. Szentiks, Carsten Nowak, Verena Harms, Anne Jarausch, Ilka Reinhardt, Gesa Kluth, Heribert Hofer, Oliver Krone. Population expansion and individual age affect endoparasite richness and diversity in a recolonising large carnivore population. Scientific Reports, 2017; 7: 41730 DOI: 10.1038/srep41730

The Origin of Dingoes

Pure dingoes come in a variety of colors including ginger, black and tan,
white and sable. Credit: Lyn Watson/Australian Dingo Foundation

A major study of dingo DNA has revealed dingoes most likely migrated to Australia in two separate waves via a former land bridge with Papua New Guinea.

The find has significant implications for conservation, with researchers recommending the two genetically distinct populations of dingoes -- in the south-east and north-west of the country -- be treated as different groups for management and conservation purposes.

"Care should be taken not to move dingoes between the different wild populations," says study first author and UNSW Sydney scientist Dr. Kylie Cairns.

"And captive breeding programs should ensure the two dingo populations are maintained separately, with genetic testing used to identify ancestry."

Further, inter-breeding also needs to be urgently prevented between domestic dogs and the south-eastern population of dingoes, which is threatened by genetic dilution, habitat loss and lethal control measures such as baiting and the recently reintroduced wild dog bounty in Victoria.

"Effective containment or neutering of male dogs in rural areas may help achieve this reduction in inter-breeding," says Dr. Cairns, of the School of Biological, Earth and Environmental Sciences.

"Additionally, baiting and culling practices break apart dingo packs, leading to increased incidence of hybridization. Alternative livestock protection measures need to be explored, such as livestock guardians, predator deterrents, and improved dingo-proof fencing," she says.

The study, by scientists from UNSW and the University of California, is published in the journal Ecology and Evolution.

The study is the first broad study of the evolutionary history of dingoes around Australia using both mitochondrial and Y-chromosome genetic markers.

The researchers sampled 127 dingoes across Australia as well as five New Guinea Singing Dogs from a North American captive population. A dataset of Y chromosome and mitochondrial control region data from 173 male dogs, including 94 dingoes, was also used.

Only genetically pure dingoes were included in the study.

The north-western population is found in Western Australia, the Northern Territory, northern parts of South Australia, and central and northern Queensland.

The south-eastern population is found in New South Wales, the Australian Capital Territory, Victoria and southern parts of Queensland (including Fraser Island).

The researchers believe the two groups may have migrated separately from Papua New Guinea over the now-flooded land bridge as long as 8000 to 10,000 years ago.

Particularly in south-eastern states, they recommend a broad survey of dingoes in national parks and state forests be carried out to focus conservation efforts in key areas, and also that state and federal legislation allowing fatal control measures be reviewed.



Citation
Kylie M. Cairns, Sarah K. Brown, Benjamin N. Sacks, J. William O. Ballard. Conservation implications for dingoes from the maternal and paternal genome: Multiple populations, dog introgression, and demography. Ecology and Evolution, 2017; DOI: 10.1002/ece3.3487

Making a New Dog

On landscapes around the world, environmental change is bringing people and large carnivores together -- but the union is not without its problems. Human-wildlife conflict is on the rise as development continues unabated and apex predators begin to reoccupy their former ranges. Further complicating matters, many of these species are now reliant on anthropogenic, or human, foods, including livestock, livestock and other ungulate carcasses, and garbage.

Writing in BioScience, Thomas Newsome, of Deakin University and the University of Sydney, and his colleagues use gray wolves and other large predators as case studies to explore the effects of anthropogenic foods. They find numerous instances of species' changing their social structures, movements, and behavior to acquire human-provisioned resources. For instance, in central Iran, gray wolves' diets consist almost entirely of farmed chickens, domestic goats, and trash.

Other instances of these phenomena abound. In a similar case in Australia, dingoes gained access to anthropogenic foods from a waste facility. The result, according to the authors, was "decreased home-range areas and movements, larger group sizes, and altered dietary preferences to the extent that they filled a similar dietary niche to domestic dogs." Moreover, wrote the authors, "the population of subsidized dingoes was a genetically distinct cluster," which may portend future speciation events. Hybridization among similar predator species may also contribute to evolutionary divergence: "Anthropogenic resources in human-modified environments could increase the probability of non-aggressive contact" between species. According to the authors, "If extant wolves continue to increase their reliance on anthropogenic foods, we should expect to observe evidence of dietary niche differentiation and, over time, the development of genetic structure that could signal incipient speciation."

Wolves' use of anthropogenic food could have serious implications for wider conservation efforts, as well. In particular, Newsome and his colleagues raise concerns about whether wolf reintroduction and recolonisation programs will meet ecosystem-restoration goals in human-modified systems. Managers will need to consider "how broadly insights into the role played by wolves gleaned from protected areas such as Yellowstone can be applied in areas that have been greatly modified by humans," say the authors.

Newsome and his colleagues call for further research -- in particular, "studies showing the niche characteristics and population structure of wolves in areas where human influence is pervasive and heavy reliance on human foods has been documented." Through such studies, they argue that "we might be able to ask whether heavy reliance of anthropogenic subsidies can act as a driver of evolutionary divergence and, potentially, provide the makings of a new dog."

Citation
Thomas M. Newsome, Peter J. S. Fleming, Christopher R. Dickman, Tim S. Doherty, William J. Ripple, Euan G. Ritchie, Aaron J. Wirsing. Making a New Dog? BioScience, 2017; 67 (4): 374 DOI: 10.1093/biosci/bix022

Dogs demonstrate perspective

Humans are able to interpret the behavior of others by attributing mental states to them (and to themselves). By adopting the perspectives of other persons, they can assume their emotions, needs, and intentions and react accordingly. In the animal kingdom, the ability to attribute mental states (Theory of Mind) is a highly contentious issue. Cognitive biologists from the Messerli Research Institute of the University of Veterinary Medicine Vienna could prove with a new test procedure that dogs are not only able to identify whether a human has an eye for a food source and, therefore, knows where the food has been hidden. They can also apply this knowledge in order to correctly interpret cues by humans and find food they cannot see themselves. This perspective-taking ability is an important component of social intelligence. It helps dogs to cope with the human environment. The results have been published in the journal Animal Cognition.

The so-called Theory of Mind describes the ability in humans to understand mental states in conspecifics such as emotions, intentions, knowledge, beliefs and desires. This ability develops in humans within the first four or five years of life while it is usually denied in animals. Indications that animals can understand mental states or even states of knowledge of others have only been found in apes and corvids so far. Dogs have been tested several times, but the results were poor and contradictory.

