Incest Uncovered at Elite Prehistoric Irish Burial Site

Home , Carrowmore, County Sligo, Irish Mesolithic, Newgrange

at the PAR, regardless of whether it was meiosis than do spermatocytes. This finding the proteins can accumulate between the X or Y; by contrast, the PAR derived from therefore suggests that the duration of early separated axes. These non-exclusive models the low-mo-2 parent did not. Moreover, meiosis might be differentially regulated to provide intriguing fodder for future research. Acquaviva and colleagues showed that mo-2 meet the different biological imperatives of How double-strand breaks are formed at arrays, along with sufficient accumulation of sperm and eggs — with a longer time frame the PAR has been a conundrum for the field. RMMAI, can lead to structural remodelling of allowing vulnerable regions such as the PAR to Acquaviva and colleagues’ model paints an non-sex chromosomes — at the end of chro- accumulate sufficient double-strand breaks. elegant picture of how a genetic element, chromosome 9, for instance. Why the axes of sister chromatids become mosome structure and the timing of meiosis Does the accumulation of RMMAI and separated at the PAR, and whether this interact to ensure proper recombination. structural remodelling at mo-2 arrays promotes break formation and recom- actually cause an increased frequency of bination, have yet to be determined. As a Ericka Humphrey and Francesca Cole are in double-strand- breaks? The protein RPA2 is consequence of axis separation, the sister the Department of Epigenetics and Molecular concentrated at sites at which recombina- chromatids of spermatocyte sex chromo- Carcinogenesis, University of Texas MD tion is under way — Acquaviva et al. therefore somes are farther apart than are those of other Anderson Cancer Center, Smithville, Texas analysed these RPA2 foci as a proxy for dou- chromosomes. The authors suggest that axis 78957, USA. ble-strand breaks. RPA2 associated highly separation might suppress ineffectual inter- e-mail: [email protected] with mo-2 arrays. Indeed, when synapsis sister recombination in favour of homologous 1. Kauppi, L. et al. Genes Dev. 27, 873–886 (2013). was nearly complete, 70% of mo-2 sites had recombination between chromosomes. In 2. Kauppi, L. et al. Science 331, 916–920 (2011). associated RPA2 foci. Further supporting addition, the group posits that chromosome 3. Acquaviva, L. et al. Nature 582, 426–431 (2020). the idea, the group showed that the overlap restructuring is linked with the accumulation 4. Templado, C., Uroz, L. & Estop, A. Mol. Hum. Reprod. 19, 634–643 (2013). between RPA2 foci and mo-2 arrays was sig- of a cohesin protein that they see at the tip of 5. Zickler, D. & Kleckner, N. Annu. Rev. Genet. 33, 603–754 nificantly lower in mice lacking the RMMAI the PAR. Cohesin accumulation in this region (1999). 6. Boekhout, M. et al. Mol. Cell 74, 1053–1068 (2019). component ANKRD31, and previous work might increase cohesion between sister chro- 7. Papanikos, F. et al. Mol. Cell 74, 1069–1085 (2019). has shown that X and Y chromosomes do not matids, which in turn would help to stabilize 8. Baudat, F., Imai, Y. & de Massy, B. Nature Rev. Genet. 14, properly pair up in these animals6,7. the association between homologous chro- 794–806 (2013). 9. Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R. D. & RMMAI accumulation therefore seems to mosomes. An alternative model is that axis Petukhova, G. V. Nature 485, 642–645 (2012). be key for promoting double-strand breaks separation might provide more ‘real estate’ 10. Thacker, D., Mohibullah, N., Zhu, X. & Keeney, S. Nature and recombination at the PAR. By contrast, on which factors promoting double-strand 510, 241–246 (2014). a mechanism involving the protein PRDM9 breaks could assemble at the PAR because This article was published online on 27 May 2020. is known8,9 to control the location of most double-strand breaks outside the PAR. The Ancient DNA authors found that the frequency of breaks was higher than average at mo-2 arrays on non-sex chromosomes, and showed that these breaks form independently of PRDM9. Incest uncovered at elite Thus, mo-2 arrays define chromosomal regions in which PRDM9- independent