Chicken origins: closing in with new genomic evidence

wild Gallus gallus spadiceus

The past week saw the publication of a landmark genomic study on chickens (Wang et al 2020, Cell Research), which clarifies much about origins, and focuses some questions for further research. For a news summary see Lawler's Science piece.

It is transformative because it includes a substantial sample of genomes from across all of the wild subspecies of Red Jungle Fowl (142 wild red jungle fowls) and other wild Gallus species. The first thing to note is that is does support the reality of these different wild taxa. They aren’t merely geographical feral populations derived from escaped chickens, but they are differentiated from each other, making it reasonable to ask which population(s) are ancestral to domesticated chickens. In addition there has, of course, been gene flow via introgressions with domesticated chickens, but this has been on a more limited scale. So the answer to big question (of origins) appears to be Gallus gallus spadiceus. G. g. spadiceus is geographically focused on Burma, Yunnan, Guangxi, northern Thailand and bits of Laos. This struck me as the most surprising—this geographical derivation. If one favours a Chinese origins then you would look to G. g. jaboulliei (of the Guangdong and Fujian and perhaps further north in the past); if one favours an Indus domestication then one looks to G. g. murghii. Previously I have accepted the likelihood of an Indus Chicken domestication and a spread through India in post-Harappan times (e.g. Fuller 2006). This now appears unlikely. Instead it probably means that wild jungle fowls attracted attention in the Harappan period as pretty birds that were captured sometimes, traded, etc.,but not really domesticated subsistence species. Presumably the first Bronze Age Mesopotamian and Ramesside Egyptian “chickens” were actually pet wild jungle fowl-- fancy exotic birds-- and not connected to chickens as we understand them now. The "multi-colored birds of Meluhha" that were imported to Mesopotamia at the end of the Third Millennium BC from the Indus region, are plausible painted ivory statuettes of murghii jungle fowl (see, e.g. During-Caspers 1990).

These new genetic data also make it clear that as chickens spread out of their northern SE Asian homeland they did pickup some genetic material through introgression with local wild jungle fowl (such as G. g. murghii in northern India) and even grey jungle fowl in South India (the source of yellow legs: G. sonneratii). This process can be called “introgressive capture” and it is widespread in most livestock and many crops. This process has sometimes confused genetic studies into inferring multiple domestications, but with more genomic data it can now be disentangled (see Larson and Fuller 2014). 

It is also quite exciting that they have some genetic loci that might be under positive selection as part of the domestication process. One of the real mysteries with animal domestication is what constitutes domestication in a genetic sense in terms of adaptations. In plant it is well known that certain genes for seed dispersal, growth habit, dormancy, grain size, etc. were selected. We can find this evidence genetically and tie it to morphological changes in the archaeobotanical record. There is so far nothing equivalent in animals that links genetic loci to the morphological adaptations we see with animal domestication. So on a more theoretical level this may be the first step to actually starting to unravel the genetics of animal domestication.

These raises fascinating questions then about the contexts in which G. g spadiceus was domesticated—what kinds of human societies and agricultural economies did it interact with in its wild form and how did it get incorporated into ecology of human settlements. Equally at what period and in what contexts did these early chickens then spread. Their phylogenetic results suggest the first wave of chickens spread through SE Asia and SW China only.  Sadly we know little about the Neolithic in Myanmar, or Guangxi or Southern Yunnan; we do have some data from northern Yunnan where Chinese millet and rice agriculture (with pigs) arrives from the North around 2600 BC. One presumes there was some further Southern diffusion towards the China/Burma borderlands. And perhaps it was in these borderland zones where early sedentary rice/millet farmers began to isolate some G. g. spadiceus populations that came feed within the human settlement niche. As hypothesized in Larson and Fuller (2014), chickens likely followed a commensal pathway to domestication. But we now need to refine the map (right). And work out when this happened.

