Decline of genetic diversity in ancient domestic stallions in Europe

Open access research article Decline of genetic diversity in ancient domestic stallions in Europe, by Wutke et al., Science (2018), 4(4):eaap9691.

Abstract (emphasis mine):

Present-day domestic horses are immensely diverse in their maternally inherited mitochondrial DNA, yet they show very little variation on their paternally inherited Y chromosome. Although it has recently been shown that Y chromosomal diversity in domestic horses was higher at least until the Iron Age, when and why this diversity disappeared remain controversial questions. We genotyped 16 recently discovered Y chromosomal single-nucleotide polymorphisms in 96 ancient Eurasian stallions spanning the early domestication stages (Copper and Bronze Age) to the Middle Ages. Using this Y chromosomal time series, which covers nearly the entire history of horse domestication, we reveal how Y chromosomal diversity changed over time. Our results also show that the lack of multiple stallion lineages in the extant domestic population is caused by neither a founder effect nor random demographic effects but instead is the result of artificial selection—initially during the Iron Age by nomadic people from the Eurasian steppes and later during the Roman period. Moreover, the modern domestic haplotype probably derived from another, already advantageous, haplotype, most likely after the beginning of the domestication. In line with recent findings indicating that the Przewalski and domestic horse lineages remained connected by gene flow after they diverged about 45,000 years ago, we present evidence for Y chromosomal introgression of Przewalski horses into the gene pool of European domestic horses at least until medieval times.

horses-y-chromosome-evolution
The frequencies of Y chromosome haplotypes started to change during the Late Bronze Age (1600–900 BCE).
Inferred temporal trajectories of haplotype frequencies. Each haplotype is displayed by a different color. The shaded area represents the 95% highest-density region. The trajectories were constructed taking the median values across frequencies from the simulations of the Bayesian posterior sample. The small chart represents the stacked frequencies; the amplitude of each colored area is proportional to the median haplotype frequencies (normalized) at a given time. The x and y axes of the small chart match those in the large one. Ka, thousands of years.

Interesting excerpts:

The first record of the modern domestic Y chromosome haplotype stems from two Bronze Age samples of similar age. Notably, both samples were found in two distantly located regions: present-day Slovakia (2000–1600 BCE, dated by archaeological context) and western Siberia (14C-dated: 1609–1436 cal. BCE). Although a very recent study proposes an oriental origin of this haplotype (14), we cannot determine the geographical origin of Y-HT-1 with certainty, because this haplotype has not been found thus far in predomestic or wild stallions. There are two possible scenarios: (i) Y-HT-1 emerged within the domestic population by mutation and (ii) Y-HT-1 was already present in wild horses and entered the domestic population either at the beginning of domestication (but initially restricted to Asian horses) or later by introgression (from wild Y-HT-1 carrying studs during the Iron Age). Crosses between domestic animals and their wild counterparts have been observed in several domestic species (15–18); thus, the simplest explanation would be that we missed Y-HT-1 in older samples because of limited geographical sampling. However, the estimated haplotype age is contemporary (Fig. 4) with the assumed starting point of horse domestication ~4000–3500 BCE (19), rendering it likely that Y-HT-1 originated within the domestic horse gene pool. Still, we cannot rule out definitively that it appeared before domestication.

Independent of its geographical origin, Y-HT-1 progressively replaced all other haplotypes—except for one additional lineage that is restricted to Yakutian horses (11). Considering our data, this trend in paternal diversity toward dominance of the modern lineage appears to start in the Bronze Age and becomes even more pronounced during the Iron Age. The Bronze Age was a time of large-scale human migrations across Eurasia (20–22), movements that were undoubtedly facilitated by the spread of horses as a means of transport and warfare. At that time, the western Eurasian steppes were inhabited by highly mobile cultures that largely relied on horses (20, 21, 23, 24). The genetic admixture of northern and central European humans with Caucasians/eastern Europeans did correlate with the spread of the Yamnaya culture from the Pontic-Caspian steppe (25), an area that has repeatedly been suggested as the center of horse domestication (19, 26, 27). Given the importance of domestic horses, it appears that deliberate selection/rejection of certain stallions by these people might have contributed to the loss of paternal diversity. The spread of humans out of this region might also have resulted in the spread of Y-HT-1 from Asia to Europe. This scenario also agrees with recent findings that the low male diversity of extant horses is not caused by recruiting only a limited number of stallions during early domestication (13).