With a new experimental approach, cognitive biologists from the Messerli Research Institute could now provide solid evidence for dogs being able to adopt our perspective. By adopting the position of a human and following their gaze, dogs understand what the human could see and, consequently, know. This ability to ascribe knowledge is only a component of a full-blown Theory of Mind, but an important one.

Identifying the right informant

The so-called Guesser-Knower paradigm is a standard test in research into the attribution of knowledge to others. This experiment involves two persons: a "Knower" who hides food, invisibly for the dog, in one of several food containers or knows where somebody else has hidden it, and a "Guesser." The Guesser has either not been in the room or covered her eyes during the hiding of the food. A non-transparent wall blocks the animals' view of the food being hidden. After that, the two humans become informants by pointing to different food containers.

The Knower always points to the baited container and the Guesser to another one. All containers smell of food. "To get the food, the dogs have to understand who knows the hiding place (Knower) and who does not and can, therefore, only guess (Guesser). They must identify the informant they can rely on if they have to decide for one food container," said principal investigator Ludwig Huber. In approximately 70 percent of the cases, the dogs chose the container indicated by the Knower - and thus were able to successfully accomplish the test. This result was independent of the position of the food container, the person acting as the Knower and where the Guesser was looking.

Dogs can adopt human perspectives

The only aim of this test series, however, was to independently confirm a study carried out in New Zealand. Clear evidence of dogs being able to adopt our perspective and take advantage of it was provided in a new test developed by the team, the so-called "Guesser looking away" test.

In this new experiment, a third person in the middle hides the food. This person does not give cues later on. The potential informants were kneeing left and right of this hider and looked to the same side and slightly down. Thus, one of the two persons looked towards the baiter, the other person looked away. "This means that the tested dogs, in order to get the food, had to judge who is the Knower by adopting the informants' perspectives and following their gazes," explained Huber. Even in this test, which is very difficult for the animals, approximately 70 percent of the trials had been mastered.

Adopting the human perspective leads to invisible food

Being able to adopt the perspective of a human does, however, not require the ability to understand intentions or wishes. "But the study showed that dogs can find out what humans or conspecifics can or cannot see," explained Huber. "By adopting the positions of humans and following their gazes geometrically, they find out what humans see and, therefore, know - and consequently whom they can trust or not."

In similar experiments, chimpanzees and few bird species such as scrub jays and ravens were able to understand the state of knowledge and also the intentions of conspecifics and modify their own behavior accordingly. For dogs, there have only been speculations and vague indications so far. But dogs understand our behavior very well, for example, our degree of attention. They can learn from directly visible cues such as gestures or gazes. Thus, they are able to find food even if their view of it has been blocked. "The ability to interpret our behavior and anticipate our intentions, which has obviously developed through a combination of domestication and individual experience, seems to have supported the ability to adopt our perspective," said Huber. "It still remains unclear which cognitive mechanisms contribute to this ability. But it helps dogs to find their way in our world very well."


Citation
Amélie Catala, Britta Mang, Lisa Wallis, Ludwig Huber. Dogs demonstrate perspective taking based on geometrical gaze following in a Guesser–Knower task. Animal Cognition, 2017; DOI: 10.1007/s10071-017-1082-x

Dogs and wolves MRCA 33,000 YBP

Dogs may be older than previously thought.

The origin of dogs has inspired a lingering controversy in academia. Where and when did dogs first split off from wolves? One of the top dogs in this dispute, population genetics expert Peter Savolainen of Sweden's KTH Royal Institute of Technology, isn't about to roll over. He hopes his latest research will finally settle the matter.

Some researchers say canines first split off from wolves in the Middle East; others say it happened in Europe. But Savolainen has long held that dogs originated in South East Asia alone, and he says his team has compiled new evidence that confirms his earlier findings.

The study concludes that the split with wolves occurred about 33,000 years ago.

Savolainen's earlier studies were based on analysis of mitochondrial DNA. But recently other researchers have used data from nuclear DNA to refute those findings, arguing that dogs originated in the Middle East, Central Asia or Europe.

But apparently, those researchers were thrown off the scent, according to Savolainen. The data they relied on did not include samples from South East Asia, he says. So if, as Savolainen says, dogs did indeed come from South East Asia, these studies would not have been able to detect it.

"Which is why we analysed the entire nuclear genome of a global sample collection from 46 dogs, which includes samples from southern China and South East Asia," he says. "We then found out that dogs from South East Asia stand out from all other dog populations, because they have the highest genetic diversity and are genetically closest to the wolf."

Savolainen says this provides strong evidence that the dog originated in South East Asia, which confirms his earlier studies of Mitochondrial DNA.

"We also found that the global dog population is based on two important events: the dog and wolf populations first began to split off about 33,000 years ago in South East Asia. The global spread of dogs followed about 18,000 years later.

He says one explanation for the split between dogs and wolves 33,000 years ago could be that the wolf population became divided and the south Chinese wolf developed into dogs. In that case, it is possible the global spread of dogs out of South East Asia is associated with domestication.

"The dog's story thus appears to have begun 33,000 years ago, but the exact path to the fully-domesticated dogs that spread throughout the world 15,000 years ago is not yet clear."


Citation

Guo-Dong Wang, Weiwei Zhai, He-Chuan Yang, Lu Wang, Li Zhong, Yan-Hu Liu, Ruo-Xi Fan, Ting-Ting Yin, Chun-Ling Zhu, Andrei D Poyarkov, David M Irwin, Marjo K Hytönen, Hannes Lohi, Chung-I Wu, Peter Savolainen, Ya-Ping Zhang. 2015. Out of southern East Asia: the natural history of domestic dogs across the world. Cell Research, DOI: 10.1038/cr.2015.147

Dogs can recognise emotions

For the first time, researchers have shown that dogs must 

form abstract mental representations of positive and 

negative emotional states, and are not simply displaying 

learned behaviours when responding to the expressions

of people and other dogs. Photo credit: University of

Lincoln.

Dogs can recognise emotions in humans by combining information from different senses – an ability that has never previously been observed outside of humans, a new study published today reveals.

For the first time, researchers have shown that dogs must form abstract mental representations of positive and negative emotional states, and are not simply displaying learned behaviours when responding to the expressions of people and other dogs.

The findings from a team of animal behaviour experts and psychologists the University of Lincoln, UK, and University of Sao Paulo, Brazil, are published in the Royal Society journal Biology Letters.

