Limb morphology of domestic and wild canids: the influence of development on morphologic change

Biomechanical hypotheses are often invoked to explain the characteristic scaling of limb proportions. Patterns of static allometry and morphologic diversity, however, may also reflect the developmental mechanisms underlying morphologic change. In this study I document the importance of such developmental influences on the evolution of limb morphology in the extremely polymorphic domestic dog and in wild canid species. I use bivariate and discriminant function analyses to compare the limb morphology of adult dogs and wild canid species. I then compare ontogenetic allometry of four dog breeds with static allometry of domestic and wild canids. Results reveal, first, that there is considerable similarity between dogs and wild canid species; many wolf-like canids cannot be distinguished from domestic dogs of equivalent size. However, all dogs are consistently separated from fox-sized, wild canids by subtle but evolutionarily significant differences in olecranon, metapodial, and scapula morphology. Second, in domestic dogs the pattern of static allometry is nearly identical to that of ontogenetic allometry. This finding can be attributed to simple heterochronic alterations of postnatal growth rates. Apparently the diversity of limb proportions among adult domestic dogs and the observed difference between dogs and wild canids are somewhat predetermined, as they directly reflect the diversity of limb proportions evident during development of the domestic dog.     

Developmental constraints on limb growth in domestic and some wild canids

The domestic dog varies remarkably in limb size. Presumably, such differences in limb size stem from inequities in postnatal specific growth rate. I test this hypothesis by examining the postnatal growth of limb bones (40–250 days post-partum) in four dog breeds of dramatically different adult size; Lhasa Apso, Cocker Spaniel, Labrador Retriever and Great Dane. The results show that the limb bones of these four breeds have similar specific growth rates throughout most of postnatal development. Thus, proportionate differences in limb bone length are established during perinatal growth (0–40 days post-partum) or before birth.
Comparisons of postnatal growth in the Great Dane and two wild canids of dramatically different leg length, the Bush dog ( Speothos venaticus ) and the Maned wolf ( Chrysocyon brachyurus ) also show a near congruency of specific growth rate curves. However, despite these similarities, the adult limb proportions of small dogs and small wild canids are different. Dogs also differ from wild canids in the relative variability of gestation time. All dogs have a similar gestation period of 60–63 days which is independent of birth weight, whereas the two are directly related in wild canids. I suggest that small dogs may differ in limb proportions from small wild canids because the latter have a shorter gestation period. Thus, the relative invariability of gestation time in domestic dogs may act as a fundamental constraint on their morphologic variability.     

Phenotypic disparity of the elbow joint in domestic dogs and wild carnivores*

In this article, I use geometric morphometrics in 2D from a sample of 366 elbow joints to quantify phenotypic disparity in domestic dog breeds, in wild canids, and across the order Carnivora. The elbow joint is a well‐established morphological indicator of forearm motion and, by extension, of functional adaptations toward locomotor or predatory behavior in living carnivores. The study of the elbow joint in domestic dogs allows the exploration of potential convergences between (i) pursuit predators and fast‐running dogs, and (ii) ambush predators and fighting breeds. The results indicate that elbow shape disparity among domestic dogs exceeds than in wolves; it is comparable to the disparity of wild Caninae, but is significantly lower than the one observed throughout Canidae and Carnivora. Moreover, fast‐running and fighting breeds are not convergent in elbow joint shape with extreme pursuit and ambush wild carnivores, respectively. The role of artificial selection and developmental constraints in shaping limb phenotypic disparity through the extremely fast evolution of the domestic dog is discussed in the light of this new evidence.     

