The Roots and Routes of Dromedary Domestication

COMMENTARY

Back to the roots and routes of

Ludovic Orlandoa,1

Unlike most other domestic animals, where the genetic diversity present in modern livestock has been Caffa

scrutinized with the objective to map domestication Istanbul Baku centers (1) and identify signatures of human-driven Athens Algiers selection (2), dromedaries have received much less Damascus Babylon Petra attention at the genetic level. In PNAS, Almathen Cairo et al. (3) now rectify this anomaly by performing what Medina is, to my knowledge, the first large-scale genetic anal- Mecca ysis of the domestic dromedary. Compared with dogs, which were already domesticated at least ∼14,000 y ago (ya) [earlier dates are still debated (4)], pigs (∼9,000 ya), ruminants (cattle Dromedary species range ∼ ∼ ∼ Incense land routes 9,000 ya, sheep 10,500 ya, and goats 10,000 ya) Ottoman Empire at its greatest (5), or even other herbivores capable of sustaining Fossils with dromedary ancient DNA long distance travels, such as the horse [∼5,500 ya (6)] and the donkey [∼5,000 ya (7)], the domestication Fig. 1. Dromedary current range. Past Incense land routes, the extent of the Ottoman Empire at its greatest extent, and the location of archeological sites that delivered of the dromedary took place rather late in human his- dromedary ancient mtDNA are indicated. tory, most likely at the transition between the second and first millennia before the Common Era (B.C.E.) (8). Archaeologists can indeed trace the emergence of Levant, effectively connecting the cultures and civili- key domestication markers around that time (9), in- zations of antiquity from the seventh century B.C.E. cluding a significant reduction in the size of bone re- to the second century Common Era (C.E.). Although mains, an increasing association with human settlement, much less transformative than horses in the history of and unambiguous artistic representations. Despite its warfare (11), the remarkable speed and endurance of late advent, the domestication of the dromedary, also dromedaries were key to the military success of, for known as the one-humped camel (Camelus dromader- example, the Achaemenind King Cyrus II of Persia ius), has represented a historical turning point for human (sixth century B.C.E.), especially to provision armies populations in the Arabian Peninsula, the Levant, north- and facilitate hasty movements. Dromedary races, ern Africa, and beyond. which are known from antiquity, are still extremely Dromedaries indeed show unique phenotypic ad- popular in Saudi Arabia and can award prizes up to aptations to extremely hot and arid environments. They 1milliondollars. can endure 30% water loss and can survive almost Today, dromedaries live essentially in the desert 1 week without drinking (10). Their hump can store zones from North Africa, in the horn of Africa, ∼35 kg of fat, helping withstand extremely limited throughout the Arabian Peninsula and the Levant environmental resources. They thus represent ideal (Fig. 1), but also in Australia, where a feral population cargo vessels for long journeys through the desert developed following their introduction in the 19th and have been essential to the development of over- century C.E. Wild dromedaries are only known in the land trade throughout the Arabian Peninsula, the Le- fossil record until ∼2,000 ya. They thus cohabited with vant, and even the Sahara. The Incense trade route domesticates only for slightly over one millennium, at (Fig. 1) is one such example, where large caravans of a time when their range was probably limited to dromedaries carried myrrh and frankincense from coastal mangrove habitats in the Arabian Peninsula, South Arabia, spices from India, and other luxury where their salt physiological requirements could goods throughout the Arabian Peninsula and the be sustained.

aCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen 1350K, Denmark Author contributions: L.O. wrote the paper. The author declares no conflict of interest. See companion article 10.1073/pnas.1519508113. 1Email: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1606340113 PNAS Early Edition | 1of3 Downloaded by guest on October 1, 2021 Almathen et al. (3) undertook to decipher the domestication coestimate the mtDNA clock and past demographic profiles (17), history of dromedaries using spatial patterns of genetic diversity the authors could detect a massive demographic expansion some (Fig. 1). Because reference genomes for dromedaries were made 600 ya. This date is consistent with the rise of the Ottoman Em- available only recently (12, 13), the authors opted for classical pire, and the increasing use of dromedaries over long-distances in tools in population genetics, surveying a total of 1,083 animals an empire that extended up to the coastal regions of North Africa for 17 nuclear microsatellites and mitochondrial markers (repre- and Arabia (Fig. 1). Because the range for the clock estimates was senting 867 bp). The mitochondrial DNA (mtDNA) data showed rather broad and fast compared with standard mtDNA mutation no phylogeographic pattern, because the two major haplogroups rates in mammals, this date is only tentative and future estimates