The researchers presented 17 domestic dogs with pairings of images and sounds conveying different combinations of positive (happy or playful) and negative (angry or aggressive) emotional expressions in humans and dogs. These distinct sources of sensory input – photos of facial expressions and audio clips of vocalisations (voices or barks) from unfamiliar subjects – were played simultaneously to the animals, without any prior training.

The team found the dogs spent significantly longer looking at the facial expressions which matched the emotional state (or valence) of the vocalisation, for both human and canine subjects.

The integration of different types of sensory information in this way indicates that dogs have mental representations of positive and negative emotional states of others.

Researcher Dr Kun Guo, from the University of Lincoln’s School of Psychology, said: “Previous studies have indicated that dogs can differentiate between human emotions from cues such as facial expressions, but this is not the same as emotional recognition.

“Our study shows that dogs have the ability to integrate two different sources of sensory information into a coherent perception of emotion in both humans and dogs. To do so requires a system of internal categorisation of emotional states. This cognitive ability has until now only been evidenced in primates and the capacity to do this across species only seen in humans.”

Co-author Professor Daniel Mills, from the School of Life Sciences at the University of Lincoln, said: “It has been a long-standing debate whether dogs can recognise human emotions. Many dog owners report anecdotally that their pets seem highly sensitive to the moods of human family members.

“However, there is an important difference between associative behaviour, such as learning to respond appropriately to an angry voice, and recognising a range of very different cues that go together to indicate emotional arousal in another. Our findings are the first to show that dogs truly recognise emotions in humans and other dogs.

“Importantly, the dogs in our trials received no prior training or period of familiarisation with the subjects in the images or audio. This suggests that dogs' ability to combine emotional cues may be intrinsic. As a highly social species, such a tool would have been advantageous and the detection of emotion in humans may even have been selected for over generations of domestication by us.”

Citation

Albuquerque N, Guo K, Wilkinson A, Savalli C, Otta E, Mills D. Dogs recognize dog and human emotions. Biol. Lett., 2016 DOI: 10.1098/rsbl.2015.0883

Bandicoots Are Naïve to Dogs

Historical coexistence with dingoes may explain bandicoot avoidance 

of domestic dogs.Photo credit: Narawan Williams; CCAL.

Domestic dogs and cats were introduced to Tasmania two centuries ago, but bandicoots still fail to recognize these introduced predators as threats, according a study published September 7, 2016 in the open-access journal PLOS ONE by Anke Frank from University of Tasmania, Australia, and colleagues.

Worldwide, introduced predators have caused declines and extinctions of native wildlife, presumably in part because native species do not see novel predators as threats and thus fail to flee or defend themselves. But this naiveté is not necessarily forever: bandicoots in Sydney avoid backyards with domestic dogs. Interestingly, however, Sydney bandicoots do not avoid domestic cats even though they, like domestic dogs, were introduced about 200 years ago. This varying behavior to introduced predators has been attributed to the fact that dingoes arrived in mainland Australia 4000 years ago, predisposing Sydney bandicoots to avoid domestic dogs.

To test this hypothesis, Frank and colleagues assessed bandicoot behavior in Tasmania, where domestic dogs have been present for 200 years but where dingoes have never been present. The researchers surveyed 548 people in Hobart, Tasmania -- 37% of whom owned at least one dog and 20% of whom owned at least one cat -- about bandicoot sightings and scats in their backyards.

More than a quarter of participants reported that their pets had killed bandicoots, showing that predation from these introduced predators was a real threat. Even so, the survey showed that Tasmanian bandicoot sightings and scats were equally likely in backyards with or without domestic dogs or cats. These findings support the hypothesis that bandicoots on mainland Australia may recognize dogs as predators due to thousands of years of exposure to dingoes, and suggests that naiveté to introduced predators can ultimately be overcome.

"By using a citizen science approach, my collaborators and I found that -- unlike Australian mainland bandicoots -- bandicoots from the island state of Tasmania are naïve to domestic dogs," said Anke Frank. "This study supports our hypothesis that naiveté towards unfamiliar predators may eventually be overcome, but that in Tasmania 200 years of exposure have been an insufficient time for bandicoots to recognize cats as well as dogs as a threat."

Anke S. K. Frank, Alexandra J. R. Carthey, Peter B. Banks. 2016. Does Historical Coexistence with Dingoes Explain Current Avoidance of Domestic Dogs? Island Bandicoots Are Naïve to Dogs, unlike Their Mainland Counterparts. PLOS ONE, 2016; 11 (9): e0161447 DOI: 10.1371/journal.pone.0161447

The Sardinian Fonni's Dog and human migration

The Fonni’s Dog (Cane Fonnese or Sardinian Sheepdog) is

endemic to Sardinia and is known for its fiercely protective

guarding behaviors. Photo Credit: Stefano Marell

A genomic analysis of 28 dog breeds has traced the genetic history of the remarkable Fonni's Dog, a herd guardian endemic to the Mediterranean island of Sardinia. The results, published in the journal GENETICS, reveal that the regional variety has developed into a true breed through unregulated selection for its distinctive behavior, and that its ancestors came from the very same geographic areas as Sardinia's human migrants. Just as Sardinian people have long provided a wealth of genetic insights to scientists, the canine natives are an example of an isolated population that could prove a powerful resource for finding genes that influence health and behavior.

Fonni's Dogs (Cane Fonnese in Italian) are large, rugged dogs known for their wariness towards strangers and their intense facial expression. Although there are descriptions of these shephard's companions dating to at least the mid-nineteenth century, it is not officially recognized as a breed by most international registries, including the largest federation of kennel clubs, the Federation Cynologique Internationale.

"If you were to look at ten Fonni's Dogs, you would see there's a lot of variation in coat color and fur length. But they are all good protectors of their flocks. That's because nobody cares what they look like; they've been bred to do a job and to do it right," says study leader Elaine Ostrander of the National Human Genome Research Institute (NHGRI).

That job is guarding the possessions of their owner, to whom they are fiercely loyal. "Fonni's are also outstanding thieves," says Ostrander. "They can be trained to sneak over to the neighbors' and bring items home." While this particular duty isn't required by today's Fonni Dogs, written records from the mid-1800's indicate that thievery was part of their historical repertoire.

