The peopling of Scandinavia and origin of the Sami

Archaeological studies have shown that humans were present in the northernmost parts of Europe soon after the end of the last glaciation, about 10 000 YBP. The finding of a western European origin of most mitochondrial haplogroups in Sami, dated at around the time of the last glacial maximum about 18 000 YBP,14, 15 suggests that these haplogroups have arisen in the populations inhabiting small refuges in Europe during that time. The colonization of the European continent after the last glaciation allowed the spread of mitochondrial lineages eastwards, possibly leading to the eastern European origin of some of the Sami mtDNA haplogroups, dated at about 8000 YBP.14, 15 It has been suggested that during the same time period, there was an influence from Mongolian and Finno-Ugric people in eastern Europe, consistent with the finding of mitochondrial haplogroups with an Asian origin in the Sami population.16 Although previous data from protein polymorphisms, blood groups, mtDNA and the Y-chromosome have indicated a contribution from Asian populations, the extent of this contribution to the Sami gene pool has not been quantified. A previous study of HLA class II variation indicated a closer relationship between a Sami population from north-western Russia and Oriental (Japanese and Korean) populations compared to non-Sami European populations.35 As that study was based on HLA typing with a lower genetic resolution than employed in our study, the two datasets are difficult to compare.

The high frequency of some class I and class II alleles in our Sami samples that are characteristic of European populations, supports the theory that the Sami gene pool is predominantly of European origin. At the same time, the high frequency of some alleles and haplotypes in the Sami population that are rare in other European populations but common in Northeast Asian (particularly Siberian) and Native American populations, provides strong evidence of a genetic contribution to the Sami from Asian populations. Our MDS and phylogenetic network analyses both place the Swedish Sami in close vicinity to other European populations, whereas some analyses indicate a similarity to some Siberian populations. The relationship among populations differs somewhat between the class I and class II loci, emphasizing the need to use multiple loci for studying the genetic relationships between populations. In the phylogenetic network for the class II loci, northern Sami were found in the group with Northeast Asian populations, in between South and North Siberian populations. Interestingly this phylogeny is similar to a previous study of SNP variation in the non-recombining part of the Y-chromosome.36

The admixture analysis also indicates that the main contribution to the Swedish Sami is from European populations, but shows a surprisingly high Asian influence (13%). The admixture estimates might depend on the choice of parental populations and we presently lack complete HLA data on most Asian populations. However, since using different contemporary Asian populations in the analyses does not change the admixture proportion substantially (data not shown), this does not appear to be a very serious limitation. In the STRUCTURE analyses based on the genotypes of individuals, about 30% of the northern Sami individuals have a genotype composition which resembles that of Northeast Asian populations. In our STRUCTURE analysis we chose to infer four population clusters. Estimating the most supported number of clusters (K) for a dataset is not trivial. Since, for our dataset, the likelihood continues to increase with increasing K (eg, due to isolation by distance or inbreeding37), we focused on a value of K=4, which captures most of the structure in the data and seems biologically relevant.

Although the estimates for time of admixture and effective population size are tentative and depend on a number of assumptions, they are interesting in relation to hypotheses for the origin of the Sami. The time estimated for admixture in the southern Sami (5300 YBP) is earlier than the presumed colonization of northern Sweden by other European populations. This might suggest that people from Central Europe reached the southern part of the Sami range earlier than previously assumed, or may reflect a migration of Sami to the southern part of their range, which at that time was already populated by other European tribes. The wide confidence interval for the estimates includes both the possibility of recent admixture or an early migration of non-Sami populations to northern Scandinavia.

The estimated effective population sizes indicate that the Sami population has existed at a size roughly 20% of the effective size of the non-Sami Swedish population. The Sami are not known to have experienced a dramatic bottleneck in historic times, but are believed to have maintained a relatively constant, but limited, population size over time. The LD between microsatellite markers has been shown to be 2–3 times higher in the southern Sami than in the non-Sami Swedish population, consistent with a more limited population size.38 Interestingly, Kauppi and collegues39 found the LD in 75 kb of MHC class II region to be similar between Sami and UK Europeans, but that many haplotypes were population specific. Our data shows that some of the HLA alleles (eg, DRB1*0801) have a much higher frequency in the northern Sami than in any other human population used for comparison. This could reflect demographic events, such as a bottleneck or genetic drift, or be the result of specific selection for this or other alleles (eg, B*2705) on the same haplotype. Indeed, our Ewens–Watterson analysis indicates that selection has been acting on two of the class II loci, consistent with the finding that balancing selection has been acting on some HLA polymorphisms.19 In addition, the smaller effective population size in both the northern and southern Sami populations makes them more sensitive to genetic drift. However, due to lack of information on nature of the putative selection, we cannot distinguish between selection and drift (or a combination of the two) as explanations for the unusually high frequency of these alleles.

Both the higher number of HLA alleles in the southern Sami and the larger allelic overlap with alleles present in the non-Sami Swedish population, are indicative of recent admixture between the southern Sami and the non-Sami Swedish population. Under this assumption of admixture between a putative ancestral Sami population (represented by the northern Sami) and the non-Sami Swedish population, the proportion of non-Sami Swedish influence in the southern Sami was estimated to be 58%. An independent estimate based on mtDNA also indicated considerable (48%) admixture of non-Sami European ancestry in the southern Sami.16

In summary, the HLA class I and class II analyses show that the main genetic contribution to the Swedish Sami has come from European populations. However, the estimated Asian influence in the northern Sami is higher than that indicated by other genetic markers. The genetic contribution from Asian populations to the southern Sami is lower compared to the northern Sami, most likely due to significant admixture with the non-Sami Swedish population.