horses-y-chromosome-map
Decline of paternal diversity began in Asia.
Maps displaying age, locality, and haplotype (different colors) of each successfully genotyped sample.

The presence of the Y chromosome haplotype carried by present-day Przewalski horses (Y-HT-2) in early domestic stallions and a European wild horse (Pie05; table S2) could be the result of introgression of Przewalski stallions. Although the original distribution of the Przewalski horse is unknown, it was probably much larger than that of the relict population in Mongolia that produced modern Przewalski horses and might even have extended into Central Europe. However, it is also possible that either Przewalski horses were among the initially domesticated horses or that Y-HT-2 occurred both in Przewalski horses and in those wild horses that are the ancestors of domestic horses, based on autosomal DNA data (30). Regardless of how Y-HT-2 entered the domestic gene pool, it was eventually lost, as were all haplotypes except Y-HT-1. In our sample set, Y-HT-2 was undetectable as early as the third time bin. However, it is possible that Y-HT-2 may have been present during this time period, but with a frequency below 0.11 (with 95% probability). The inferred time trajectories for Y-HT-2 frequencies suggest that it could nevertheless have persisted at very low frequencies until the Middle Ages (Fig. 3). On the basis of these simulations, this finding could be interpreted as a relic of this haplotype’s formerly higher frequency in the domestic horse gene pool. It is also possible that the presence of this haplotype could be the result of mating a wild stallion with a domestic mare, a frequently reported breeding practice when wild horses were still widely distributed. However, a significant contribution of the Przewalski horse to the gene pool of modern domestic horses has been almost ruled out by recent genomic studies (13, 31, 32).

horses-y-chromosome-selection
Stallion lineages through time.
Temporal haplotype network of the four detected Y chromosome haplotypes. Age of the samples indicated by multiple layers separated by color; vertical lines connecting the haplotypes of consecutive layers/ages represent which haplotype was transferred into a later/younger period. Numbers constitute the respective number of individuals showing this particular haplotype for that period. Prz, Przewalski; Dom, domestic.

Related:

The origins of the Tumulus culture: Proto-Lusatian and potential Proto-Balto-Slavic origins

Interesting chapter The birth of a new world. Barrows, warriors, and metallurgists, by Przemyslaw Makarowicz. In: Urbańczyk P. (Ed.) THE PAST SOCIETIES. Polish lands from the first evidence of human presence to the Early Middle Ages, Warszawa 2017, vol. 3, U. Bugaj (Ed.) (2000 – 500 BC), Warszawa, pp. 127-186.

Some interesting excerpts from the introduction (emphasis mine):

In the 17th century BC the northern reaches of the Únětice culture oecumene experienced a structural crisis and a settlement hiatus; no such interruption in development occurred in the southern or western regions, or further west in the circle of the Blechkreiskulturen (Innerhofer 2000; Müller 2012, 257f.). In light of the most recent research, the decline of Únětice structures in the north was associated with a growing social and ecological crisis that resulted e.g., in the well-documented regression in the development of the fortified settlement in Bruszczewo in Greater Poland/Wielkopolska, which occurred ca. 1650/1600 BC (Kneisel 2012; Kneisel 2013, 101f.; Müller 2012). The settlement structure in that region only stabilized after several decades, with the emergence of Tumulus culture (Schurbein 2009; Cwaliński 2012, 16). In some parts of Central Europe (e.g., Bohemia, Bavaria, Hesse, Thuringia) a relatively gradual and smooth transition in the form of bronze items and pottery was observed between the periods of BA2 and BB1, diagnostic for the Early and Middle Bronze Age respectively (Rittershofer 1984; Innerhofer 2000). The term ‘pre-Tumulus’ horizon (BA3) was introduced to denote the stage that followed the disappearance of Early Bronze Age cultural structures and preceded the formation of Tumulus culture at the foothills of the Alps (Innerhofer 2000, 241f.)