The island home of the Fonni's Dog has long held the interest of geneticists. Because Sardinia is geographically isolated, its human inhabitants share a unique ancestry and relatively low genetic diversity. Those characteristics make it easier to study genetic influences on disease and aging in Sardinians than in other human groups. Ostrander and other canine geneticists argue that each of the hundreds of different dog breeds also represents an isolated population that could be harnessed for genetic studies.

"Dogs get all the same diseases as humans, and there are lots of dog breeds with genetic predispositions, for example to particular types of cancer," Ostrander says. "Once we understand the genetic history of a breed we can search for disease genes in a much more powerful way than is possible in humans, enabling us to hone in on medically-relevant genes."

To better understand how the Fonni's Dog developed, scientists from the NHGRI, the University of Milan, and G. d'Annunzio University analyzed blood samples from Fonni's Dogs living in different parts of Sardinia and sequenced the whole genome of one of these dogs. To trace the Fonni's relationship to dogs from around the Mediterranean, the team compared the data to DNA from 27 other European, Middle Eastern, and North African breeds.

The data revealed that the Fonni's dog shows all the genetic hallmarks of being a breed, even though it developed in the absence of a regulated pedigree program and only arose through the tendency of Sardinian shepherds to choose their best guard dogs for breeding. The researchers compared individual dogs from within the same breed and across different breeds, quantifying many aspects of genome variation and genetic distinctiveness. All these measures confirmed that the Fonni's Dog, in genetic terms, is a breed.

The study also revealed the ancestors of the Fonni's Dog were related to the Saluki, a swift and graceful "sight" hound from the Near and Middle East, and a large mastiff like the Komondor, a powerfully-built sheep guardian from Hungary that looks a bit like a mop.

Strikingly, the origins of the Fonni's Dog mirror human migration to Sardinia. Studies of the island's human inhabitants have shown they share greatest genetic similarity with people from Hungary, Egypt, Israel, and Jordan. "The map we can draw of the dog's origins is the same as the map of human migration to Sardinia," says Ostrander. "Clearly ancient people traveled with their dogs, just as they do now."

The close parallels between the history of the dog and human inhabitants of the island has a practical implication, says Ostrander. "Our study shows how closely dog migration parallels human migration. It could be that if you have missing pieces in a study of a human population's history, samples collected from dogs in the right place could fill in those gaps."

The team plans next to study in greater detail eleven regions of the genome that likely make the Fonni's Dog distinct -- these may be responsible for their characteristically loyal and protective behavior.

Ostrander points out the study was a collaborative effort with scientists from Italy, including Sardinia, and says she is gratified to find so many researchers across the world interested in similar questions. Her group is hoping to work with colleagues in a range of countries to explore other so-called "niche" dog populations, regional varieties that often have a history of being bred for a particular job. Their goals are to better understand how dogs have evolved and to demonstrate yet another important job for these faithful human companions: tracking down disease genes.

Citation
D. L. Dreger, B. W. Davis, R. Cocco, S. Sechi, A. Di Cerbo, H. G. Parker, M. Polli, S. P. Marelli, P. Crepaldi, E. A. Ostrander. 2016. Commonalities in Development of Pure Breeds and Population Isolates Revealed in the Genome of the Sardinian Fonni's Dog. Genetics, 204 (2): 737 DOI: 10.1534/genetics.116.192427

A dual origin of domestic dogs

Man's best friend. Dogs were domesticated not once, but

twice in  different parts of the world. Photo Credit:

© lenaivanova2311 / Fotolia

The question, 'Where do domestic dogs come from?', has vexed scholars for a very long time. Some argue that humans first domesticated wolves in Europe, while others claim this happened in Central Asia or China. A new paper, published in Science, suggests that all these claims may be right. Supported by funding from the European Research Council and the Natural Environment Research Council, a large international team of scientists compared genetic data with existing archaeological evidence and show that man's best friend may have emerged independently from two separate (possibly now extinct) wolf populations that lived on opposite sides of the Eurasian continent. This means that dogs may have been domesticated not once, as widely believed, but twice.
A major international research project on dog domestication, led by the University of Oxford, has reconstructed the evolutionary history of dogs by first sequencing the genome (at Trinity College Dublin) of a 4,800-year old medium-sized dog from bone excavated at the Neolithic Passage Tomb of Newgrange, Ireland. The team (including French researchers based in Lyon and at the National Museum of Natural History in Paris) also obtained mitochondrial DNA from 59 ancient dogs living between 14,000 to 3,000 years ago and then compared them with the genetic signatures of more than 2,500 previously studied modern dogs.
The results of their analyses demonstrate a genetic separation between modern dog populations currently living in East Asia and Europe. Curiously, this population split seems to have taken place after the earliest archaeological evidence for dogs in Europe. The new genetic evidence also shows a population turnover in Europe that appears to have mostly replaced the earliest domestic dog population there, which supports the evidence that there was a later arrival of dogs from elsewhere. Lastly, a review of the archaeological record shows that early dogs appear in both the East and West more than 12,000 years ago, but in Central Asia no earlier than 8,000 years ago.
Combined, these new findings suggest that dogs were first domesticated from geographically separated wolf populations on opposite sides of the Eurasian continent. At some point after their domestication, the eastern dogs dispersed with migrating humans into Europe where they mixed with and mostly replaced the earliest European dogs. Most dogs today are a mixture of both Eastern and Western dogs -- one reason why previous genetic studies have been difficult to interpret.
The international project (which is combining ancient and modern genetic data with detailed morphological and archaeological research) is currently analysing thousands of ancient dogs and wolves to test this new perspective, and to establish the timing and location of the origins of our oldest pet.
Senior author and Director of Palaeo-BARN (the Wellcome Trust Palaeogenomics & Bio-Archaeology Research Network) at Oxford University, Professor Greger Larson, said: 'Animal domestication is a rare thing and a lot of evidence is required to overturn the assumption that it happened just once in any species. Our ancient DNA evidence, combined with the archaeological record of early dogs, suggests that we need to reconsider the number of times dogs were domesticated independently. Maybe the reason there hasn't yet been a consensus about where dogs were domesticated is because everyone has been a little bit right.'
Lead author Dr Laurent Frantz, from the Palaeo-BARN, commented: 'Reconstructing the past from modern DNA is a bit like looking into the history books: you never know whether crucial parts have been erased. Ancient DNA, on the other hand, is like a time machine, and allows us to observe the past directly.'
Senior author Professor Dan Bradley, from Trinity College Dublin, commented: 'The Newgrange dog bone had the best preserved ancient DNA we have ever encountered, giving us prehistoric genome of rare high quality. It is not just a postcard from the past, rather a full package special delivery.'
Professor Keith Dobney, co-author and co-director of the dog domestication project from Liverpool University's Department of Archaeology, Classics and Egyptology, is heartened by these first significant results. 'With the generous collaboration of many colleagues from across the world-sharing ideas, key specimens and their own data -- the genetic and archaeological evidence are now beginning to tell a new coherent story. With so much new and exciting data to come, we will finally be able to uncover the true history of man's best friend.'

