Thursday, October 2, 2014

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.

Wednesday, October 1, 2014

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.


Paleodogs and the date of domestication

Top. A fox skull used to illustrated greatest patatal breadth 
and condylobasal length. Bottom. A bivariate plot from 
Morey (2014) of GPB (Greatest Palatal Breadth) by CL 
(Condylobasal Length) for three groups of modern or 
Holocene wolves, and one series of established prehistoric
dogs, post-dating 10,000 BP, from North America and Europe.
 The contours indicate the range of plotted scores for each 
group. Superimposed on this plot are the corresponding values 
for several putative Paleolithic dogs. Using CL as a guide, one 
can see that the putative Paleolithic dogs are wolf-sized, but 
have unusually broad palatal dimensions. A comparable plot is 
provided by Boudadi-Maligne and Escarguel (2014: 86, Fig. 5),
 based on the same variables and using a larger series of wolves. 
That plot includes the earliest of the putative Paleolithic dogs
 considered here (Goyet Cave, Razboinichya Cave, Predmostí), 
and shows the same basic result.
In a forth coming article Morey (2014) examines the evidence for paleodogs, dogs that are older than the fossil record has traditionally supported.

Archaeological evidence has, for a very long time placed the origin of the domestic dog between 15,000 to 12,000 YBP. But, recent works report fossil evidence suggesting a much earlier origin, dating to Paleolithic times and perhaps exceeding 100,000 years. With such studies as a backdrop, scenarios for more ancient dates for dog origins and domestication have been made and they exceed 30,000 YPB. Morey examines this evidence and suggests such studies exhibit conceptual and methodological flaws.

When a series of cases for putative Paleolithic dogs is assessed, the author finds convincing cases for such dogs are confined to about the past 15,000 years. Morey looks at the timing of reproduction and skull and tooth morphometrics and with two exceptions, finds the putative Paleolithic dogs fall within the range of established wolves. See the figure for an explanation. Thus, the morphometrics do not support the assessment of these canids as dogs.

He also discusses the age at first reproduction of wolves and dogs, noting it may have been almost two years for wild wolves; and noting captive wolves may breed much sooner. The point being that even first reproduction at two years old, the generational time translates into dozens of generations over a mere few hundred years. Combined with directional selection, the wolf/dog would change its morphology substantially in a very short time. So genetic isolation was likely not in place at first, resulting in some delay in the recognizable appearance of certain domestication traits. But, genetic isolation was never complete, since dogs and wolves continue to hybridize to a limited degree to the present day. Therefore, he concludes that allowing for modest delay in the appearance of domestication changes, 16,000-17,000 YBP is a reasonable estimate for the beginnings of sustained canid domestication.

The morphometric evidence is somewhat at odds with the genetic data. One study done in 1997 suggests dogs diverged from wolves somewhere between 100,000 to 30,000 YPB. A more recent (2013) study using mitochondrial genomes estimates 33,000 to 18,000 YBP, and a yet more recent study (2014) places the divergence date of wolves and dogs between 50,000 and 11,000, although the authors, suggest that a more recent date is probable.

Resolving the differences in the molecular studies with the morphometrics promises to be challenging and as several recent authors have suggested, the domestication of the dog is much more complex than previously imagined.


Citation
Morey, D. F. (2014). In Search of Paleolithic Dogs: A Quest with Mixed Results. Journal of Archaeological Science. 52:300-307.