The processes behind the development of this new cultural phenomenon may become clearer if one considers the origins of the new ideology of warriorhood apparent in the most progressive formations of the late stages of the early Bronze Age in the Carpathian Basin (Vandkilde 2007, 129; 2014; the beginnings of the Middle Bronze Age in Hungarian chronology; Hänsel 1968; Bóna 1992; Harding 2000, Fig. 1.3).This factor is particularly relevant in the case of the centralized communities of the Otomani-Füzesabony culture. Its members built impressive fortified settlements, knew advanced methods of bronze casting, and maintained a vast network of contacts that connected the north of Europe with the eastern reaches of the Mediterranean world (e.g., Bouzek 1985; Furmánek, Veliačik, Vladár 1991; Kristiansen, Larrson 2005; David 2007)
(…)
The composition of some spectacular hoards and the presence of military items in some of the graves associated with such communities may suggest that a new type of individualized elite (military aristocracy) emerged in this very culture (Kristiansen 1998, 376f.; 1999; Kristiansen, Larrson 2005). The attractive ideology would then have spread to the west and north-west and be adapted by the ‘post-Early-Bronze’, de-centralized and mobile communities (most likely based on kinship) of animal farmers inhabiting the upper Danube basin and the upper Rhine basin, as well as by the peoples of the Nordic regions (Vandkilde 2014, Fig. 5). This process went hand in hand with the dissemination of the custom of tumulus-building and the associated religious concepts, funerary practices, and territorial behaviour. The mechanism behind the adoption of this custom remains unknown. It may have been the result of imitating the barrows of Corded Ware culture, already present in the landscape of Central Europe – a similar process took place in the communities of the Trzciniec circle (Makarowicz 2009; 2010; 2011). It is also possible that the tumuli were based on the few existing Únětice barrows, though in this case the similarities are more apparent in the stone elements beneath the barrows’ mound. In both cases there was no direct contact between the earlier cultural formation and the emerging group.

proto-lusatian-tumulus
Spatial range of the Silesian-Greater Polish Tumulus Culture (‘Vorlauzitzer Kultur’) after M. Gedl 1992, amended

The new lifestyle became a pan-European phenomenon, but involved a considerable degree of regional diversity that stemmed primarily from contact with local tradition (Bóna 1975; Gedl 1989; Jockenhövel, Kubach [eds.] 1994; David 2002; Jockenhövel 2013). But how did this model spread? It appears that analogies for this development may be found in the social processes and interactions that took place at the beginning of the 3rd millennium BC and led to the emergence of the Bell Beaker phenomenon (Burgess 1986; Nicolis 2001 [ed.]; Czebreszuk 2001; 2004 [ed.]; Heyd 2013; Van der Linden 2013, further literature therein). The most important elements of the ‘Tumulus set of cultural patterns’ included: warriorhood (conveyed through the presence of individual weaponry as grave goods), characteristic types of territorial behaviour (methods of familiarizing space that largely relied on constructing tumuli – monumental graves with a unique external form and internal architecture that was singular, spectacular, and immensely symbolic), and a specific array of valuables made of bronze or, less frequently, of amber or glass (such items indicated the status, gender, and sometimes also the social role of the deceased with whom they were buried). Local cultural milieux transmitted and adapted a set of ideological, social, and political principles that gave the emerging formation coherence and a new ‘quality’. The symbolism of the stone barrow construction (rings, kerbs, cores, rays, etc.), the high value of bronze and amber, and the emergence of the custom of cremation suggests that ‘Tumulus’ communities had a large part to play in the dissemination of the solar cult during the Middle Bronze Age (cf. Kristiansen, Larsson 2005; Czebreszuk 2011, 164-171).