Citation
L. A. F. Frantz, V. E. Mullin, M. Pionnier-Capitan, O. Lebrasseur, M. Ollivier, A. Perri, A. Linderholm, V. Mattiangeli, M. D. Teasdale, E. A. Dimopoulos, A. Tresset, M. Duffraisse, F. McCormick, L. Bartosiewicz, E. Gal, E. A. Nyerges, M. V. Sablin, S. Brehard, M. Mashkour, A. B l  escu, B. Gillet, S. Hughes, O. Chassaing, C. Hitte, J.-D. Vigne, K. Dobney, C. Hanni, D. G. Bradley, G. Larson. 2016. Genomic and archaeological evidence suggests a dual origin of domestic dogs. Science, 2016; 352 (6290): 1228 DOI: 10.1126/science.aaf3161

Praise or food preference in dogs

Chowhound: Ozzie, a shorthaired terrier mix, was the only dog in the
experiments that chose food over his owner's praise 100 percent
of the time. "Ozzie was a bit of an outlier," Berns says,"but Ozzie's
owner understands him and still loves him." Credit: Gregory Berns

Given the choice, many dogs prefer praise from their owners over food, suggests a new study published in the journal Social, Cognitive and Affective Neuroscience. The study is one of the first to combine brain-imaging data with behavioral experiments to explore canine reward preferences.

"We are trying to understand the basis of the dog-human bond and whether it's mainly about food, or about the relationship itself," says Gregory Berns, a neuroscientist at Emory University and lead author of the research. "Out of the 13 dogs that completed the study, we found that most of them either preferred praise from their owners over food, or they appeared to like both equally. Only two of the dogs were real chow-hounds, showing a strong preference for the food."

Dogs were at the center of the most famous experiments of classical conditioning, conducted by Ivan Pavlov in the early 1900s. Pavlov showed that if dogs are trained to associate a particular stimulus with food, the animals salivate in the mere presence of the stimulus, in anticipation of the food.

"One theory about dogs is that they are primarily Pavlovian machines: They just want food and their owners are simply the means to get it," Berns says. "Another, more current, view of their behavior is that dogs value human contact in and of itself."

Berns heads up the Dog Project in Emory's Department of Psychology, which is researching evolutionary questions surrounding man's best, and oldest friend. The project was the first to train dogs to voluntarily enter a functional magnetic resonance imaging (fMRI) scanner and remain motionless during scanning, without restraint or sedation. In previous research, the Dog Project identified the ventral caudate region of the canine brain as a reward center. It also showed how that region of a dog's brain responds more strongly to the scents of familiar humans than to the scents of other humans, or even to those of familiar dogs.

For the current experiment, the researchers began by training the dogs to associate three different objects with different outcomes. A pink toy truck signaled a food reward; a blue toy knight signaled verbal praise from the owner; and a hairbrush signaled no reward, to serve as a control.

The dogs then were tested on the three objects while in an fMRI machine. Each dog underwent 32 trials for each of the three objects as their neural activity was recorded.

All of the dogs showed a stronger neural activation for the reward stimuli compared to the stimulus that signaled no reward, and their responses covered a broad range. Four of the dogs showed a particularly strong activation for the stimulus that signaled praise from their owners. Nine of the dogs showed similar neural activation for both the praise stimulus and the food stimulus. And two of the dogs consistently showed more activation when shown the stimulus for food.

The dogs then underwent a behavioral experiment. Each dog was familiarized with a room that contained a simple Y-shaped maze constructed from baby gates: One path of the maze led to a bowl of food and the other path to the dog's owner. The owners sat with their backs toward their dogs. The dog was then repeatedly released into the room and allowed to choose one of the paths. If they came to the owner, the owner praised them.

"We found that the caudate response of each dog in the first experiment correlated with their choices in the second experiment," Berns says. "Dogs are individuals and their neurological profiles fit the behavioral choices they make. Most of the dogs alternated between food and owner, but the dogs with the strongest neural response to praise chose to go to their owners 80 to 90 percent of the time. It shows the importance of social reward and praise to dogs. It may be analogous to how we humans feel when someone praises us."

The experiments lay the groundwork for asking more complicated questions about the canine experience of the world. The Berns' lab is currently exploring the ability of dogs to process and understand human language.

"Dogs are hypersocial with humans," Berns says, "and their integration into human ecology makes dogs a unique model for studying cross-species social bonding."

Citation

Peter F. Cook, Ashley Prichard, Mark Spivak, Gregory S. Berns. Awake canine fMRI predicts dogs’ preference for praisevsfood. 2016. Social Cognitive and Affective Neuroscience, 2016; nsw102 DOI: 10.1093/scan/nsw102

Ancient wolf genome reveals an early divergence of domestic dog ancestors

Dogs' special relationship to humans may go back 27,000 to 40,000 years, according to genomic analysis of an ancient Taimyr wolf bone. Earlier genome-based estimates have suggested that the ancestors of modern-day dogs diverged from wolves no more than 16,000 years ago, after the last Ice Age. Dogs' special relationship to humans may go back 27,000 to 40,000 years, according to genomic analysis of an ancient Taimyr wolf bone reported in the Cell Press journal Current Biology on May 21. Earlier genome-based estimates have suggested that the ancestors of modern-day dogs diverged from wolves no more than 16,000 years ago, after the last Ice Age.

The genome from this ancient specimen, which has been radiocarbon dated to 35,000 years ago, reveals that the Taimyr wolf represents the most recent common ancestor of modern wolves and dogs.

"Dogs may have been domesticated much earlier than is generally believed," says Love Dalén of the Swedish Museum of Natural History. "The only other explanation is that there was a major divergence between two wolf populations at that time, and one of these populations subsequently gave rise to all modern wolves." Dalén considers this second explanation less likely, since it would require that the second wolf population subsequently became extinct in the wild.

"It is [still] possible that a population of wolves remained relatively untamed but tracked human groups to a large degree, for a long time," adds first author of the study Pontus Skoglund of Harvard Medical School and the Broad Institute.

