The pattern of phylogenomic evolution of the Canidae

Canidae species fall into two categories with respect to their chromosome composition: those with high numbered largely acrocentric karyotypes and others with a low numbered principally metacentric karyotype. Those species with low numbered metacentric karyotypes are derived from multiple independent fusions of chromosome segments found as acrocentric chromosomes in the high numbered species. Extensive chromosome homology is apparent among acrocentric chromosome arms within Canidae species; however, little chromosome arm homology exists between Canidae species and those from other Carnivore families. Here we use Zoo-FISH (fluorescent in situ hybridization, also called chromosomal painting) probes from flow-sorted chromosomes of the Japanese raccoon dog (Nyctereutes procyonoides) to examine two phylogenetically divergent canids, the arctic fox (Alopex lagopus) and the crab-eating fox (Cerdocyon thous). The results affirm intra-canid chromosome homologies, also implicated by G-banding. In addition, painting probes from domestic cat (Felis catus), representative of the ancestral carnivore karyotype (ACK), and giant panda (Ailuropoda melanoleuca) were used to define primitive homologous segments apparent between canids and other carnivore families. Canid chromosomes seem unique among carnivores in that many canid chromosome arms are mosaics of two to four homology segments of the ACK chromosome arms. The mosaic pattern apparently preceded the divergence of modern canid species since conserved homology segments among different canid species are common, even though those segments are rearranged relative to the ancestral carnivore genome arrangement. The results indicate an ancestral episode of extensive centric fission leading to an ancestral canid genome organization that was subsequently reorganized by multiple chromosome fusion events in some but not all Canidae lineages.     

Adult male emigration and a female-based social organization in swift foxes, Vulpes velox

Members of the family Canidae are distinguished from other carnivore families by pair bonding and male care of the young. Because of the importance of food provisioning and territorial defence by males, social structure among canids is shared or even dominated by males. However, small, insectivorous species of canids show little male parental care, although whether social structure differs from other canids is unknown. We combined data from three independent research projects on a small canid, the swift fox, to help elucidate the social organization of this species. Based on data on movements of 35 adult mated pairs and the fate of litters, we found that adult females maintained territories and family structure, whereas adult males tended to emigrate. This is the first evidence of a female-based social organization among any canid species. This type of social organization probably resulted from the decreased importance of territorial defence and food provisioning by males, as their diet is primarily insectivorous during summer when young are weaned. Our results, along with others, indicate that variations in social structure among canid species are strongly influenced by the importance of food provisioning and territorial defence by males.     

A noninvasive method for distinguishing among canid species: amplification and enzyme restriction of DNA from dung

Endangered San Joaquin kit foxes Vulpes macrotis mutica can be sympatrically distributed with as many as four other canids: red fox, gray fox, coyote and domestic dog. Canid scats are often found during routine fieldwork, but cannot be reliably identified to species. To detect and study the endangered kit fox, we developed mitochondrial DNA markers that can be amplified from small amounts of DNA extracted from scats. We amplified a 412-bp fragment of the mitochondrial cytochrome- b gene from scat samples and digested it with three restriction enzymes. The resulting restriction profiles discriminated among all five canid species and correctly identified 10 'unknown' fox scats to species in blind tests. We have applied our technique to identify canids species for an environmental management study and a conservation study. We envision that our protocol, and similar ones developed for other endangered species will be greatly used for conservation management in the future.     

Species-specific features of the distribution of restriction sites in Bsp-repeats of Canidae genome]

Differences and similarities of the Bsp-repeats' organization in fox, dog, polar fox and raccoon dog genomes were studied. Specificity of Bsp-repeats to the Canidae family was demonstrated. The repeats are mainly organized in large clusters in all species studied. The species-specific features in restriction patterns were revealed for all five genomes, in spite of high intragenomic polymorphism exhibited in each case. This suggests that certain unique sets of structural versions of Bsp-repeats were fixed in canid genomes by amplification during the process of speciation. Fox and polar fox exhibited the highest similarity in restriction patterns of Bsp-repeats. Raccoon dog pattern is most unusual among others: its distinguishable character is the absence of large multimeric series. The EcoRI hydrolysate of raccoon dog Bsp-repeats consists mainly of one band corresponding to 1600 bp. These are in accordance with phylogenetic relations between canids.     