A Simple Genetic Architecture Underlies Morphological Variation in Dogs

Domestic dogs exhibit tremendous phenotypic diversity, including a greater variation in body size than any other terrestrial mammal. Here, we generate a high density map of canine genetic variation by genotyping 915 dogs from 80 domestic dog breeds, 83 wild canids, and 10 outbred African shelter dogs across 60,968 single-nucleotide polymorphisms (SNPs). Coupling this genomic resource with external measurements from breed standards and individuals as well as skeletal measurements from museum specimens, we identify 51 regions of the dog genome associated with phenotypic variation among breeds in 57 traits. The complex traits include average breed body size and external body dimensions and cranial, dental, and long bone shape and size with and without allometric scaling. In contrast to the results from association mapping of quantitative traits in humans and domesticated plants, we find that across dog breeds, a small number of quantitative trait loci (≤3) explain the majority of phenotypic variation for most of the traits we studied. In addition, many genomic regions show signatures of recent selection, with most of the highly differentiated regions being associated with breed-defining traits such as body size, coat characteristics, and ear floppiness. Our results demonstrate the efficacy of mapping multiple traits in the domestic dog using a database of genotyped individuals and highlight the important role human-directed selection has played in altering the genetic architecture of key traits in this important species.     

Out of southern East Asia: the natural history of domestic dogs across the world

The origin and evolution of the domestic dog remains a controversial question for the scientific community, with basic aspects such as the place and date of origin, and the number of times dogs were domesticated, open to dispute. Using whole genome sequences from a total of 58 canids (12 gray wolves, 27 primitive dogs from Asia and Africa, and a collection of 19 diverse breeds from across the world), we find that dogs from southern East Asia have significantly higher genetic diversity compared to other populations, and are the most basal group relating to gray wolves, indicating an ancient origin of domestic dogs in southern East Asia 33 000 years ago. Around 15 000 years ago, a subset of ancestral dogs started migrating to the Middle East, Africa and Europe, arriving in Europe at about 10 000 years ago. One of the out of Asia lineages also migrated back to the east, creating a series of admixed populations with the endemic Asian lineages in northern China before migrating to the New World. For the first time, our study unravels an extraordinary journey that the domestic dog has traveled on earth.     

Serologic evidence of Leishmania infection in free-ranging wild and domestic canids around a Brazilian National Park

Transmission of disease between wildlife, domestic animals, and humans is of great concern to conservation issues and public health. Here we report on the prevalence of anti-Leishmania sp. antibodies in 21 wild canids (7 Chrysocyon brachyurus, 12 Cerdocyon thous, and 2 Lycalopex vetulus) and 74 free domestic dogs (Canis familiaris) sampled around the Serra do Cipó National Park. In dogs, the apparent prevalence was 8.1% and in wild canids it was 19% (2 crab-eating foxes, C. thous, and 2 maned wolves, C. brachyurus). Management of the domestic dog population with evaluation of incidence changes in humans and wildlife, and enlightenment on the role of wild reservoirs are essential issues for future action and research.     

Unequal contribution of sexes in the origin of dog breeds

Dogs (Canis familiaris) were domesticated from the gray wolf (Canis lupus) at least 14,000 years ago, and there is evidence of dogs with phenotypes similar to those in modern breeds 4000 years ago. However, recent genetic analyses have suggested that modern dog breeds have a much more recent origin, probably <200 years ago. To study the origin of contemporaneous breeds we combined the analysis of paternally inherited Y chromosome markers with maternally inherited mitochondrial DNA and biparentally inherited autosomal microsatellite markers in both domestic dogs and their wild ancestor, the gray wolf. Our results show a sex bias in the origin of breeds, with fewer males than females contributing genetically, which clearly differs from the breeding patterns in wild gray wolf populations where both sexes have similar contributions. Furthermore, a comparison of mitochondrial DNA and Y chromosome diversity in dog groups recognized by the World Canine Organization, as well as in groups defined by the breeds' genetic composition, shows that paternal lineages are more differentiated among groups than maternal lineages. This demonstrates a lower exchange of males than of females between breeds belonging to different groups, which illustrates how breed founders may have been chosen.     