The researchers made these discoveries based on a small piece of bone picked up during an expedition to the Taimyr Peninsula in Siberia. Initially, they didn't realize the bone fragment came from a wolf at all; this was only determined using a genetic test back in the laboratory. But wolves are common on the Taimyr Peninsula, and the bone could have easily belonged to a modern-day wolf. On a hunch, the researchers decided to radiocarbon date the bone anyway. It was only then that they realized what they had: a 35,000-year-old bone from an ancient Taimyr wolf.

The DNA evidence also shows that modern-day Siberian Huskies and Greenland sled dogs share an unusually large number of genes with the ancient Taimyr wolf.

"The power of DNA can provide direct evidence that a Siberian Husky you see walking down the street shares ancestry with a wolf that roamed Northern Siberia 35,000 years ago," Skoglund says. To put that in perspective, "this wolf lived just a few thousand years after Neandertals disappeared from Europe and modern humans started populating Europe and Asia."

Citation

Skoglund et al. 2015. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Current Biology, 2015 DOI: 10.1016/j.cub.2015.04.019

The Goyet and Eliseevichi skulls were wolves not dogs, and a thought on the wolf-dog transition

The dates for dog domestication have been controversial. Some evidence (the Goyet cave fossils) pointed to the Pleistocene with the skulls suggesting dogs were transitioning from wolves to dogs, while other evidence suggested wolves transitioned to dogs when humans were hunter-gatherers, or during the Neolithic, when humans began living in more permanent settlements and engage in agriculture. Recently discovered Paleolithic fossil skulls, Goyet dated 31,680 +/− 250 YBP in the Czech Republic and Eliseevich 1 MAE (13,905 +/− 55 YBP) from the Bryansk Region in the central Russian Plain, were identified as dogs, establishing the date of dog domestication in the Paleolithic contemporaneous with human hunter-gatherers.

In a new paper Drake et al. (2015) use 3D geometric morphometric analyses to compare the cranial morphology of Goyet and Eliseevichi MAE to that of ancient and modern dogs and wolves. They find the Paleolithic canids are definitively wolves and not dogs. When compared to wolf-like breeds the skulls from Goyet and Eliseevichi MAE lack a cranial flexion and the dorsal surface of their muzzles do not have a concavity near the orbits. Morphologically, the fossils resemble wolves and no longer support the establishment of dog domestication in the Paleolithic.

The analysis in Drake et al. suggest previous measurement methodologies do not provide the resolution needed for distinguishing dogs from wolves and that 3D landmark-based geometric morphometric methods are better suited for the job. Geometric morphometric methods preserve size and shape information and allow for the inclusion of shape variation that cannot be gathered via calipers measurements.

Mitochondrial genomes revealed that Goyet, and other Paleolithic wolves, form the sister to all ancient and modern dogs. The Eliseevichi MAE, was not recovered in a clade with modern dogs but was genetically affiliated with modern wolves from Finland and Russia. The data from Drake et al is in accordance with the genetic evidence and they conclude that the Goyet and Eliseevichi MAE skulls lie within the wolf morphospace, together with the Paleolithic Alaskan wolves and Trou Balleux from Belgium. Drake et al. suggest a reassessment of the classification of the other fossil canids such as the Altai specimen (dated about 33,000 YBP) using 3D landmark-based geometric morphometric methods combined with genetic data, is needed to address the origin of domestication.

The Drake paper’s new classification of Goyet and Eliseevichi MAE as wolves, also suggests a reestablishment of the timing of dog domestication in the Neolithic. If shown to be correct it supports the Coppinger and Coppinger hypothesis that dog domestication occurred in the Neolithic when wolves began to scavenge near human settlements. Their hypothesis suggested human settlements provided a new niche because of the permanent supply of waste food and when combined with the Belyaev's experiment suggested wolf domestication could occur quickly. The establishment of permanent settlements in the Neolithic would have created an environment where sustained selection for tameness could exist for many generations thus setting the stage for dog domestication.

It seems unlikely this is the final word on the date of dog domestication and it simply shows that these skulls were wolves. But, they were wolves associated with archeological sites, not randomly found fossils. Thus the possibility that they were in some way associated with humans suggests there is more to the story. Pre-adaptive behaviors in wolves likely preceded domestication events. Yes, human settlements would have provided a continuous supply of garbage that could be scavenged. But prior to human settlements there was also a likely supply of wasted food that could have been exploited by wolves, paleo-dogs, and other scavengers – leftovers from megafauna kills. Large mammals killed during a hunt were unlikely to be completely consumed by the human hunters. 

Scavenging these large patches of waste nutrients would have brought humans and wolves into close contact – long before humans were living in Neolithic settlements. This scenario is more in line with the genetic results of Wang et al. (2013) suggesting parallel evolution between humans and dogs. The interesting part of this story is not necessarily the date when dogs and wolves diverged, but the events leading up to that date and the prior relationship between the dog’s ancestor and early humans. This was a relationship that likely changed the evolutionary trajectory of both the canine and the primate.

Citations

Drake AG,Coquerelle M, Colombeau G. 2015. 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic. Scientific Reports 2015/02/05/online. http://dx.doi.org/10.1038/srep08299

Wang GD, et al. (2013). The genomics of selection in dogs and the parallel evolution between dogs and humans. Nature communications, 4, 1860.

More on paleolithic hunters and dogs at Predmosti

Biogeologists have shown how Gravettian people shared their food 30,000 years ago. About 30,000 years ago Predmosti was inhabited by people of the pan-European Gravettian culture, who used the bones of more than 1000 mammoths to build their settlement and to ivory sculptures. Did prehistoric people collect this precious raw material from carcasses -- easy to spot on the big cold steppe -- or were they the direct result of hunting for food? Předmostí I is an exceptional prehistoric site located near Brno in the Czech Republic. Around 30,000 years ago it was inhabited by people of the pan-European Gravettian culture, who used the bones of more than 1000 mammoths to build their settlement and to ivory sculptures. Did prehistoric people collect this precious raw material from carcasses -- easy to spot on the big cold steppe -- or were they the direct result of hunting for food? This year-round settlement also yielded a large number of canids remains, some of them with characteristics of Palaeolithic dogs. Were these animals used to help hunt mammoths?

To answer these two questions, Tübingen researcher Hervé Bocherens and his international team carried out an analysis of carbon and nitrogen stable isotopes in human and animal fossil bones from the site. Working with researchers from Brno and Brussels, the researchers were able to test whether the Gravettian people of Předmostí ate mammoth meat and how the "palaeolithic dogs" fit into this subsistence picture.