mech- prehistoric Irish burial site anisms of break formation can occur, with RMMAI accumulation crucial to this process. Alison Sheridan Both double-strand breaks and synapsis occur later at mo-2 arrays than at other The huge, elaborate, 5,000-year-old tomb at Newgrange, chromosomal regions in spermatocytes. Ireland, is thought to have been built for a powerful elite. The double-strand-break machinery is DNA of a man buried there reveals a case of incest. Was this a suppressed once chromosomes have fully synapsed1,10. The authors therefore hypoth- strategy to maintain a dynastic bloodline? See p.384 esized that delayed synapsis might underlie the increased frequency of double-strand breaks at mo-2 arrays. To test this, they A study of the DNA of Ireland’s Stone Age famous Irish passage tomb is the enormous investigated chromosome structure and inhabitants has produced spectacular results, monument at Newgrange (Fig. 1), which is part break frequency in the meiotic precursors with far-reaching consequences for our under- of a World Heritage site of the United Nations of eggs, oocytes. The X chromosomes of standing of prehistoric population movement Educational, Scientific and Cultural Organ- oocytes do have mo-2-rich PAR regions in and the structure of that ancient society. On ization. This huge circular mound is one of which RMMAI accumulates, but they do not page 384, Cassidy et al.1 report their striking three major tombs built in the Brú na Bóinne rely on these regions for synapsis, because discoveries from this project. cemetery complex in County Meath, north of the two X chromosomes share homology The authors looked at the period, around Dublin, in eastern Ireland. along their whole lengths. X chromosomes 4000 bc, when farming appeared as a new, Newgrange was constructed between therefore synapse with the same efficiency Neolithic way of life, supplanting the older around 3200 and 3000 bc. It was built using as do non-sex chromosomes. and more mobile Mesolithic lifestyle based on sophisticated engineering to ensure that, at Consistent with their model, Acquaviva fishing, hunting and foraging for wild foods. the end of a long, stone-lined passage, a burial et al. showed that levels of double-strand Cassidy et al. examined the social structures chamber is lit up for a few minutes every year breaks are not as high in the PAR of oocytes as of these farming communities over the fol- by the rays of the rising Sun, on and around in that of spermatocytes. However, the group lowing 1,500 years, focusing on the people the shortest day of the year. The monument could trigger high-level break formation on buried in passage tombs — a type of monument pre-dates, by around 500 years, the huge mo-2 arrays by delaying synapsis. Normally, featuring a chamber, covered by a mound, trilithon stones at Stonehenge, which align oocytes progress more rapidly through early that is entered along a passage. The most to the winter and summer solstices. Marking

News & views KEN WILLIAMS/SHADOWSANDSTONE.COM KEN Figure 1 | Newgrange passage tomb, Ireland. Cassidy et al.1 report that the analysis of DNA from a man buried in this 5,000-year-old monument reveals evidence of incest. the winter solstice was crucial for early farmers’ relationship with the indigenous of remains from Poulnabrone portal tomb farmers, who needed to know when the days Irish Mesolithic fisher-hunter-foragers. The (a single-chamber monument with a huge cap- would start to get longer. It took a massive authors also checked whether any genetic links stone and tall entrance stones) in County Clare, effort to build Newgrange, and archaeologists could be detected among and between farmers western Ireland, reveals the appearance of new think it was constructed as a burial place for a buried according to particular traditions over genomic signatures. This indicates the arrival wealthy and powerful elite. People probably the course of the fourth millennium bc. In addi- in Ireland of people from elsewhere, from at journeyed there from far and wide to parti tion, Cassidy et al. obtained radiocarbon dates least as early as 3800 bc, and is consistent with cipate in major solstice-marking ceremonies. and stable-isotope data for 