Studies of modern Italian dog populations reveal multiple patterns for domestic breed evolution

Through thousands of years of breeding and strong human selection, the dog (Canis lupus familiaris) exists today within hundreds of closed populations throughout the world, each with defined phenotypes. A singular geographic region with broad diversity in dog breeds presents an interesting opportunity to observe potential mechanisms of breed formation. Italy claims 14 internationally recognized dog breeds, with numerous additional local varieties. To determine the relationship among Italian dog populations, we integrated genetic data from 263 dogs representing 23 closed dog populations from Italy, seven Apennine gray wolves, and an established dataset of 161 globally recognized dog breeds, applying multiple genetic methods to characterize the modes by which breeds are formed within a single geographic region. Our consideration of each of five genetic analyses reveals a series of development events that mirror historical modes of breed formation, but with variations unique to the codevelopment of early dog and human populations. Using 142,840 genome‐wide SNPs and a dataset of 1,609 canines, representing 182 breeds and 16 wild canids, we identified breed development routes for the Italian breeds that included divergence from common populations for a specific purpose, admixture of regional stock with that from other regions, and isolated selection of local stock with specific attributes.     

Observations of scent-marking and discriminating self from others by a domestic dog (Canis familiaris): tales of displaced yellow snow

Little is known about what stimuli trigger urinating or scent-marking in domestic dogs, Canis familiaris, or their wild relatives. While it is often suggested that the urine of other animals influences urinating and scent-marking patterns in canids, this has not been verified experimentally. To investigate the role of urine in eliciting urinating and marking, in this pilot study I moved urine-saturated snow ('yellow snow') from place-to-place during five winters to compare the responses of an adult male domestic dog, Jethro, to his own and others' urine. Jethro spent less time sniffing his own urine than that of other males or females, and that while his interest in his own urine waned with time it remained relatively constant for other individuals' urine. Jethro infrequently urinated over or sniffed and then immediately urinated over (scent-marked) his own urine. He marked over the urine of other males more frequently than he marked over females' urine. The method used here can be extended to other species for which experimental data are lacking. Though based on one dog, these novel data may further our knowledge of the role of scent-marking in territorial behavior and of sex differences in territory acquisition and maintenance.     

Detection of Echinococcus granulosus coproantigens in Australian canids with natural or experimental infection

Coproparasitological and purging methods for diagnosing canids infected with the intestinal helminth Echinococcus granulosus, an important zoonotic parasite, are unreliable. Detection of coproantigens in feces of infected dogs by enzyme-linked immunosorbent assay (ELISA) is suitable for detecting patent and prepatent infections with a high degree of sensitivity and specificity. In the present study, natural and experimental infections in domestic and wild Australian canids were investigated using a coproantigen capture ELISA. Experimental infection of dogs with E. granulosus was detected at between 14 and 22 days postinfection (PI), and optical density (OD) values remained high until termination of experiments 35 days PI. After chemotherapy, coproantigen levels in infected dogs dropped rapidly, becoming negative 2-4 days after treatment. In experimentally infected red foxes (Vulpes vulpes), the coproantigen excretion profile was different, with ELISA OD levels peaking 15-17 days PI, then falling to low or undetectable levels by 30 days PI. Coproantigens were detected in the feces of naturally infected Australian wild dogs (dingoes, dingo/domestic dog hybrids) with infection levels ranging between 2 worms and 42,600. Preliminary data on the stability of coproantigen in dog feces exposed to environmental conditions indicated that there was no change in antigenicity over 6 days. The results suggest the coproantigen ELISA could be successfully used to monitor E. granulosus prevalence rates in Australian domestic dogs, foxes, and wild dogs.     

