Abstract
BackgroundIn Europe, golden jackals (Canis aureus) have been expanding their range out of the southern and southeastern Balkans towards central Europe continually since the 1960s. Here, we investigated the level of functional diversity at the MHC class II DLA-DQA1 exon 2 in golden jackal populations from Bulgaria, Serbia, and Hungary. Specifically, we tested for positive selection on and geographic variation at that locus due to adaptation to supposedly regionally varying pathogenic landscapes. To test for potential fitness effects of different protein variants on individual body condition, we used linear modeling of individual body mass indexes (bmi) and accounted for possible age, sex, geographical, and climatic effects. The latter approach was performed, however, only on Serbian individuals with appropriate data.ResultsOnly three different DLA-DQA1 alleles were detected, all coding for different amino-acid sequences. The neutrality tests revealed no significant but positive values; there was no signal of spatial structuring and no deviation from the Hardy–Weinberg equilibrium across the studied range of expansion. However, we found a signal of trans-species polymorphism and significant test results for positive selection on three codons. Our information-theory based linear modeling results indicated an effect of ambient temperature on the occurrence of individual DLA-DQA1 genotypes in individuals from across the studied expansion range, independent from geographical position. Our linear modeling results of individual bmi values indicated that yearlings homozygous for DLA-DQA1*03001 reached values typical for adults contrary to yearlings carrying other genotypes (protein combinations). This suggested better growth rates and thus a possible fitness advantage of yearlings homozygous for DLA-DQA1*03001.ConclusionsOur results indicate a demographic (stochastic) signal of reduced DLA-DQA1 exon 2 variation, in line with the documented historical demographic bottleneck. At the same time, however, allelic variation was also affected by positive selection and adaptation to varying ambient temperature, supposedly reflecting geographic variation in the pathogenic landscape. Moreover, an allele effect on body mass index values of yearlings suggested differential fitness associated with growth rates. Overall, a combination of a stochastic effect and positive selection has shaped and is still shaping the variation at the studied MHC locus.
Highlights
In Europe, golden jackals (Canis aureus) have been expanding their range out of the southern and southeastern Balkans towards central Europe continually since the 1960s
We investigated the level of functional diversity at the Major Histocompatibility Complex (MHC) class II Dog leukocyte antigen system (DLA)-DQA1 exon 2 in the golden jackal populations that have over the last 50–60 years expanded continuously from Bulgaria into Serbia, and presumably from there into Hungary [2, 30]
In total, of all 164 golden jackals studied from Bulgaria, Serbia and Hungary (Fig. 1), only three different DLA-DQA1 alleles based on eight polymorphic nucleotide positions were detected (Fig. 2); all of them were already found previously in canid species (Fig. 3)
Summary
In Europe, golden jackals (Canis aureus) have been expanding their range out of the southern and southeastern Balkans towards central Europe continually since the 1960s. In Europe, golden jackals have historically been restricted to some occurrences on the Balkans where they have experienced a drastic decline until the 1960s due to habitat loss and overhunting Their subsequent recovery in the 1960s and 1970s under legislative protection has eventually led to an initially slow but continuous northward expansion of their range towards central Europe from the 1980s onward (e.g., [2]) with the latest reproduction record from as far north as Poland [3] and beyond. Since pathogenic selection may vary over space and time due to various ecological factors, such as community structure, prevalence of intermediate hosts, and habitat-specific transmission rates, the immunogenetic diversity of those expanding golden jackal populations may reflect a response to adaptation to likely varying regional pathogenic landscapes
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