Because of its unique evolutionary history, the genus Canis is a valuable model system to study the evolutionary response to environmental change at the species level and the inter-specific interactions level. The grey wolf (Canis lupus) is one of the few large carnivoran mammals that survived the period of megafaunal extinctions during the Late Pleistocene and maintained large geographic range in the Holarctic. Similar as other large mammalian species, the wolf experienced a considerable demographic decline at the end of the Pleistocene (e.g. Pilot et al. 2014), which was associated with local extinctions and changes in the phylogeographic structure of the species (e.g. Pilot et al. 2010, 2019).
At the end of the Pleistocene, when the wolf was experiencing these changes, one of its evolutionary lineages started a process of adaptation to a new ecological niche of a scavenger feeding with the food remains left by humans, which started the process of the evolution of the domestic dog (Canis lupus familiaris) (reviewed in Freedman & Wayne 2017). According to one of the leading theories on the wolf domestication, this process resulted from ecological changes in population of this species at the end of the Pleistocene, and its initial stage did not necessarily result from deliberate human actions aimed at the creation of a domesticated subspecies (see Frantz & Larson 2018). The domestic dog was the first domesticated animal and the only large carnivoran mammals that became domesticated. The evolutionary success of the domesticated subspecies had an important effect on the wild wolf populations, resulting in the food competition, transmission of diseases and hybridisation (see Lescureux & Linnell 2014).
The golden jackal (Canis aureus) is a medium-sized wolf-like canid species, native to Middle East and large parts of Southern Asia. Historical distribution in Europe, exact date of species appearance and its source population remain controversial or insufficiently studied. Until recently jackal distribution in Europe was mostly restricted to Adriatic and Black Sea cost and small, isolated populations in Balkans. Over the last two decades rapid northwards expansion of golden jackal is observed, most likely due to anthropogenic factors (climate change and habitat transformation). It has been suggested that the distribution and abundance of golden jackals is to be limited by the presence of wolves and interspecific killing was reported (Mohammadi et al. 2017). However, there is also growing evidence for hybridization events between golden jackals and other canid species (Galov et al. 2015, Moura et al. 2014). As the current jackal distribution increasingly overlaps with the areas occupied by wolves, more frequent inter-species encounters can be expected in future. Our current research is focused on interactions between golden jackals, wolves and domestic dogs.
References
Frantz L.A., Larson G. 2018. A genetic perspective on the domestication continuum. Pages 41-56 in Hybrid Communities. Red. Stépanoff C., Vigne J.-D. Routledge, London.
Freedman A.H., Wayne R.K. 2017. Deciphering the origin of dogs: From fossils to genomes. Annual Review of Animal Biosciences, 5: 281-307.
Galov A., Fabbri E., Caniglia R., Arbanasić H., Lapalombella S., Florijančić T., Bošković I., Randi E. 2015. First evidence of hybridization between golden jackal (Canis aureus) and domestic dog (Canis familiaris) as revealed by genetic markers. Royal Society Open Science 2 (12): 1‑14.
Lescureux, N., & Linnell, J.D.C. 2014. Warring brothers: The complex interactions between wolves (Canis lupus) and dogs (Canis familiaris) in a conservation context. Biological Conservation, 171: 232–245.
Mohammadi A., Kaboli M., López-Bao J. V. 2017. Interspecific killing between wolves and golden jackals in Iran. European Journal of Wildlife Research, 63, 61.
Moura A.E., Tsingarska E., Dąbrowski M.J., Czarnomska S.D., Jędrzejewska B., Pilot M. 2014. Unregulated hunting and genetic recovery from a severe population decline: the cautionary case of Bulgarian wolves. Conservation Genetics, 15: 407-415.
Pilot M., Branicki W., Jędrzejewski W., Goszczyński J., Jędrzejewska B., Dykyy I., Shkvyrya M., Tsingarska E. 2010. Phylogeographic history of grey wolves in Europe. BMC Evolutionary Biology, 10: 104.