27 individuals, the idea that farming was brought to Ireland by Perhaps this elite claimed to have divine power revealing information about diet. immigrants8. These people were genetically by ‘controlling’ the Sun’s movement2. The genetic data obtained from human affiliated to the Neolithic population in Britain, Cassidy and colleagues’ analysis of remains dating to around 4700 bc (from and their roots lie in continental Europe. One ancient DNA from human remains reveals a Killuragh Cave, County Limerick, in south- way or another, these immigrants had a major rare and unexpected incidence of incest. A west Ireland) and to around 4100 bc (from effect on the small and insular indigenous man buried in the chamber of Newgrange Sramore Cave, County Leitrim, in the north- Mesolithic population, whose genetic signa- around 5,000 years ago was the offspring of west and Stoneyisland, County Galway, in the ture disappeared almost completely over the a first-degree incestuous union: his parents west) are the first DNA results for Ireland’s next few generations. However, DNA evidence were either siblings or parent and child. This hunter-fisher-forager groups. These Meso- from Parknabinnia court tomb (a monument finding led the team to speculate that the elite lithic Irish people were genetically distinct with a segmented chamber and a forecourt) in associated with this magnificent monument County Clare shows that indigenous and immi- practised incest as a way of maintaining a “A man buried in the grant intermixing did occur, possibly as late as dynastic bloodline. Such a strategy, which 3750–3500 bc, and therefore that the indig- breaks a near-universal social taboo against chamber of Newgrange enous population was clearly not wiped out. incest, was also practised much later by ruling around 5,000 years ago was The authors clarify Neolithic population elites in ancient Egypt, in the Inca empire and the offspring of a first-degree dynamics and familial linkages in Ireland in ancient Hawaii. incestuous union.” through the analysis of individuals from But this is only one of many revelations a variety of burial contexts spanning the from this groundbreaking report. Cassidy fourth millennium bc and extending into the et al. carried out whole-genome DNA analysis from their Mesolithic neighbours across the mid-third millennium bc. For those buried in of 2 Mesolithic and 42 Neolithic individuals, the Irish Sea in Britain, suggesting a prolonged Early Neolithic court and portal tombs, the latter from a variety of burial contexts includ- period of genetic isolation after these people team found an example of approximately ing caves, passage tombs and other types of sailed6 across to Ireland around 8000 bc. In fourth-degree relatives at Parknabinnia, and monument. By considering their data alongside other words, even though they might have kinship more distant than that between a DNA data previously obtained for 16 Neolithic ranged widely over Ireland when choosing man buried at this monument and two men (approximately 4000–2500 bc) and Early partners, members of these communities did buried at Poulnabrone portal tomb, 7 kilo- Bronze Age (2200–1500 bc) individuals from not sail back to Britain or across to the conti- metres away. An earlier study had identified Ireland3,4, and for other prehistoric individuals nent to interact with people there — contrary a Neolithic father–daughter pair at Primrose from Britain and continental Europe4,5, Cassidy to what some archaeologists have proposed7. Grange court tomb, County Sligo, in northwest and colleagues contextualized their results. Thus, there is no evidence to support some Ireland4. Otherwise, the picture is generally The authors’ findings address key archaeologists’ assertion7 that Mesolithic one of genetically unrelated groups using the issues, such as the insularity of Ireland’s groups were responsible for introducing the same burial monuments. This implies a fairly Mesolithic population, the immigra- Neolithic farming lifestyle to Ireland. sizeable community. tion of Neolithic farming groups and the Instead, Cassidy and colleagues’ analysis However, Cassidy et al. report that those

