Post by Admin on May 4, 2023 18:35:47 GMT
Analysis of genetic continuity across Britain
The Pictish data allow us to obtain a transect of Iron Age/early medieval genomes across Britain and directly look at the pattern of haplotype sharing between them and present-day genomes. The Iron Age and Roman period (except 6DT3) individuals from England and Scotland share more IBD segments >1 cM (both in terms of number and length) with present-day individuals from Scotland (including Orkney), Northern Ireland and Wales than with any other European populations included in our analyses (Figs 3 and S20), consistent with the structure observed in the PCA analysis (Fig 2A). We also show that all early medieval individuals (excluding I0777) share more IBD with modern Danish than with any other present-day population (Fig 3), suggesting genetic continuity between modern-day Danish and the ancestors of these individuals (section S1.6 in S1 Text).
The analysis also revealed high IBD sharing between early medieval individuals from England and present-day people across Britain following a southeast/northwest cline (Figs 4 and S22). This pattern suggests that northern continental European ancestry associated with Anglo-Saxon migrations expanded out of south-eastern England followed by admixture with local populations, a scenario consistent with previous research [11,14,17,18,46,47]. BAL003 and LUN004 share a high proportion of IBD segments with present-day people from western Scotland, Wales and Northern Ireland, similar to the individuals from Late Iron Age Orkney and England (Figs 4 and S22). However, unlike these individuals, LUN004, and to a lesser extent BAL003, shares fewer IBD segments with the present-day eastern Scottish population sample (Figs 4 and S22). Byrne et al. [47] and Gilbert et al. [46] previously suggested that the genetic structure between western and eastern Scotland could result from the divide between the kingdoms of the Gaelic-speaking Dál Riata in the west and Picts in the east, which is seemingly in contradiction with the results presented here. Instead, the present-day genetic structure in Scotland likely results from more complex demographic processes that cannot be reduced to a single model.
Fig 4. Average IBD sharing >1 cM between present-day and ancient groups from the UK.
IBD sharing between each of the ancient genomes and modern samples is illustrated in S22 Fig. Ancient individuals are indicated with coloured symbols. The black dots represent the geographic location of present-day people from 35 regions of the UK [11, 53], by the county town.
We propose two non-exclusive processes that might explain the observed pattern of IBD sharing between the Iron Age and early medieval populations and the present-day Scottish population. The first is substantial admixture from immigrants that brought Iron Age Orcadian-, and England-like ancestries (likely independently), which partially replaced the eastern Scottish early medieval gene pool. Indeed, in the following centuries (1,100–1,300 CE), eastern Scotland received substantial immigration, such as settlers from Britain south of the Forth, France, and the Low Countries [48–50]. Under this scenario, BAL003 and LUN004 are good representatives of the broader ancestry present in Scotland during the Pictish period. Alternatively, the ancestors of BAL003 and LUN004 share more IBD segments with present-day people from western Scotland, Wales, and Northern Ireland because they (or their direct ancestors) migrated from these regions but did not contribute substantially to later generations via admixture with local groups in eastern Scotland. This scenario is consistent with an emerging picture of west-east lifetime mobility of both males and females in the early medieval period in Scotland [51,52]. Under such a model, it may be feasible that there are indeed still undiscovered ‘pockets’ of eastern Pictish-period ancestry, that was differentiated from ancestry carried by BAL003 and LUN004 and which contributed significantly to present-day populations from eastern Scotland. Oxygen and strontium isotope analysis of teeth from these individuals holds promise to characterise this further. Importantly, we also emphasise that stochasticity likely affected the pattern of IBD sharing in such a small sample size. Indeed, high variability in IBD sharing is observed amongst individuals from the early medieval and Iron Age groups, and to some extent between BAL003 and LUN004 (S22Fig).
Our results also show substantial IBD sharing between Iron Age, Viking Age and present-day Orcadians, supporting our observations using allele-frequency based methods of strong genetic continuity in this region over time (Figs 2, 4, and S22). Therefore, the marked genetic differentiation between Orkney and mainland Britain is not only a result of Scandinavian admixture, as previously hypothesised [11,46,54–57] but also pronounced genetic continuity that persisted for at least 2,000 years. The relatively low IBD sharing between BAL003 and LUN004 and modern-day Orcadians (Fig 4) suggests the emergence of Pictish culture in Orkney [22,23,37] was not associated with population replacement but largely due to cultural diffusion and connections.