Pilot M., Greco C., vonHoldt B.M., Jędrzejewska B., Randi E., Jędrzejewski W., Sidorovich V.E., Ostrander E.A., Wayne R.K. 2014. Genome-wide signatures of population bottlenecks and diversifying selection in European wolves. Heredity, 112: 428–442.
Pilot M., Moura A. E., Okhlopkov I. M., Mamaev N. V., Alagaili A. N., Mohammed O. B., Yavruyan E. G., Manaseryan N. H., Hayrapetyan V., Kopaliani N., Tsingarska E., Krofel M., Skoglund P., Bogdanowicz W. (2019). Global phylogeographic and admixture patterns in grey wolves and genetic legacy of an ancient Siberian lineage. Scientific Reports, 9: 1-13.
CURRENT RESEARCH
Causes and consequences of canid hybridisation Our recent study demonstrated that more than 60% of wolves in Eurasia carry in their genomes small DNA fragments originating from past hybridisation with dogs (Pilot et al. 2018). Wolf-dog hybrids are fertile and can interbreed with individuals from their both parents' populations, resulting in the retention of hybridisation-derived genetic variants in gene pools of wolves and dogs – a process called introgression. Recent studies based on the analysis of complete genomes showed that introgression has played a profound and complex role in evolution, affecting a broad range of animal and plant species. Introgression can lead to a decreased fitness of admixed individuals or even the extinction of a species via “genetic swamping” – a gradual increase in the frequency of genetic variants from a different species until native variants disappear from the gene pool. However, in some circumstances exchange of genetic variants between species or subspecies can help them adapt to rapid environmental change. Therefore, ability to predict the consequences of introgression is crucial for effective mitigation of impacts of the ongoing climate change on wild animals. Yet factors determining the costs and benefits of hybridisation are largely unknown, and difficult to study in cases where interbreeding species share similar phenotypes.
In the current project, we aim at understanding the evolutionary consequences of hybridisation using the genus Canis as a model system. The advantage of genus Canis is that all its representatives – from apex predators heavily affected by anthropogenic changes to domestic dogs that are well adapted to living in human-dominated ecosystems – can naturally interbreed despite their great morphological and behavioural diversification. The study will address important questions regarding the introgressive hybridisation process: What factors affect the introgression rate of hybridisation-derived variants? In which circumstances the benefits of hybridisation are higher than its costs? What are the functions of genes where hybridisation-derived variants are under positive selection? How does hybridisation with dogs affect phenotypic traits of wild canids? By addressing these questions, we aim at defining the circumstances when introgressive hybridisation can constitute an adaptive evolutionary process or when it should be prevented as a threat to the species. This will guide the management strategies and legal regulations for increasingly common admixed populations. The project is funded by the Polish National Science Center (NCN; Sonata BIS programme) and the Polish National Agency for Academic Exchange (NAWA; Polish Returns Programme).
Testing the Domestication Syndrome hypothesis in free-ranging domestic dogs Domestic animals differ significantly from their wild ancestors in many morphological, physiological and behavioral traits. All domestic animals have limited aggression and limited fear of humans compared to their wild ancestors. Many species of domestic mammals also have characteristic morphological features, such as large variation in coat colour, floppy ears and curly tails. Different domesticated species have a similar set of modified phenotypic traits, called “Domestication Syndrome”. According to the hypothesis that explains the co-occurrence of these traits, they have a common origin during embryonic development, and therefore the selection pressure (natural or artificial) on one of these traits could lead to correlated changes in the whole set of traits. A growing number of studies suggest that domestication may have affected gene regulatory networks that control the rate of migration of neural crest cells. Neural crest cells are stem cells that develop at the edge of the neural tube during the vertebrate embryonic development, and migrate throughout the developing body to give rise to various tissue types and organs and influence a range of neurobiological and physiological functions. Therefore, changes in the migration rate of these cells may underlie the Domestication Syndrome. On the other hand, several recently published papers questioned the existence of the Domestication Syndrome, suggesting that individual traits characteristic of domestic animals could have arisen as a result of the independent action of natural selection on each of these traits. In this project we will test the hypothesis that the phenotypic features characteristic of domestic mammals constitute a Syndrome and that they have an origin in the reduction of the migration rate of neural crest cells. As a model for this research, we will use free-ranging domestic dogs. A multidisciplinary approach developed for this project, based on a combination of behavioural, genetic and ecological methods, will allow us to test the relationship between genetic variation and behavioural and morphological traits of free-living dogs, for which the potential adaptive functions of these traits can be very important. This is a collaborative project with Dr Sarah Marshall-Pescini and Prof. Friederike Range from the Konrad Lorenz Institute of Ethology, University of Veterinary Medicine Vienna. The project is funded by the Austrian Science Fund (Fonds zur Förderung der wissenschaftlichen Forschung, FWF) and the Polish National Science Center (NCN).