Comparative Scaling of Humeral Cross-Sections of Felids and Canids Using Radiographic Images

The cortical thickness of long bones can be an effective indicator of locomotor modes and other stresses encountered by bone. Felids and canids are two carnivoran families that have similar levels of phylogenetic diversity and overlap in body size, but differ in their locomotor habits. Many canids and felids are cursorial, but felids also climb more frequently than canids. Felids also display a secondary use for their forelimbs not observed in any canids: they use their forelimbs to grasp and subdue prey. Large felids use their forelimbs much more extensively to subdue prey than do large canids and, therefore, should have proportionately greater forces applied to their forelimbs. This study uses a non-invasive radiographic approach to examine the differences in cortical thickness in the humerus between the Felidae and Canidae, as well as between size groups within these two families. Results show few significant differences between the two families, with a slight trend toward more positive allometry in the felids. Overall, radiographic measurements were found to be better predictors of body mass than either prey killing behavior or locomotor mode in these two carnivoran families. One canid that demonstrated exceptionally high cortical area was the bush dog, Speothos venaticus. The rarely observed bush dog has been postulated to swim and dig regularly, and it may be that the thickened cortical bone reflects these behaviors.     

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.     

Comparative molecular phylogeny and evolution of sex chromosome DNA sequences in the family Canidae (Mammalia: Carnivora)

To investigate the molecular phylogeny and evolution of the family Canidae, nucleotide sequences of the zinc-finger-protein gene on the Y chromosome (ZFY, 924-1146 bp) and its homologous gene on the X chromosome (ZFX, 834-839 bp) for twelve canid species were determined. The phylogenetic relationships among species reconstructed by the paternal ZFY sequences closely agreed with those by mtDNA and autosomal DNA trees in previous reports, and strongly supported the phylogenetic affinity between the wolf-like canids clade and the South American canids clade. However, the branching order of some species differed between phylogenies of ZFY and ZFX genes: Cuon alpinus and Canis mesomelas were included in the wolf-like canid clades in the ZFY tree, whereas both species were clustered in a group of Chrysocyon brachyurus and Speothos venaticus in the ZFX tree. The topology difference between ZFY and ZFX trees may have resulted from the two-times higher substitution rate of the former than the latter, which was clarified in the present study. In addition, two types of transposable element sequence (SINE-I and SINE-II) were found to occur in the ZFY final intron of the twelve canid species examined. Because the SINE-I sequences were shared by all the species, they may have been inserted into the ZFY of the common ancestor before species radiation in Canidae. By contract, SINE-II found in only Canis aureus could have been inserted into ZFY independently after the speciation. The molecular diversity of SINE sequences of Canidae reflects evolutionary history of the species radiation.     

Unique inhibitory cascade pattern of molars in canids contributing to their potential to evolutionary plasticity of diet

Developmental origins that guide the evolution of dental morphology and dental formulae are fundamental subjects in mammalian evolution. In a previous study, a developmental model termed the inhibitory cascade model was established. This model could explain variations in relative molar sizes and loss of the lower third molars, which sometimes reflect diet, in murine rodents and other mammals. Here, I investigated the pattern of relative molar sizes (inhibitory cascade pattern) in canids, a taxon exhibiting a wide range of dietary habits. I found that interspecific variation in canid molars suggests a unique inhibitory cascade pattern that differs from that in murine rodents and other previously reported mammals, and that this variation reflects dietary habits. This unique variability in molars was also observed in individual variation in canid species. According to these observations, canid species have greater variability in the relative sizes of first molars (carnassials), which are functionally important for dietary adaptation in the Carnivora. In conclusion, an inhibitory cascade that differs from that in murine rodents and other mammals may have contributed to diverse dietary patterns and to their parallel evolution in canids.     

