Here, we for the first time analyzed modern haplotypic composition of a wild boar population introduced at the northern edge of the species’ range and tested three hypotheses about genetic consequences of establishing a population originating from numerous introductions of different subspecies. Below we discuss each hypothesis and outline questions arising from our results.
Phylogenetic lineages in natural and introduced populations
Our phylogenetic tree is similar to other published phylogenies based on the mtDNA control region 18,33,35 in terms of the splitting of the whole dataset into South-Eastern Asian, Eastern, and Western (including Near Eastern) clades. Our analysis was aimed at determining the positions of previously unsampled (or poorly sampled) populations within the reported clades. It yielded several interesting results. First of all, the position of Central-Asian mtDNA samples is unambiguously within the Eastern clade, and most of these haplotypes are situated on the basal branch and do not cluster together. Khalilzadeh et al. (2016) 33 found the “Eastern” haplotypes in eastern Iran, while in southern and western Iran, the “Western” (therefore Near-Eastern and European) haplotypes were predominant. By combining this finding with our data, we propose that the east coast of the Caspian Sea is the western boundary of the Eastern clade. Far-Eastern haplotypes are also (expectedly) in the Eastern clade, and three of them group into a highly supported cluster within this clade. The history of Far-Eastern wild boar populations has been discussed previously in several articles 28,35; for this reason, we did not focus on this topic in this work.
MtDNA samples from the Eastern Caucasus ended up (in equal proportions) in European and Near Eastern clades. Khederzadeh et al. (2019) 34 reported that Dagestanian haplotypes are distant from all the other European individuals and suggested possible gene flow from the Caucasus to southern Europe. Most probably, the haplotypes analyzed in that study belong to the Near-Eastern clade because other haplotypes found in the Eastern Caucasus grouped well with the mtDNA samples found by Niedziałkowska et al. (2021) 42 in Central and Eastern Europe. The presence of highly distant haplotypes in the Eastern Caucasus points to complex history of the wild boar population in this region.
Finally, the haplotypes from the Urals (the introduced population) proved to be affiliated with Eastern, Near-Eastern, and European clades. The current haplotypes found in the Urals could have originated from representatives of different subspecies brought not only from the Caucasus, Central Asia, and Eastern Europe (Belarus and Western Russia) but also from mixed populations transferred to the Urals from Central Russia (Markov et al., in press). The Near-Eastern haplotype found in the Urals is identical to that registered in the Eastern Caucasus. Two of three Asian haplotypes detected in the Ural region are identical to those found in Central Asia (Uzbekistan and Kazakhstan). Whatever the source of these haplotypes is, our results show that Near-Eastern and some Asian mtDNA haplotypes got preserved through many generations and did not go extinct during colonization of the region that is situated at the north-eastern periphery of the geographical range. Of note, in the Urals, we did not find haplotypes identical to those from the Far East, though 123 individuals were released there, and wild boars from the Central-Russian populations could also possess these haplotypes. There may be two explanations. First, the Far-Eastern animals could have migrated from the site of the release to the unsampled parts of the Urals. Second, for some reason, they could go extinct while expanding to new territories. Testing the first supposition would require wider sampling in the Ural region. The second supposition will be discussed in the subsection where we compare the proportions of Western and Eastern haplotypes among released animals to those in the current population.
Predominance of the Western clade and a decline of Eastern mitochondrial lineages in the introduced population of wild boars
We demonstrated that in the Ural population, the proportions of Eastern and Western haplotypes changed in comparison with those at the time of introduction. The strong increase in the proportion of European haplotypes and a respective decrease in Asian haplotypes could be explained in three ways:
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Animals from Asia were not detected in the sampled region because they dispersed to some other territories. Validation of this explanation requires wider sampling across the whole Ural region.
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The proportion of European haplotypes went up due to unofficial releases in the 2000s. Neither the number of individuals released during such unofficial introductions nor their origin are known. It is unlikely that wild boars were brought to the Urals from distant regions of Russia (such as the Russian Far East or Caucasus) or from Central Asia. Most probably, they were taken from local populations or brought from mixed populations of Central Russia, where the European lineage is more prevalent than the Asian one 39. They could also be hybrids between wild boars and domestic pigs. All these factors could affect genetic composition of the introduced population in some way. On the other hand, the current population of wild boars was established much earlier than the 2000s. Thus, we believe that haplotype frequencies in the current population are a consequence of natural processes.
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Our third explanation is that animals carrying Western mitochondrial haplotypes are better adapted for survival and expansion in a new environment than those from the Eastern haplogroup. The lower survival rate of Eastern (particularly Far-Eastern) haplotypes could be caused by two processes. First, the animals from the Caucasus, Central Asia, and Russian Far East could disperse across long distances from the release site. A possible reason is a difference in habitat composition between the Urals and the regions of the animals’ origin (natal habitat preference induction hypothesis 43). More distant dispersal could lead to higher mortality 44 and hence to a decrease in the proportion of Asian haplotypes. The second process is related to genetic diversity in founder populations. Recently, Kostyunina et al. (2022) 45 showed lower genomic variation in Far-Eastern wild boars than in European ones. It is possible that the low genetic variation could cause low adaptability of Far-Eastern wild boars, which in turn has led to the elimination of their mitochondrial haplotypes. Besides, Tsai et al. (2016) 46 demonstrated that domestic pigs with “European” mitochondrial haplotypes produce significantly larger litters, while the haplotypes that cluster with Asian mitochondrial haplotypes have the lowest reproductive efficiency rates.
The prevalence of European haplotypes in the mixed populations of wild boars in Western Russia was reported by Davidova et al. (2013) 39, but their sample sizes in many regions did not exceed 2 individuals, and they did not compare data from mixed populations to those from the founder populations.
The wild boar in the Urals as a model of genetic processes in expanding (or invading) populations
The scenario of wild-boar expansion in the eastern Urals looks similar to the scenarios of this species’ expansions after the Last Glacial Maximum. According to the contraction–expansion hypothesis 47,48, the postglacial expansion of the species proceeded from the few refugia that were typically characterized by high genetic diversity in comparison with the continent in general. In case of the wild boar in the eastern Urals, the sites of releases could be compared to the refugia where many genetic lineages were present before the expansion. Expansion with one lineage dominating the others is similar to the scenarios of expansion of Sus scrofa 29,32 and other mammalian species, e.g., the red deer Cervus elaphus and the European roe deer Capreolus capreolus 49,50, and is in agreement with the postglacial leading edge expansion hypothesis 51,52. Consequently, genetic processes in this population could be used for clarifying temporal dynamics of expanding populations on a larger spatial and temporal scale. Especially interesting is the monitoring of spatial and temporal variation in proportions of dominant and rare genetic lineages and investigating the factors that could shape this variation.
In conclusion, in our analysis based on reliable mtDNA samples from both founders’ and introduced populations, we demonstrate that 38 years after the introductions of various subspecies of the wild boar into the eastern part of the Urals, the current population i) has genetic diversity similar to or higher than that in the founders’ populations, thus supporting hypothesis 1; ii) retains haplotypes from all the major mtDNA lineages (European, Near-Eastern, and Asian) independently of the number of released representatives of these lineages, thereby supporting hypothesis 2; iii) the proportion of the European haplogroup increased while the proportions of other haplogroups decreased in comparison with those suggested for the released individuals, thus refuting hypothesis 3. The last result allows us to theorize that the European genotypes are better adapted for expansion and survival in a new harsh environment in comparison with the Asian genotypes.