They found that humans did consume mammoth -- and in large quantities. Other carnivores, such as brown bears, wolves and wolverines, also had access to mammoth meat, indicating the high availability of fresh mammoth carcasses, most likely left behind by human hunters. Surprisingly, the dogs did not show a high level of mammoth consumption, but rather consumed essentially reindeer meat that was not the staple food of their owners. A similar situation is observed in traditional populations from northern regions, who often feed their dogs with the food that they do not like. These results also suggest that these early dogs were restrained, and were probably used as transportation helpers.

These new results provide clear evidence that mammoth was a key component of prehistoric life in Europe 30,000 years ago, and that dogs were already there to help.

Citation

Bocherens H, Drucker DG, Germonpré M, Lázničková-Galetová M, Naito YI, Wissing C, JBrůžek J, Oliva M. 2014. Reconstruction of the Gravettian food-web at Předmostí I using multi-isotopic tracking (13C, 15N, 34S) of bone collagen. Quaternary International, 2014; DOI:10.1016/j.quaint.2014.09.044

Thoughts on the origin of dogs. 1.

1.    

Jean-Baptist Lamarck seems to be the first scientist to suggest dogs were descended from wolves. In his 1809 Zoological Philosophy he wrote, “No doubt a single, original race, closely resembling the wolf if indeed it was not actually the wolf, was at some period reduced by man to domestication.”

Dog ancestry has been debated ever since Lamarck’s comments and a variety of hypotheses have been proposed and tested in various ways.

Olsen (1985) suggested hominids and wolves have had a relationship that started sometime between 500,000 and 200,000 YPB. He wrote,

“One of the earliest known associations of Canis lupus with hominids (Homo erectus pekinensis) is from the fossil site at Zhoukoudian, located about 42 kilometers southwest of Beijing… Although this association of hominids and wolves at this early period does not imply in any way either taming or early domestication it does place both genera of animals in contemporary association that apparently continued until such time that these events did occur.”

In fact evidence of hominids and canids living in proximity dates to 810,000-760,000 YBP in Spain (Garcia and Arsuaga, 1999); and to about 521,000 YBP at Boxgrove, England. Garcia and Arsuage consider the Boxgrove canid to be Canis mosbachensis. Thus, Olsen’s comment is further supported – the two genera, Canis and Homo have a long relationship, even if it was only sharing the same landscape as competitors – they were part of the same fauna and destined to interact. Keep in mind that members of a fauna adapt to each other, the adaptations may be obvious or subtle.

Stories of dog domestication are numerous, each with their own twists and wrinkles added by the authors, for now I will summarize the domestication event stories by saying. Humans picked up wolf cubs raised them and the wolves adopted their human family. Wolves were selected for tameness and they quickly morphed over generations into the ancestor of the domestic dog of today.

This has become a “just so story” that is relatively well accepted in the minds of the general public and probably most people who study dogs. Just so stories are dangerous because they become dogma until they are replaced with an alternative story based upon a changing paradigm as more contrary evidence accumulates to suggest an alternative scenario.

Most of the popular literature and scientific work affirm Lamarck’s proposal, the grey wolf (Canis lupus) is the ancestor of the domestic dog. Evidence for a close relationship between grey wolves and dogs is quite substantial using morphology, genetics, and the fact that dogs and wolves hybridize. Below is a phylogeny for canids from Linblad et al. (2005), they used a  

“…a high-quality draft genome sequence of the domestic dog (Canis familiaris), together with a dense map of single nucleotide polymorphisms (SNPs) across breeds. The dog is of particular interest because it provides important evolutionary information and because existing breeds show great phenotypic diversity for morphological, physiological and behavioural traits….”

There are a large number of phylogenies in the literature and most of them show a similar arrangement when it comes to dogs and the grey wolf. The arrangement is as sister species – not ancestor-descendant. A general principle of cladistics suggests that when one species separates into two, the ancestral species “dies,” meaning it no longer exists. In its place are the two sister species. Following this idea, Canis lupus and Canis familaris are sister species not ancestor and decedent.  The sister species relationship is supported in numerous studies and should not be controversial.

However, only extant species are represented in the tree. There are likely several to many extinct members of the genus Canis not in the tree because their DNA is not available. If they could be added, the tree would have a different topography. As more fossil Canis are found it is likely ancient DNA will be extracted from them and added to the tree. When this occurs the sister relationship between C. lupus and C. familaris is likely to change.

Our knowledge of canids is still incomplete. Leonard and colleagues (2007) examined remains of 56 ancient wolves from the permafrost near Fairbanks, Alaska and found a continuous population from 12,500 YBP to beyond the capacity of radiocarbon (about 58,000 years) to resolve a date for them. Only a single wolf was dated after the 12,500 year mark, at 7,647 YBP. The older wolf remains showed wider palates with larger carnassial teeth suggesting they had a greater bite force. Their teeth also showed greater degrees of wear suggesting that they were specialized for killing and consuming large prey or habitually scavenging on exceptionally large prey – the megafauna. Leonard and colleagues obtained ancient DNA from 20 of these wolves from the late Pleistocene of eastern Beringia and recovered a haplotype that was not shared with any existing wolf population. The Pleistocene gray wolf was quiet distinct from the modern gray wolf. However, three wolves from the Ukraine and one from Altia (Russia) dated between 30,000 and 28,000 YBP shared the same haplotype as the Fairbanks remains  ―suggesting the Pleistocene Gray Wolf was widely distributed in the Northern Hemisphere from at least 50,000 YBP to about 12,500 YBP. These wolves lived north of the ice sheets. A nitrogen isotope analysis of the bones showed the Pleistocene Gray Wolf preyed and scavenged on mammoth, bison, musk ox and caribou.

The lack of overlap between modern wolves and the Pleistocene wolves is striking and suggests the ancient wolves became extinct and were not ancestral to the modern wolf. As the megafauna herbivores disappeared so did their predators, the Pleistocene Gray Wolf was one of them.

While I don’t claim to have the ultimate answer to dog origins the following seem likely and obvious:

      1) Dogs shared an ancestor with a wolf – but not the extant gray wolf.
2) Dogs are primarily scavengers, but they can act as predators.
3) The social structure found in dogs is not as rigid as that found in extant gray wolves.
4) Dogs and wolves do hybridize, but wolves often show aggression towards domestic dogs, reducing the likelihood of hybridization under natural conditions.
5) The geographic point of origin is likely somewhere in Eurasia as opposed to Africa or North America – but African Canis familaris do show substantial genetic diversity
6) The dog or its ancestor was pre-adapted for interacting with humans.
7)  Humans (and in the broad sense, hominins) have a long history of interacting with dogs (and probably their ancestor), thus dog-human interactions, and dogs as a species predate agriculture.