Social Play in the American Black Bear: Its Similarity to Canid Social Play and an Examination of its Identifying Characteristics

Bears evolved from a canid stock at quite a recent date (earlyMiocene). Despite this recent origin, bcars show substantialmorphological, physiologicai, and ecological differences whencompared to modern day canids. However, the display behaviorsof Canidae and Ursidae have remained remarkably similar. Inthis paper, the motor patterns of black bear social play aredescribed in detail. Numerous similarities between canid andursid social play are pointed out. Agonistic displays commonto both families are also pointed out. These behavioral similaritiessupport the principle that social behavior, particularly displaybehavior, will frequently be conservative in its evolution ascompared to the evolution of morphology, anatomy, or ecologicaladaptations. Beach (1945) stressed the importance of identifying and testingthe general characteristics of play. A large number of characteristicshave been suggested as being diagnostic of play, but these characteristicshave received very little testing. Five characteristics of socialplay were tested in this study, and two were found to be onlypartially valid for black bear social play. Extensive testingof the general characteristics of play on as wide a range ofspecies as possible is definitely recommended for future research.     

CRANIAL MORPHOLOGY OF DOMESTIC AND WILD CANIDS: THE INFLUENCE OF DEVELOPMENT ON MORPHOLOGICAL CHANGE

The domestic dog varies remarkably in cranial morphology. In fact, the differences in size and proportion between some dog breeds are as great as those between many genera of wild canids. In this study, I compare patterns of intracranial allometry and morphologic diversity between the domestic dog and wild canid species. The results demonstrate that the domestic dog is morphologically distinct from all other canids except its close relatives, the wolf-like canids. Following this, I compare patterns of static and ontogenetic scaling. Data on growth of domestic dogs are presented and used to investigate the developmental mechanisms underlying breed evolution. Apparently, most small breeds are paedomorphic with respect to certain morphologic characters. In dogs and other domestic animals, morphologic diversity among adults seems to depend on that expressed during development.     

Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis

The world's most endangered canid is the Ethiopian wolf Canis simensis , which is found in six isolated areas of the Ethiopian highlands with a total population of no more than 500 individuals. Ethiopian wolf populations are declining due to habitat loss and extermination by humans. Moreover, in at least one population, Ethiopian wolves are sympatric with domestic dogs, which may hybridize with them, compete for food, and act as disease vectors. Using molecular techniques, we address four questions concerning Ethiopian wolves that have conservation implications. First, we determine the relationships of Ethiopian wolves to other wolf-like canids by phylogenetic analysis of 2001 base pairs of mitochondrial DNA (mtDNA) sequence. Our results suggest that the Ethiopian wolf is a distinct species more closely related to gray wolves and coyotes than to any African canid. The mtDNA sequence similarity with gray wolves implies that the Ethiopian wolf may hybridize with domestic dogs, a recent derivative of the gray wolf. We examine this possibility through mtDNA restriction fragment analysis and analysis of nine microsatellite loci in populations of Ethiopian wolves. The results imply that hybridization has occurred between female Ethiopian wolves and male domestic dogs in one population. Finally, we assess levels of variability within and between two Ethiopian wolf populations. Although these closely situated populations are not differentiated, the level of variability in both is low, suggesting long-term effective population sizes of less than a few hundred individuals. We recommend immediate captive breeding of Ethiopian wolves to protect their gene pool from dilution and further loss of genetic variability.     

The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism

The origin of endemic South American canid fauna has been traditionally linked with the rise of the Isthmus of Panama, suggesting that diversification of the dog fauna on this continent occurred very rapidly. Nevertheless, despite its obvious biogeographic appeal, the tempo of Canid evolution in South America has never been studied thoroughly. This issue can be suitably tackled with the inference of a molecular timescale. In this study, using a relaxed molecular clock method, we estimated that the most recent common ancestor of South American canids lived around 4 Ma, whereas all other splits within the clade occurred after the rise of the Panamanian land bridge. We suggest that the early diversification of the ancestors of the two main lineages of South American canids may have occurred in North America, before the Great American Interchange. Moreover, a concatenated morphological and molecular analysis put some extinct canid species well within the South American radiation, and shows that the dental adaptations to hypercarnivory evolved only once in the South American clade.     

The canid genome: behavioral geneticists' best friend?