PAST RESEARCH
Our earlier work contributed to knowledge of the factors shaping the evolutionary history of wolves and dogs with the following findings:
Modern evolutionary lineages of wolves in Europe represent only a small proportion of the species' genetic diversity during the Late Pleistocene (Pilot et al. 2010).
The probable cause of the genetic diversity loss was the continuous demographic decline of wolf populations since the Last Glacial Maximum, resulting from climate change (Pilot et al. 2014a, b).
Genetic differentiation among wolf populations is strongly correlated with differences in their habitat type and diet composition, implying the limited gene flow among populations living in habitats that differ in the composition of ungulate species, which are the main wolf prey (Pilot et al. 2006, 2012).
Contemporary phylogeographic structure of the wolf is considerably different from the phylogeographic structure of this species in the Late Pleistocene; the change of this structure probably resulted from the extinction of the evolutionary lineages specialised in hunting large ungulates associated with the ecosystem of Late Pleistocene steppes (Pilot et al. 2010).
Genetic diversity of wolves from the Iberian and Apennine Peninsulas shows that they experienced a long-term bottleneck effect as a result of geographic isolation and small population sizes. Morphological differentiation between these populations and wolves from Eastern Europe result from both genetic drift and natural selection acting on genes associated with the embryonic development and growth (Pilot et al. 2014a).
The domesticated wolf subspecies, the domestic dog, is characterised by an extensive morphological diversification within inbred lines (breeds), but smaller diversification among free-ranging dogs. Relaxation of natural and sexual selection in pure-bred dogs as compared with free-ranging dogs could have led to differentiation in the regulation of the Hedgehog signalling pathway, which downregulates the migration of neural crest cells from the neural tube. Small deficit of these cells during embryonic development results in the modifications of various morphological and physiological traits, which may provide a mechanism of differentiation among dog breeds (Pilot et al. 2016).
Free-ranging dog populations are genetically distinct from pure-bred dogs and they did not originate from admixture between different breeds. Contemporary phylogeographic structure of free-ranging dogs in Eurasia was shaped by a large-scale geographic expansion from East Asia westwards, through central and west Asia to the Middle East and Europe, which occurred during the Neolithic (Pilot et al. 2015).
Due to the lack of reproductive barriers, wolves and dogs can cross-breed and produce fertile offspring. Our research on wolf-dog hybridisation showed that this process has been occurring during the recent generations as well as in the more distant history of both subspecies. As a result, 62% of Eurasian wolves studied carried a small percentage of alleles originating from dogs. This result shows that the evolutionary histories of wolves and dogs have been interconnected from the time of divergence of their lineages until present (Pilot et al. 2018).
Unregulated hunting on wolves contributes to the increase in the wolf-dog hybridisation rate due to the disruption of the pack structure (Moura et al. 2014).
Global phylogeographic structure of wolves is affected by local admixture with dogs, coyotes and golden jackals, suggesting that introgression from ecologically diverse con-specific and con-generic populations was common in the wolf evolutionary history (Pilot et al. 2019).