Genetic characterization of four native Italian shepherd dog breeds and analysis of their relationship to cosmopolitan dog breeds using microsatellite markers

Very little research into genetic diversity of Italian native dog breeds has been carried out so far. In this study we aimed to estimate and compare the genetic diversity of four native Italian shepherd dog breeds: the Maremma, Bergamasco, Lupino del Gigante and Oropa shepherds. Therefore, some cosmopolitan dog breeds, which have been widely raised in Italy for a long time past, have also been considered to check possible influence of these dog populations on the Italian autochthonous breeds considered here. A total of 212 individuals, belonging to 10 different dog breeds, were sampled and genotyped using 18 autosomal microsatellite loci. We analyzed the genetic diversity of these breeds, within breed diversity, breed relationship and population structure. The 10 breeds considered in this study were clearly genetically differentiated from each other, regardless of current population sizes and the onset of separate breeding history. The level of genetic diversity explained 20% of the total genetic variation. The level of H_E found here is in agreement with that found by other studies. The native Italian breeds showed generally higher genetic diversity compared with the long established, well-defined cosmopolitan dog breeds. As the Border Collie seems closer to the Italian breeds than the other cosmopolitan shepherd dogs considered here, a possible utilization of this breed to improve working performance in Italian traditional working shepherd dogs cannot be ignored. The data and information found here can be utilized in the organization of conservation programs planned to reduce inbreeding and to minimize loss of genetic variability.     

History of canids in Chile and impacts on prey adaptations

Artiodactyl prey species of Chile, especially guanacos (Lama guanicoe), are reported to be very susceptible to predation by pack‐hunting feral dogs. It has been previously suggested that guanacos and endemic South American deer may have evolved in the absence of pack‐hunting cursorial predators. However, the paleoecology of canid presence in southern South America and Chile is unclear. Here, we review the literature on South American and Chilean canids, their distributions, ecologies, and hunting behavior. We consider both wild and domestic canids, including Canis familiaris breeds. We establish two known antipredator defense behaviors of guanacos: predator inspection of ambush predators, for example, Puma concolor, and rushing at and kicking smaller cursorial predators, for example, Lycalopex culpaeus. We propose that since the late Pleistocene extinction of hypercarnivorous group‐hunting canids east of the Andes, there were no native species creating group‐hunting predation pressures on guanacos. Endemic deer of Chile may have never experienced group‐hunting selection pressure from native predators. Even hunting dogs (or other canids) used by indigenous groups in the far north and extreme south of Chile (and presumably the center as well) appear to have been used primarily within ambush hunting strategies. This may account for the susceptibility of guanacos and other prey species to feral dog attacks. We detail seven separate hypotheses that require further investigation in order to assess how best to respond to the threat posed by feral dogs to the conservation of native deer and camelids in Chile and other parts of South America.     

Artificial insemination in canids: a useful tool in breeding and conservation

Artificial insemination (AI) and semen freezing have become services available to dog owners worldwide, and the demand for services to freeze semen is increasing. In other canids such as the fox, the fur industry utilizes fresh or frozen semen to artificially inseminate vixens to produce pelts. Clearly, AI facilitates the use of a male to sire several females by diluting the ejaculate, increases breeding hygiene, and allows crossing between species with slightly different breeding seasons. The African wild dog (Lycaon pictus) is currently considered by the World Conservation Union (IUCN) as one of most endangered canids. In captive populations of African wild dogs, semen has been frozen with encouraging results, using a standard cryopreservation protocol for domestic dogs, but successful AI has not been reported. In wolves, there is one report regarding the live birth of an offspring after intravaginal AI of a deslorelin-induced estrous female. In 2005, three Mexican gray wolf females were artificially bred by intrauterine insemination with freshly collected semen from unrelated males, and all females whelped. Artificial insemination may be vaginal, intrauterine or intratubal, and the semen may be fresh, fresh and chilled (diluted), or frozen-thawed, and the source of semen may be epididymal or ejaculated. In the domestic dog, the results are good to excellent for AI with all three types of processed semen when the source is ejaculated semen, whereas epididymal sperm still yields poorer results. Species differences in female physiology, as well as differences in the cryotolerance of the sperm from various canid species, warrant further research and development.     