We review a range of studies on the genetic contribution to behavior in canid species. We begin by identifying factors that make canids a promising model in behavioral genetics and proceed to review research over the last decade that has used canids to identify genetic contributions to behavior. We first review studies that have selectively bred dogs to identify genetic contributions to behavior and then review studies that estimate heritability from populations of non‐laboratory bred dogs. We subsequently review studies that used molecular genetics to identify gene–behavior associations and note associations that have been uncovered. We then note challenges in canid behavioral genetics research that require further consideration. We finish by suggesting alternative phenotyping methods and identify areas in which canids may have as yet unexploited advantages, such as in gene–environment interaction studies where genetic factors are found to moderate the effects of environmental variables.     

Chromosomal evolution of the Canidae. I. Species with high diploid numbers

The Giemsa banding patterns of seven canid species, including the grey wolf (Canis lupus), the maned wolf (Chrysocyon brachyurus), the bush dog (Speothos venaticus), the crab-eating fox (Cerdocyon thous), the grey fox (Urocyon cinereoargenteus), the bat-eared fox (Otocyon megalotis), and the fennec (Fennecus zerda), are presented and compared. Relative to other members of Canidae, these species have high diploid complements (2n greater than 64) consisting of largely acrocentric chromosomes. They show a considerable degree of chromosome homoeology, but relative to the grey wolf, each species is either missing chromosomes or has unique chromosomal additions and rearrangements. Differences in chromosome morphology among the seven species were used to reconstruct their phylogenetic history. The results suggest that the South American canids are closely related to each other and are derived from a wolf-like progenitor. The fennec and the bat-eared fox seem to be recent derivatives of a lineage that branched early from the wolf-like canids and which also includes the grey fox.     

A Global overview of canids used in traditional medicines

Canids are among the mammal species most frequently used in traditional folk medicine around the world. In this context, this paper assesses the global use of canids in traditional folk medicine and their implications. Our review indicated that 19 species of canid are used in traditional medicine worldwide, representing 54.2% of described canid species. Of the species in medicinal use, two are listed as Endangered and three as near threatened on the IUCN Red List. For some species medicinal use represents an additional direct pressure that may have contributed to declines of natural populations. In addition, use of medicinal animals may have indirect impacts on the conservation of other species through the spread of disease. To minimize both harvest impacts and disease spread, guidance on use of medicinal species may be useful. This could include an exploration of the use of alternatives and implementation of sanitary measures.     

Asymmetrical intraguild interactions with coyotes,red foxes,and domestic dogs may contribute to competitive exclusion of declining gray foxes

Species coexistence is governed by availability of resources and intraguild interactions including strategies to reduce ecological overlap. Gray foxes are dietary generalist mesopredators expected to benefit from anthropogenic disturbance, but populations have declined across the midwestern USA, including severe local extirpation rates coinciding with high coyote and domestic dog occurrence and low red fox occurrence. We used data from a large‐scale camera trap survey in southern Illinois, USA to quantify intraguild spatial and temporal interactions among the canid guild including domestic dogs. We used a two‐species co‐occurrence model to make pairwise assessments of conditional occupancy and detection rates. We also estimated temporal activity overlap among species and fit a fixed‐effects hierarchical community occupancy model with the four canid species. We partitioned the posterior distributions to compare gray fox occupancy probabilities conditional on estimated state of combinations of other species to assess support for hypothesized interactions. We found no evidence of broadscale avoidance among native canids and conclude that spatial and temporal segregation were limited by ubiquitous human disturbance. Mean guild richness was two canid species at a site and gray fox occupancy was greater when any combination of sympatric canids was also present, setting the stage for competitive exclusion over time. Domestic dogs may amplify competitive interactions by increasing canid guild size to the detriment of gray foxes. Our results suggest that while human activities can benefit some mesopredators, other species such as gray foxes may serve as bellwethers for habitat degradation with trophic downgrading and continued anthropogenic homogenization.     

Concerted evolution of light satellite DNA in genus Mus implies amplification and homogenization of large blocks of repeats

Light satellite DNA components present in species belonging to the genus Mus and to related murids were studied using the Southern blot technique. The results show species variations in both the amount and periodic structure of the repeating units, which suggests that families of related higher-order repeats developed in a common ancestor and were then amplified and/or deleted to different extents during the subsequent evolutionary period. Although the patterns generated by a series of type B enzymes (restriction enzymes that possess sites in a limited number of segments making up the total satellite DNA) in the species closely related to the M. musculus complex were very similar, sequence analysis of cloned unit repeats in two of these species (M. musculus domesticus and M. spretoides) showed near fixation of species-diagnostic variant nucleotides. This suggests that the important amplification and homogenization events that occurred after the divergence of M. spretus must have involved large blocks of sequences.     