References

Freedman AH, Gronau I, Schweizer RM, Ortega-Del Vecchyo D, Han E, et al. (2014) Genome Sequencing Highlights the Dynamic Early History of Dogs. PLoS Genetics 10(1): e1004016. doi:10.1371/journal.pgen.1004016

Garcı́a, N., & Arsuaga, J. L. (1999). Carnivores from the Early Pleistocene hominid-bearing Trinchera Dolina 6 (Sierra de Atapuerca, Spain). Journal of Human Evolution, 37(3), 415-430.

Lamarck, JB 1809. Zoological Philosophy: An Exposition with Regard to the Natural History of Animals, vol. 1, Dentu, Paris, France.

Leonard, J. A. C. Vilia, K. Fox-Dobbs, P. L. Koch, R. K. Wayne, and B. V. Valkenburgh. 2007. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Current Biology 17:1146-1150.

Lindblad-Toh, K., et al.  2005. Genome sequence, comparative analysis and haplotype structure of the domestic dog." Nature 438.7069: 803-819.

Olsen, SJ. 1985. The Origins of the Domestic Dog, the Fossil Record. University of Arizona Press.

Ancestry informative markers in wolves and dogs demonstrate hybridization events

Figure 1 from Godinho et al. (2014) (a) Wolf–dog hybrid from 

Barbanza. Photo courtesy of A. Perez. (b) Location of wolf 

reference samples. Approximate wolf distribution area is 

showen in dark grey (Alvares et al. 2005). The red arrow 
shows the location of Barbanza. (c) Distribution of wolf packs 

(100-km2 circles) in Barbanza (red circle) and the surrounding 

area (black circles) between 1999 and 2003. Dots denote the

location of NIS.

Across the globe, millions of free-ranging dogs coexist with a few tens of thousands of wolves. Wolf-dog hybridization provide a classic example of the ecological and conservation implications of hybridization events between wild and domesticated forms. However the ability to understanding the implications of hybridization has been hampered by high genetic similarity and the difficulties in obtaining tissue samples. Consequently, there are many opportunities for wolves and dogs to hybridize, and cumulative data suggest that hybridization may be more frequent than previously suspected. Previous hybridization studies have required the slow and expensive use of tissue samples collected from dead or trapped animals, thus limiting population-level assessments. Furthermore, difficulties have been reported in correctly identifying wolf–dog backcrosses using simulated individuals and sets of 16–18 microsatellites, typically resulting in a large threshold implemented in clustering analyses.

In a forthcoming article Godinho et al. (2014) assess the occurrence and extension of hybridization in a pack of wolf–dog hybrids in northwestern Iberia, Godinho et al. compare the power of 52 nuclear markers implemented on tissue samples with a subset of 13 ancestry informative markers (AIMs) typed in noninvasive samples (NIS).

Godinho et al. (2014) find the 13 AIMs are as accurate as the 52 markers that were chosen without regard to the power to differentiate between wolves and dogs. The AIMs also having the advantage of being rapidly screened on noninvasive samples. The efficiency of AIMs significantly outperformed ten random sets of similar size and an additional commercial set of 18 markers.

Bayesian clustering analysis implemented on AIMs and NIS identified nine hybrids, two wolves and two dogs. Four hybrids were unambiguously assigned to F¹ x Wolf backcrosses. The new approach (AIMs + NIS) overcomes previous difficulties related to sample availability and informative power of markers, allowing a quick identification of wolf–dog hybrids in the first phases of hybridization episodes. This provides managers with a reliable tool to evaluate hybridization and estimate the success of their actions. This approach may be easily adapted for other pairs of wild/domesticated species, thus improving our understanding of the introgression of domestication genes into natural populations.

The hybridization event at Barbanza started with a cross between a female wolf and a male dog, as inferred by the presence of an Iberian wolf mtDNA haplotype in all hybrids, corresponding to the typical direction of wolf–dog hybridization. Despite the uncertainty of the impact of these crosses in the genetic composition of wolf populations (for example, due to difficulties of hybrid integration in packs), the results do suggest that the Barbanza pack has quickly evolved towards a hybrid swarm, with a minimum of two generations of backcrossing to wolves. These findings are alarming because wolf packs in nonexpanding populations generally consist of related individuals, and thus, other unobserved individuals in the area may also exhibit admixed ancestries.

Identifying wolf–dog hybrids is crucial for conservation and management strategies, particularly in the first phases of an episode of hybridization, as well as to evaluate the success of the strategies that have been implemented. Assuming a minimum territory size of 100 km² centered in the rendezvous site of the Barbanza pack, the area sampled covered a substantial portion of that territory (40%).

Moreover, the authors identified 11 wolf-like canids, 80% of the estimated population, which is fully compatible with the values reported in Iberia for pack size after reproduction, plus some floater animals, suggesting that the AIM’s method allows a comprehensive evaluation of hybridization in a given area. The goal to obtain a quick method to identify hybridization events was successful. Once there is the suspicion of a hybridization event, an estimate of about two months would be required to know the extent of the problem in an area equivalent to a pack territory.

Finally, the authors note that the logistic and economic investment to evaluate hybridization in this area was feasible (ca. 1500€ for the fieldwork – one person working 8 days – plus ca. 5000€ for laboratory work – one person working 3 weeks). Current management guidelines state that every practical measure should be implemented to remove obvious hybrids from the wild once an event of hybridization has been detected. This implies mainly lethal control, although keeping hybrids in captivity and sterilization have also been suggested. Nevertheless, the efficiency of removing hybrids from the wild remains very uncertain. Therefore, the methods shown here constitute a step forward towards the effective management of wolf–dog hybridization. The combination of NIS and AIMs may offer an opportunity to better understand the extension and persistence of hybridization between wolves and dogs at a global scale and its ecological, evolutionary and conservation consequences.

Citation

Godinho, R., López‐Bao, J. V., Castro, D., Llaneza, L., Lopes, S., Silva, P., & Ferrand, N. (2014). Real‐time assessment of hybridization between wolves and dogs: combining noninvasive samples with ancestry informative markers. Molecular Ecology Resources. Early On-line.