buried between around 3500 and 2500 bc ancient individuals, and the world's earliest signature. But many pieces of the genetic in passage tombs (and also at a different definitive evidence (dated to 3629–3371 bc) for jigsaw are still missing, and more analyses of but related type of monument at Millin Bay, a case of Down’s syndrome — in an infant boy, Neolithic French individuals will be needed to County Down, in the north) display familial buried at Poulnabrone portal tomb. However, settle the question of the origins of Ireland’s relationships that extend over considerable there are also contentious issues, not least the first farmers. Nevertheless, Cassidy et al. have geographical distances and span several gen- use of social-evolutionary terminology. For produced a fascinating and invaluable study erations. People buried in passage tombs also example, it is questionable to characterize the providing much food for thought and debate seem to be differentiated from those in other society of those responsible for building the about prehistoric Irish society. kinds of burial monument by having had a major Brú na Bóinne passage tombs as pos- particularly meat-rich diet. sessing attributes found in early state societies Alison Sheridan is a research associate and The authors found genetic links between and their precursors, with all that that implies emerita principal curator in the Department some individuals analysed from the major in terms of bureaucracy, centralized power of Scottish History and Archaeology, National passage-tomb complexes at Carrowmore and structures and so on. Museums Scotland, Edinburgh EH1 1JF, UK. Carrowkeel in County Sligo, and individuals Moreover, in emphasizing the genetic e-mail: [email protected] buried 150 kilometres away at Brú na Bóinne affinities between Irish and British Neo- (and also at the Millin Bay monument). The lithic farmers and those in Iberia (Spain and authors interpret these links as providing evi- Portugal), the authors seem to fall into the 1. Cassidy, L. M. et al. Nature 582, 384–388 (2020). 2. Sheridan, J. A. in Entre archéologie et écologie, une dence for a non-random selection of partners trap of assuming that Ireland’s farmers had préhistoire de tous les milieux. Mélanges offerts à Pierre over large territories, implying a high level of sailed up from Iberia — an argument for which Pétrequin (eds Arbogast, R.-M. & Greffier-Richard, A.) societal complexity. These genetic data sup- there is no archaeological evidence. Instead, 303–314 (Presses univ. Franche-Comté, 2014). 3. Cassidy, L. M. et al. Proc. Natl Acad. Sci. USA 113, 368–373 port the argument that the trajectory of Irish the archaeology points towards the Morbihan (2015). passage-tomb development over time — gen- area of Brittany in northwest France, and the 4. Sánchez-Quinto, F. et al. Proc. Natl Acad. Sci. USA 116, erally speaking, going from small and simple Nord-Pas de Calais region of northern France, 9469–9474 (2019). 5. Brace, S. et al. Nature Ecol. Evol. 3, 765–771 (2019). to larger and more ostentatious — reflects an as the ultimate areas of origin for Ireland’s 6. Woodman, P. Ireland’s First Settlers: Time and the 9 increasingly hierarchical society . The evi- immigrant farmers — with those from northern Mesolithic (Oxbow, 2015). dence of incest found at Newgrange, suggest- France probably arriving in Ireland via north- 7. Thomas, J. The Birth of Neolithic Britain: An Interpretive 8 10 Account (Oxford Univ. Press, 2013). ing dynastic behaviour, is consistent with this ern Britain . A recently published analysis of 8. Sheridan, J. A. in The Neolithic of Europe: Papers in overall picture. DNA samples from Neolithic French farmers Honour of Alasdair Whittle (eds Bickle, P., Cummings, V., Cassidy and colleagues’ report has many lends support to this scenario, revealing that Hofmann, D. & Pollard, J.) 298–313 (Oxbow, 2017). 9. Sheridan, J. A. J. Irish Archaeol. 3, 17–30 (1986). other fascinating insights, including data on some of these individuals shared elements 10. Rivollat, M. et al. Sci. Adv. 6, eaaz5344 https://doi. the probable skin, hair and eye colour of the of this ‘Iberian’ or ‘Mediterranean’ genetic org/10.1126/sciadv.aaz5344 (2020).

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