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.     

Highly repetitive component α and related alphoid DNAs in man and monkeys

The genomes of Old-World, New-World, and prosimian primates contain members of a large class of highly repetitive DNAs that are related to one another and to component DNA of the African green monkey by their sequence homologies and restriction site periodicities. The members, of this class of highly repetitive DNAs are termed the alphoid DNAs, after the prototypical member, component of the African green monkey which was the first such DNA to be identified (Maio, 1971) and sequenced (Rosenberg et al., 1978). The alphoid DNAs appear to be uniquely primate sequences. — From the restriction enzyme cleavage patterns and Southern blot hybridizations under different stringency conditions, the alphoid DNAs comprise multiple sequence families exhibiting varying degrees of homology to component DNA. They also share common elements in their restriction site periodicities (172 · n base-pairs), in the long-range organization of their repeating units, and in their banding behavior in CsCl and Cs₂SO₄ buoyant density gradients, in which they band within the bulk DNA as cryptic repetitive components. — In the three species from the Family Cercopithecidae examined, the alphoid DNAs represent the most abundant, tandemly repetitive sequence components, comprising about 24% of the African green monkey genome and 8 to 10% of the Rhesus monkey and baboon genomes. In restriction digests, the bulk of the alphoid DNAs among the Cercopithecidae appeared quantitatively reduced to a simple series of arithmetic segments based on a 172 base-pair (bp) repeat. In contrast with these simple restriction patterns, complex patterns were observed when human alphoid DNAs were cleaved with restriction enzymes. Detailed analysis revealed that the human genome contains multiple alphoid sequence families which differ from one another both in their repeat sequence organization and in their degree of homology to the African green monkey component DNA. — The finding of alphoid sequences in other Old-World primate families, in a New-World monkey, and in a prosimian primate attests to the antiquity of these sequences in primate evolution and to the sequence conservatism of a large class of mammalian highly repetitive DNA. In addition, the relative conservatism exhibited by these sequences may distinguish the alphoid DNAs from more recently evolved highly repetitive components and satellite DNAs which have a more restricted taxonomical distribution.     

Convergence and divergence in prey of sympatric canids and felids: opportunism or phylogenetic constraint?

Since the canids and felids diverged in the mid‐Eocene or earlier, each family has developed a suite of morphological and behavioural adaptations for obtaining and consuming prey. We here distinguish between prey taxa captured and eaten as a result of these phylogenetic adaptations, and those because they are fortuitously encountered, and argue that such supplementary prey, often opportunistically caught, create a buffer between sympatric, and potentially competitive, canids and felids and thus enhance coexistence. We base our analysis on dietary data derived from the stomach contents of four sympatric canid and felid species in the Free State Province, South Africa (canids: Cape fox Vulpes chama and black‐backed jackal Canis mesomelas; felids: African wild cat Felis silvestris lybica and caracal Caracal caracal), and from results of studies on these species elsewhere in southern Africa. The two canid species preyed heavily on invertebrates, and thus opportunistically, while the felids (especially the caracal) concentrated on mammals, prey they are phylogenetically adapted to capture. Only three species of mammalian prey are shared by the four species. The ratio of opportunistically‐to‐phylogenetically mediated prey taxa used (the O/P ratio) differ between the species, with the black‐backed jackal having the most opportunistically caught taxa in its diet, and the caracal the least. As predicted, a comparison of this data with those from dietary studies of the same species carried out elsewhere indicates that the number of opportunistically obtained prey taxa varies more than those resulting from phylogenetic adaptations. The largest canid had the widest food spectrum (35 prey taxa) while the smallest felid had the most restricted one (11 prey taxa). We argue that using the O/P distinction allows a better understanding of changes in food niche breadth of particular species, especially in xeric areas, and gives a better indication of possible exploitative competition for food by sympatric carnivores than when regarding all prey taxa as actively pursued. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 527–538.