IBD segments in Iron Age individuals from south-eastern England are widespread throughout western and northern Britain compared to the more recent Romano-British individuals from northern England; the latter, however, do not share substantial IBD with any present-day people of the British Isles (Figs 4 and S22). The only exception is 6DT3 who was from the same genetic population as two early medieval individuals (I0159 and I0773) with Scandinavian-, and northern European-like ancestry (‘pop12’, S22 Fig and section S1.6 in S1 Text). 6DT3 also share relatively more IBD segments >1 cM with the present-day population from Scandinavia, Belgium and the UK (Fig 3), suggesting that Scandinavian-like ancestry could have spread to the British Isles before the early medieval period.
These results need to be interpreted with caution because of existing flaws in the IBD segment detection. First, it has previously been demonstrated that the false positive rate (genomic regions falsely attributed to IBD segments) is high, especially for small IBD segments [43]. They are usually created from the concatenation of shorter IBD segments into a false longer one. The false positive rate is around 10–40% for ≤2 cM IBD segments, but decreases with the length of the segment and is close to 0% for IBD segments ≥5 cM. Several factors can influence this rate, the main ones being data quality and population history. The detection of false positives varies with the density and informativeness of genetic markers. For example, segments of the genome containing many rare alleles are easier to identify as IBD. Regions with low SNP density will be associated with a higher false positive rate. Ralph and Coop [43] also detected significant variation in the false positive rate between populations for IBD segments <2 cM, with populations from Spain, Portugal and Italy showing significantly higher false positive rates than other European populations. A likely explanation given by the authors is that IBD detection algorithms are based on haplotype frequency, so the false positive rate should increase in populations that are more differentiated from the rest of the sample; in this case, they are the populations sharing the least common genetic ancestors both within their respective populations and with other European populations. A second flaw is the low power to detect true small IBD <2 cM, as demonstrated in [43] using fastIBD [58]. They estimate that the power of detecting <2 cM IBD segments is <50%. However, in the present study, we used RefinedIBD [59], which was shown to be more powerful in detecting true 1–2 cM IBD segments, reaching 40% power for 1 cM IBD segments (with segment LOD >3), against only 20% using fastIBD. One possible reason that can break down haplotypes is genotyping error [43, 60]; however, we merged segments having at most one discordant homozygote <0.6 cM apart (see section S1.6 in S1 Text) to overcome this issue. Other effects could influence IBD detection, such as a higher chance of difference in recombination rates among ancient samples and the HapMap dataset or presence of structural variants [61].
The Pictish data allow us to obtain a transect of Iron Age/early medieval genomes across Britain and directly look at the pattern of haplotype sharing between them and present-day genomes. The Iron Age and Roman period (except 6DT3) individuals from England and Scotland share more IBD segments >1 cM (both in terms of number and length) with present-day individuals from Scotland (including Orkney), Northern Ireland and Wales than with any other European populations included in our analyses (Figs 3 and S20), consistent with the structure observed in the PCA analysis (Fig 2A). We also show that all early medieval individuals (excluding I0777) share more IBD with modern Danish than with any other present-day population (Fig 3), suggesting genetic continuity between modern-day Danish and the ancestors of these individuals (section S1.6 in S1 Text).
The analysis also revealed high IBD sharing between early medieval individuals from England and present-day people across Britain following a southeast/northwest cline (Figs 4 and S22). This pattern suggests that northern continental European ancestry associated with Anglo-Saxon migrations expanded out of south-eastern England followed by admixture with local populations, a scenario consistent with previous research [11,14,17,18,46,47]. BAL003 and LUN004 share a high proportion of IBD segments with present-day people from western Scotland, Wales and Northern Ireland, similar to the individuals from Late Iron Age Orkney and England (Figs 4 and S22). However, unlike these individuals, LUN004, and to a lesser extent BAL003, shares fewer IBD segments with the present-day eastern Scottish population sample (Figs 4 and S22). Byrne et al. [47] and Gilbert et al. [46] previously suggested that the genetic structure between western and eastern Scotland could result from the divide between the kingdoms of the Gaelic-speaking Dál Riata in the west and Picts in the east, which is seemingly in contradiction with the results presented here. Instead, the present-day genetic structure in Scotland likely results from more complex demographic processes that cannot be reduced to a single model.
Fig 4. Average IBD sharing >1 cM between present-day and ancient groups from the UK.
IBD sharing between each of the ancient genomes and modern samples is illustrated in S22 Fig. Ancient individuals are indicated with coloured symbols. The black dots represent the geographic location of present-day people from 35 regions of the UK [11, 53], by the county town.