Phylogenetic distinctiveness of Middle Eastern and Southeast Asian village dog Y chromosomes illuminates dog origins

Modern genetic samples are commonly used to trace dog origins, which entails untested assumptions that village dogs reflect indigenous ancestry or that breed origins can be reliably traced to particular regions. We used high-resolution Y chromosome markers (SNP and STR) and mitochondrial DNA to analyze 495 village dogs/dingoes from the Middle East and Southeast Asia, along with 138 dogs from >35 modern breeds to 1) assess genetic divergence between Middle Eastern and Southeast Asian village dogs and their phylogenetic affinities to Australian dingoes and gray wolves (Canis lupus) and 2) compare the genetic affinities of modern breeds to regional indigenous village dog populations. The Y chromosome markers indicated that village dogs in the two regions corresponded to reciprocally monophyletic clades, reflecting several to many thousand years divergence, predating the Neolithic ages, and indicating long-indigenous roots to those regions. As expected, breeds of the Middle East and East Asia clustered within the respective regional village dog clade. Australian dingoes also clustered in the Southeast Asian clade. However, the European and American breeds clustered almost entirely within the Southeast Asian clade, even sharing many haplotypes, suggesting a substantial and recent influence of East Asian dogs in the creation of European breeds. Comparison to 818 published breed dog Y STR haplotypes confirmed this conclusion and indicated that some African breeds reflect another distinct patrilineal origin. The lower-resolution mtDNA marker consistently supported Y-chromosome results. Both marker types confirmed previous findings of higher genetic diversity in dogs from Southeast Asia than the Middle East. Our findings demonstrate the importance of village dogs as windows into the past and provide a reference against which ancient DNA can be used to further elucidate origins and spread of the domestic dog.     

Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps

Abstract The management of wild canids (wild dogs/dingoes and foxes) presents a conservation dilemma for land managers across Australia. These canids are predators of wildlife and domestic stock but dingoes are considered native and anecdotal reports suggest that they may suppress foxes such that dingo/dog conservation may have a net benefit to wildlife. This study examines dietary and spatial interactions between wild dogs and foxes in the Greater Blue Mountains region of NSW to address the possibility of suppression through competitive exclusion by dogs on foxes. Predator diets were compared using faecal analysis as well as an analysis of 19 dietary studies from similar forest habitats in eastern Australia. Spatial relationships were examined using data from an extensive canid control programme. Diets of wild dogs and foxes showed a high degree of overlap in species taken, indicating potential for competition. But there was also evidence of resource partitioning with the size and arboreality of mammalian prey differing between the two predators. Wild dogs and foxes responded to different landscape‐scale variation in the physical environment, but there was no clear evidence of large‐scale differences in their distribution. At the fine scale there was a negative association between these predators that indicated possible temporal avoidance or localized habitat shifts. Therefore, there is evidence for dietary competition and fine‐scale exclusion, but no support for landscape‐scale exclusion of foxes by wild dogs in the Blue Mountains.     

Evolutionary genomics of dog domestication

We review the underlying principles and tools used in genomic studies of domestic dogs aimed at understanding the genetic changes that have occurred during domestication. We show that there are two principle modes of evolution within dogs. One primary mode that accounts for much of the remarkable diversity of dog breeds is the fixation of discrete mutations of large effect in individual lineages that are then crossed to various breed groupings. This transfer of mutations across the dog evolutionary tree leads to the appearance of high phenotypic diversity that in actuality reflects a small number of major genes. A second mechanism causing diversification involves the selective breeding of dogs within distinct phenotypic or functional groups, which enhances specific group attributes such as heading or tracking. Such progressive selection leads to a distinct genetic structure in evolutionary trees such that functional and phenotypic groups cluster genetically. We trace the origin of the nuclear genome in dogs based on haplotype-sharing analyses between dogs and gray wolves and show that contrary to previous mtDNA analyses, the nuclear genome of dogs derives primarily from Middle Eastern or European wolves, a result more consistent with the archeological record. Sequencing analysis of the IGF1 gene, which has been the target of size selection in small breeds, further supports this conclusion. Finally, we discuss how a black coat color mutation that evolved in dogs has transformed North American gray wolf populations, providing a first example of a mutation that appeared under domestication and selectively swept through a wild relative.     