The decline of the Central European early Bronze Age civilization and the birth of a new, pan-European formation was a complex process that lasted at least several decades. It may be surmised that the downfall of Únětice structures and the Otomani-Füzesabony-Gyulavarsánd complex in the Carpathian Basin was brought about primarily by internal structural crises, yet the reasons for the emergence of Tumulus culture lay in the attractive, almost ‘Dionysian’ ideology of warriorhood. Its solidification coincided with the decline of the ‘old’ Early Bronze Age elites that ruled over centralized structures that were territorial in character (fortified settlements with proto-urban characteristics) and were buried in magnificent, richly furnished graves covered with mounds (Fürstengräber). It was also concurrent with the emergence of active kinship-based and de-centralized groups led by the ‘new’ elite class of warriors (the beginnings of military aristocracy?). The significance of such groups continued to grow during the pivotal period – and the decline of the Únětice world and the final turbulent phase of the development of centres in the Carpathian Basin may well be thus described. The process was facilitated by the escalation of military conflicts that occurred in the Bronze Age (Harding 1999; 2007; Kristiansen 1999; Osgood, Monks, with Thoms 2000; Kristiansen, Larsson 2005; Hårde 2006; Vandkilde 2011; 2014). War became an inherent part of social life, as indicated by the increasing presence of weaponry in male graves, rock carvings and steles depicting warriors and their equipment, as well as arrowheads and spearheads embedded in the bones (soft tissues) of the deceased, and plentiful evidence of injuries caused by melee weapons (e.g., Osgood 2006). New types of weaponry (swords, spears) started to be used in the first half of the 2nd millennium BC, leading to more efficient methods of combat (e.g., Harding 2006; Thrane 2006). This must have resulted in the emergence of new types of units, combat styles, and military strategies. It may also be surmised that ‘Tumulus’ communities adopted a hitherto unknown, institutionalized model of warriorhood based on groups of men who dealt with warfare professionally (cf. Sarauw 2007, 66).

The origin of the Tumulus culture meant therefore a pan-European ideological socio-political and ideological change, that may be associated with the last true North-West Indo-European dialect continuum in Europe, as evidenced in Archaeology by long-distance cultural contacts, in Linguistics potentially by late layers of shared vocabulary, and in Ancient Genomics by the different origins of combatants studied from the the Tollense valley.

proto-lusatian-settlements
Settlement points of the Silesian-Greater Polish Tumulus Culture in the Prosna-Odra interfluve (‘close zone’) superimposed on a hypsometric map. By Jakub Niebieszczański

The origins of Tumulus culture in what is now Polish territory most likely resulted from a combination of different factors. In the hitherto prevailing narrative its arrival in the Odra-middle Vistula interfluve was associated with an invasion (aggressive migration) of the Tumulus peoples from enclaves in the middle Danube basin, the destruction of Únětice centres and the Nowa Cerekwia Group, and the subsequent conquest of the western territories inhabited by members of the Trzciniec culture (Gedl 1975, 81; 1989; 1992; Gediga 1978). There is, however, much evidence to suggest that the provenance of this cultural group is more complex.

Recent archaeological research and environmental analyses indicate that the decline of the Únětice culture in the northern reaches of its scope (e.g., the economic and settlement crisis of the Kościan agglomeration with its centre in Bruszczewo and the princely barrow graves in Łęki Małe) was mainly the result of excessive human activity and overly intense exploitation of natural resources (Kneisel 2012; 2013; Müller 2012). Palynological data from the period of1700-1500 BC collected in this part of the North European Plain indicates a decline of human activity. It coincides with the devolution of settlement centres (hamlets and necropolises) dated to the end of the Early Bronze Age and the beginning of the Middle Bronze Age (depopulation?). The decline of Early Bronze Age settlements occurred between 1700 and 1600 BC, whereas the beginning of the Silesian-Greater Polish Tumulus culture may be dated to 1600-1500 BC. A renewed increase in human activity, indicated e.g., by the ‘opening’ of the landscape, did not occur until ca. 1500-1400 BC, in the classic period of the development of ‘Tumulus’ cultural structures (Kneisel 2012, 221).