We propose two non-exclusive processes that might explain the observed pattern of IBD sharing between the Iron Age and early medieval populations and the present-day Scottish population. The first is substantial admixture from immigrants that brought Iron Age Orcadian-, and England-like ancestries (likely independently), which partially replaced the eastern Scottish early medieval gene pool. Indeed, in the following centuries (1,100–1,300 CE), eastern Scotland received substantial immigration, such as settlers from Britain south of the Forth, France, and the Low Countries [48–50]. Under this scenario, BAL003 and LUN004 are good representatives of the broader ancestry present in Scotland during the Pictish period. Alternatively, the ancestors of BAL003 and LUN004 share more IBD segments with present-day people from western Scotland, Wales, and Northern Ireland because they (or their direct ancestors) migrated from these regions but did not contribute substantially to later generations via admixture with local groups in eastern Scotland. This scenario is consistent with an emerging picture of west-east lifetime mobility of both males and females in the early medieval period in Scotland [51,52]. Under such a model, it may be feasible that there are indeed still undiscovered ‘pockets’ of eastern Pictish-period ancestry, that was differentiated from ancestry carried by BAL003 and LUN004 and which contributed significantly to present-day populations from eastern Scotland. Oxygen and strontium isotope analysis of teeth from these individuals holds promise to characterise this further. Importantly, we also emphasise that stochasticity likely affected the pattern of IBD sharing in such a small sample size. Indeed, high variability in IBD sharing is observed amongst individuals from the early medieval and Iron Age groups, and to some extent between BAL003 and LUN004 (S22Fig).
Our results also show substantial IBD sharing between Iron Age, Viking Age and present-day Orcadians, supporting our observations using allele-frequency based methods of strong genetic continuity in this region over time (Figs 2, 4, and S22). Therefore, the marked genetic differentiation between Orkney and mainland Britain is not only a result of Scandinavian admixture, as previously hypothesised [11,46,54–57] but also pronounced genetic continuity that persisted for at least 2,000 years. The relatively low IBD sharing between BAL003 and LUN004 and modern-day Orcadians (Fig 4) suggests the emergence of Pictish culture in Orkney [22,23,37] was not associated with population replacement but largely due to cultural diffusion and connections.
IBD segments in Iron Age individuals from south-eastern England are widespread throughout western and northern Britain compared to the more recent Romano-British individuals from northern England; the latter, however, do not share substantial IBD with any present-day people of the British Isles (Figs 4 and S22). The only exception is 6DT3 who was from the same genetic population as two early medieval individuals (I0159 and I0773) with Scandinavian-, and northern European-like ancestry (‘pop12’, S22 Fig and section S1.6 in S1 Text). 6DT3 also share relatively more IBD segments >1 cM with the present-day population from Scandinavia, Belgium and the UK (Fig 3), suggesting that Scandinavian-like ancestry could have spread to the British Isles before the early medieval period.
These results need to be interpreted with caution because of existing flaws in the IBD segment detection. First, it has previously been demonstrated that the false positive rate (genomic regions falsely attributed to IBD segments) is high, especially for small IBD segments [43]. They are usually created from the concatenation of shorter IBD segments into a false longer one. The false positive rate is around 10–40% for ≤2 cM IBD segments, but decreases with the length of the segment and is close to 0% for IBD segments ≥5 cM. Several factors can influence this rate, the main ones being data quality and population history. The detection of false positives varies with the density and informativeness of genetic markers. For example, segments of the genome containing many rare alleles are easier to identify as IBD. Regions with low SNP density will be associated with a higher false positive rate. Ralph and Coop [43] also detected significant variation in the false positive rate between populations for IBD segments <2 cM, with populations from Spain, Portugal and Italy showing significantly higher false positive rates than other European populations. A likely explanation given by the authors is that IBD detection algorithms are based on haplotype frequency, so the false positive rate should increase in populations that are more differentiated from the rest of the sample; in this case, they are the populations sharing the least common genetic ancestors both within their respective populations and with other European populations. A second flaw is the low power to detect true small IBD <2 cM, as demonstrated in [43] using fastIBD [58]. They estimate that the power of detecting <2 cM IBD segments is <50%. However, in the present study, we used RefinedIBD [59], which was shown to be more powerful in detecting true 1–2 cM IBD segments, reaching 40% power for 1 cM IBD segments (with segment LOD >3), against only 20% using fastIBD. One possible reason that can break down haplotypes is genotyping error [43, 60]; however, we merged segments having at most one discordant homozygote <0.6 cM apart (see section S1.6 in S1 Text) to overcome this issue. Other effects could influence IBD detection, such as a higher chance of difference in recombination rates among ancient samples and the HapMap dataset or presence of structural variants [61].