Origin and phylogenetic analysis of Tibetan Mastiff based on the mitochondrial DNA sequence

At present, the Tibetan Mastiff is the oldest and most ferocious dog in the world. However, the origin of the Tibetan Mastiff and its Phylogenetic relationship with other large breed dogs such as Saint Bernard are unclear. In this study, the primers were designed according to the mitochondrial genome sequence of the domestic dog, and the 2,525 bp mitochondrial sequence, containing the whole sequence of Cytochrome b, tRNA-Thr, tRNA-Pro, and control region of the Tibetan Mastiff, was obtained. Using grey wolves and coyotes as outgroups, the Tibetan Mastiff and 12 breeds of domestic dogs were analyzed in phylogenesis. Tibetan Mastiff, domestic dog breeds, and grey wolves were clustered into a group and coyotes were clustered in a group separately. This indicated that the Tibetan Mastiff and the other domestic dogs originated from the grey wolf, and the Tibetan Mastiff belonged to Carnivora, Canidae, Canis, Canis lupus, Canis lupus familiaris on the animal taxonomy. In domestic dogs, the middle and small breed dogs were clustered at first; German Sheepdog, Swedish Elkhound, and Black Russian Terrier were clustered into one group, and the Tibetan Mastiff, Old English Sheepdog, Leonberger, and Saint Bernard were clustered in another group. This confirmed the viewpoint that many of the famous large breed dogs worldwide Such as Saint Bernard possibly had the blood lineage of the Tibetan Mastiff, based on the molecular data. According to the substitution rate, we concluded that the approximate divergence time between Tibetan Mastiff and grey wolf was 58,000 years before the present (YBP), and the approximate divergence time between other domestic dogs and grey wolf was 42,000 YBP, demonstrating that the time of origin of the Tibetan Mastiff was earlier than that of the other domestic dogs.     

The <Emphasis Type="Italic">IGF1</Emphasis>small dog haplotype is derived from Middle Eastern grey wolves

Background

A selective sweep containing the insulin-like growth factor 1 (IGF1) gene is associated with size variation in domestic dogs. Intron 2 of IGF1 contains a SINE element and single nucleotide polymorphism (SNP) found in all small dog breeds that is almost entirely absent from large breeds. In this study, we surveyed a large sample of grey wolf populations to better understand the ancestral pattern of variation at IGF1 with a particular focus on the distribution of the small dog haplotype and its relationship to the origin of the dog.

Results

We present DNA sequence data that confirms the absence of the derived small SNP allele in the intron 2 region of IGF1 in a large sample of grey wolves and further establishes the absence of a small dog associated SINE element in all wild canids and most large dog breeds. Grey wolf haplotypes from the Middle East have higher nucleotide diversity suggesting an origin there. Additionally, PCA and phylogenetic analyses suggests a closer kinship of the small domestic dog IGF1 haplotype with those from Middle Eastern grey wolves.

Conclusions

The absence of both the SINE element and SNP allele in grey wolves suggests that the mutation for small body size post-dates the domestication of dogs. However, because all small dogs possess these diagnostic mutations, the mutations likely arose early in the history of domestic dogs. Our results show that the small dog haplotype is closely related to those in Middle Eastern wolves and is consistent with an ancient origin of the small dog haplotype there. Thus, in concordance with past archeological studies, our molecular analysis is consistent with the early evolution of small size in dogs from the Middle East.See associated opinion by Driscoll and Macdonald: http://jbiol.com/content/9/2/10