The whole paper is interesting from the point of view of the potential formation of a Proto-Balto-Slavic community in the Proto-Lusatian or Silesian-Greater Polish Tumulus culture, before its expansion to the east.

After O&M 2018, the only plausible alternative to this model of Balto-Slavic homeland is that Proto-Lusatian represents a Temematic community instead, and an Indo-Slavonic community formed in East Yamna, whereby Balto-Slavic would have possibly expanded with Srubna, and only much later over Temematic territory, absorbing its language as a North-West Indo-European substratum.

See also:

Iberia in the Copper and Early Bronze Age: Cultural, demographic, and environmental analysis

bell-beaker-ritual

New paper (behind paywall), Cultural, Demographic and Environmental Dynamics of the Copper and Early Bronze Age in Iberia (3300–1500 BC): Towards an Interregional Multiproxy Comparison at the Time of the 4.2 ky BP Event, Blanco-González, Lillios, López-Sáez, et al. J World Prehist (2018).

Abstract (emphasis mine):

This paper presents the first comprehensive pan-Iberian overview of one of the major episodes of cultural change in later prehistoric Iberia, the Copper to Bronze Age transition (c. 2400–1900 BC), and assesses its relationship to the 4.2 ky BP climatic event. It synthesizes available cultural, demographic and palaeoenvironmental evidence by region between 3300 and 1500 BC. Important variation can be discerned through this comparison. The demographic signatures of some regions, such as the Meseta and the southwest, diminished in the Early Bronze Age, while other regions, such as the southeast, display clear growth in human activities; the Atlantic areas in northern Iberia barely experienced any changes. This paper opens the door to climatic fluctuations and inter-regional demic movements within the Peninsula as plausible contributing drivers of particular historical dynamics.

iberia-culture-history-areas
Division of Iberia into 5 study areas according to their culture history (3300–1550 BC)

Interesting excerpts summarizing key trends in the different regions:

  • Between 2200 and 1900 BC, the northernmost regions (i.e. Galicia, the Cantabrian strip and the northeastern sector to the north of the Ebro valley) underwent relatively minor changes in the realms of settlement and burial practices. (…) In addition, some Atlantic areas show a marked and statistically significant fall in human activity c. 2200 BC, with a subsequent recovery c. 1600 BC, and such observations are matched by paleoenvironmental proxies and a lack of known EBA sites
  • The overall impression from the Meseta is one of sharp disruption in cultural practices; these include both settlement and burial patterns, abrupt shifts in local climate conditions, and striking differences in human pressure on vegetation. However, there was also clear intra-regional variability, with remarkable internal particularities and differential tempos between the western and eastern sectors. In terms of material culture, discontinuity with the Copper Age is the main trend in the western Duero and the Tagus valleys, yet EBA communities to the north of the Central System adopted far more distinctive and therefore traceable site types (hilltops) and material repertoire. This shift was even stronger in the case of the Motillas culture at La Mancha, whose pathway seems closely tied to the Argaric area.
  • Intra-regional variability is also apparent within the northeast (…) In the second millennium BC, material culture changed, long-distance exchange intensified and anthropogenic pressure increased, despite continuity in diverse realms of social practice.
  • The pattern in the southwest was one of marked discontinuity with two key features: a) it follows the general decreasing trends manifest across Atlantic Iberia; and b) its temporality was clearly different from the rest of the Peninsula and apparently unrelated to the 4.2 ky BP event. Thus, a highly conspicuous and rich variety of cultural expressions in the Chalcolithic, with an early and marked peak in human activity during the Beaker phase c. 2500 BC, gave way to a sudden cultural collapse prior to the onset of the EBA
  • The southeast exhibits one of the most remarkable cultural shifts in Western Europe. (…) The radical transformation in Chalcolithic materiality and ways of life could be regarded as a kind of societal collapse. The Argaric, a highly hierarchical and integrated regional polity, is the clearest example of a new scenario that emerged after the 4.2 ky BP event, yet the contributing role of environmental change and immigration from other regions remains to be fully explored.