identified (HA and HB) were found throughout their whole distri- based on additional data might confirm this or earlier events, such bution range. Similarly, no geographic region stood out in terms as the Arab expansion from the eighth century C.E. or earlier of microsatellite heterozygosity levels and allelic richness, two camel-borne trade routes (Fig. 1), as the drivers of this expansion. measures of population genetic diversity. Therefore, it appears impossible to track, genetically, from modern individuals the geo- Almathen et al. undertook to decipher the graphic location of the dromedary domestication center, which, as a domestication source, should harbor the largest levels of ge- domestication history of dromedaries using netic diversity. This finding contrasts with previous work in cattle, spatial patterns of genetic diversity. where declines of genetic diversity were found from the Middle East, where aurochs was first domesticated, to Europe (14). This There are lots of additional interesting observations in the work result rather points to a much more dynamic population history, of Almathen et al. (3). For instance, their microsatellite data sug- where the movements of dromedaries along cross-continental gested the existence of demographic collapses before domesti- trading routes could have eroded preexisting phylogeographic cation, some ∼5,000–8,000 ya. They also revealed the presence patterns resulting from their initial domestication. Alternatively, of two major ancestry components within modern dromedaries. it is possible that no such population structure ever existed in Both are represented throughout their entire distribution range, the wild, due to the strong dispersal capacities of the animal. but the first is maximized in East Africa, whereas the second is In the absence of a living wild population, the authors tested most common to all other regions. This distribution suggests that these scenarios by generating ancient DNA sequence data from the ecogeographic barriers from East Africa and/or the cultural archaeological remains, succeeding, in a technical tour-de-force, differences (dromedaries there are predominantly used for their to sequence 531 bp of mtDNA in 15 ancient remains, despite the milk instead of riding and transportation) have limited the extent extremely fast rates of DNA decay in warm environments (15). The of the homogenizing process in this region. In addition, despite oldest remain was ∼7,000 y old and was excavated in the United clearly belonging to a common population extending from North Arab Emirates (UAE), a country where summer temperatures can Africa to Southwest Asia, populations from isolated montane regions reach 45 °C. This success is extremely encouraging for ancient in the south of the Arabian Peninsula showed slight genetic distinc- DNA research because it demonstrates that traces of DNA can tions. Here, the geographic accessibility of the regions thus seems to be exploited even after several millennia of decay in extremely have also somewhat limited the extent of the homogenizing force. hot environments. This report is all the more encouraging because Surprisingly, the populations from South Arabia show minimal ge- none of the most sensitive laboratory methods available now, netic distance to those populations from East Africa, and not North which are based on target enrichment and high-throughput Arabia. It likely suggests an early introduction from South Arabia into DNA sequencing (16), were used. It suggests that additional East Africa by boats, through the Red Sea. When this took place is genetic information can likely be retrieved in the rich archaeolog- presently unknown, but could probably be inferred in the future using ical collections from such regions (e.g., Anatolia), where the ear- methods in statistical genomics exploiting genome-wide information liest civilizations rose following the domestication of animal and (e.g., the over the 1 million SNPs identified while generating the two plant species. dromedary reference genomes) (12, 13). Of the 15 ancient remains for which mtDNA was retrieved, For now, the authors implemented such analyses on their seven were ancient domestic individuals (three early Byzantine microsatellite data to test different domestication scenarios, specimens from Syria and Turkey, three Mamluk and Ottoman involving one or multiple domestication sources, in contact or specimens from Jordan, and one specimen from the Ottoman– in isolation with wild populations. Coalescent simulations Hapsburg wars). The haplotypes detected are still segregating followed by approximate Bayesian computation strongly sup- in modern populations. The remaining eight ancient specimens ported a population history where dromedaries were first were wild individuals and spanned the 5,000–500 B.C.E. tempo- domesticated from a small founder group, and later further

ral range. Although three of these individuals showed typical HB restocked from the wild. This result echoes similar reports in haplotypes, three novel additional haplotypes were found, in other domestic animals, such as horses (18, 19), pigs (20), and line with the domestication process capturing only part of the cattle (21), suggesting that in animals, domestic phenotypes diversity preexisting in the wild. Being limited to the UAE region, rarely evolved in pure isolation but can be maintained despite the ancient DNA data recovered from wild individuals is unfor- introgression from the wild. Whether the maintenance of the tunately inconclusive regarding the presence or absence of structure domesticphenotypewasdueinthecaseofthedromedaryto in the populations from the Arabian Peninsula before domestication. the limited temporal overlap of wild and domestic animals or to However, because the age of the ancient mtDNA sequences the presence of genomic islands of domestication, resisting could be deduced from their archaeological context, the authors such gene flow as proposed earlier for pigs (20), remains un- could calibrate the mtDNA clock to date important population known. Testing the latter will require genome sequences and/or changes. This approach exploits a well-known advantage of genome-wide information from modern domesticates as well as, ancient DNA data and temporal series in general. Using a most importantly from ancient wild dromedaries. Collecting such in- statistical package that leverages on time-structured datasets to formation might prove difficult, given the poor DNA preservation

2of3 | www.pnas.org/cgi/doi/10.1073/pnas.1606340113 Orlando Downloaded by guest on October 1, 2021 conditions in Arabia. However, the authors’ success at characterizing there might be hope. Such data, together with the data from early mtDNA fragments from wild specimens and the recent se- domesticates, could also help identify the early genetic targets of quencing of megabases of nuclear sequence information from selection and whether genomic blocks introgressed from the wild ∼400,000-y-old remains from archaic hominins (22) suggest that underpinned important adaptive features for life in hot deserts.

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