Since R1b-DF27 lineages are widely distributed in modern western Europe, it is only logical that the recent find of its first ancient sample in Iberia has sparked the interest for Chalcolithic and Early Bronze Age Iberian cultures.

There is not much literature in English about Iberian prehistory, especially on the evolution of Bell Beaker culture. Also, most papers in Spanish on this cultural phenomenon – in my humble opinion, as a non-archaeologist – seem to be written from a merely descriptive archaeological point of view, many of them still sharing the radiocarbon-based assessment of origin and distribution of materials, instead of more complex anthropological models of cultural change and potential migrations.

Nevertheless, changes and influences in Iberian cultures are obvious regardless of the view taken on population movements (which are becoming quite clear now), and this paper seems to me a thorough review, very interesting for international researchers when interpreting ancient DNA from Iberia.

Featured image, modified from the paper: “The Bell Beaker culture in the northern Meseta: an artistic recreation of funerary ritual at Fuente Olmedo (Valladolid). Source: Garrido-Pena et al. 2011, Fig. 7.7”.

EDIT (21 MAR 2018): Interesting C14 date repository project Cronología de la Prehistoria de la Península Ibérica (read a brief description, in Spanish).

Related:

Holocene rise in mobility in at least three stages: Strong link between technological change and human mobility in Western Eurasia

estimating-mobility

New interesting article at PNAS: Estimating mobility using sparse data: Application to human genetic variation, by Loog et al (2017).

Download links and supplemental information.

Significance

Migratory activity is a critical factor in shaping processes of biological and cultural change through time. We introduce a method to estimate changes in underlying migratory activity that can be applied to genetic, morphological, or cultural data and is well-suited to samples that are sparsely distributed in space and through time. By applying this method to ancient genome data, we infer a number of changes in human mobility in Western Eurasia, including higher mobility in pre- than post-Last Glacial Maximum hunter–gatherers, and oscillations in Holocene mobility with peaks centering on the Neolithic transition and the beginnings of the Bronze Age and the Late Iron Age.

Abstract

Mobility is one of the most important processes shaping spatiotemporal patterns of variation in genetic, morphological, and cultural traits. However, current approaches for inferring past migration episodes in the fields of archaeology and population genetics lack either temporal resolution or formal quantification of the underlying mobility, are poorly suited to spatially and temporally sparsely sampled data, and permit only limited systematic comparison between different time periods or geographic regions. Here we present an estimator of past mobility that addresses these issues by explicitly linking trait differentiation in space and time. We demonstrate the efficacy of this estimator using spatiotemporally explicit simulations and apply it to a large set of ancient genomic data from Western Eurasia. We identify a sequence of changes in human mobility from the Late Pleistocene to the Iron Age. We find that mobility among European Holocene farmers was significantly higher than among European hunter–gatherers both pre- and postdating the Last Glacial Maximum. We also infer that this Holocene rise in mobility occurred in at least three distinct stages: the first centering on the well-known population expansion at the beginning of the Neolithic, and the second and third centering on the beginning of the Bronze Age and the late Iron Age, respectively. These findings suggest a strong link between technological change and human mobility in Holocene Western Eurasia and demonstrate the utility of this framework for exploring changes in mobility through space and time.

Featured image, from the article: Estimation of mobility through time from empirical data. (A) Relative mobility rate estimates in Western Eurasia over the last 14,000 y, using a 4,000-y sliding window (121 windows). The solid black line represents the mean α value from 10,000 date resampled iterations; the colored area represents the 95% confidence intervals of the jackknife distribution.