There estimate of the age of the last common ancestor of domesticated chickens and G. g. spadiceus 9500 BP (+/- 3000). But I would regard domestication any time between 10000 BC and 4500 BC as highly unlikely. As the authors themselves not in the first paragraph of their discussion such genetic estimates of domestication age tend to be over estimates (by upto 15,000 years!), so these are not exactly reliable.  In fact I would regard the tendency genetic coallesence ages as to tell us anyting about the timing of domestication to be a highly  misleading tradition that is entrenched in genetics but has little to back it up. Take the example of rice (Oryza sativa), where the genetic estimate of last common ancestor of cultivated rice and modern wild population is ca. 18,000 (Choi et al 2017). But archaeologically even the more generous estimates are ~10,000 (and more like 7,000-6500 by more cautious approaches). I suspect a more general problem is that what is being picked up the last major cladogenetic event that structured wild populations and not domestication itself. Often this can be expected to be something climatic, so 9500 BP is telling us something about how Early Holocene climatic changes—which restructured vegetation in big ways—restructured wild jungle fowl. Then it was one of these localized population that millennia later got domesticated. In all likelihood that localized population that was actually domesticated won’t exist anymore. It is also worth noting that the reality of domestication bottlenecks is itself somewhat dubious and is in the past year or two come to be questioned. Where ancient DNA is available (e.g. maize, sorghum, barley) it is demonstrable that no such bottleneck occurred and age estimates (see Allaby, Ware and Kistler 2019) that conceive some sort of a bottleneck may not be really telling up about domestication. 

Given what we know of the archaeology of SE Asia, one would tend think the initial  domestication and spread of chicken is unlikely earlier than the grain-based Neolithic that starts around 2500 BC (in southern bits of China) and reaches southern Thailand at 2000 BC. However, as far as I know there are no archaeological chicken finds at early sites. So I wonder whether the first spread of domesticated chicken might represent a secondary later spread perhaps closer to 1000 BC (the period when Bronze working spread southwards from China); this might also be the period when new crops spread like sticky rice. It may be that at that time chickens also spread rapidly via trade routes to India. I have long argued (e.g. Fuller 2007) that in South India the Dravidian linguistics suggest arrival of chickens after the South, South-Central and Central languages had fully diverged (which is something like 3000 years ago). Not long after this there are good chicken terminologies in Sanskrits and Prakrits from the 1^st Millennium BC, so it makes sense that chickens really only became established as livestock in India at around that time, and of course it is the later Iron Age when they first turn up in the west , such as the Hellenistic era evidence from the Levant (Perry-Gal et al 2015), or as an exotic animal in western Europe (Sykes 2012).

Rice awn reduction: not a domestication trait

In a recent paper in Economic Botany, Svizzero, Ray and Chakraborty (2019) ask whether awn reduction is really part of the domestication syndrome of rice or instead a crop improvement trait. It is true that I once listed this as part of the domestication syndrome traits in cereals (Fuller 2007): awn/appendage reduction, but I don't think I really pressed for this to a be central part of domestication. It was only meant to identify a tendency that recurs across most cereals. I would now agree that this post-domestication and varietal improvement trait. That this should be regarded as post-domestication/improvement trait is clear from the fact that it affects only some lineages of rice (most temperate japonica, many indica, but few tropical japonica or circum-aus, and mostly not Oryza glaberrima). Many cultivars have awns of varying length. The authors usefully illustrate diagrammatically how economy (foraging, pre-domestication cultivation, agriculture), harvesting methods and the evolution of some morphological traits (like the awn) are not synchronous changes. These are part of what makes domestication a protracted and entangled process.

In the case of rice, the presence of awns may have actually been necessary during the early stages of cultivation! This is the implication of recent work by the Kobe rice genetics group (Ishii, Ishikawa and colleagues), who have recently published data identify three interacting loci in rice (Amarasinghe et al 2020 in Rice) . They have worked the slow processingf of backcrossing indica genetic components into a population of wild rice, and are able to document the additive effects of 3 loci on reducing the awn length. The reason that awns are important in wild rice has to do with seed dispersal-- like in other cereals awns help to propel spikelets across and into the soil, and in the case of rice they likely also play a role in dispersal across water. But the reason they would have been important to early rice gatherers and the first rice cultivators is that awns mean that grains, even after they have shattered, to get stuck within the rice panicle, making them more readily gatherable by people. This goes hand in hand with a key domestication trait, previously identified by work at Kobe, namely the closed panicle morphology (controlled by the OsLG1 mutation, also called SPR3, published in Nature 2013). This closed panicle trait would make the more compact panicles easier to harvest, especially with long awns that allow shattered spikelets to get caught. Indeed, the data in Ishii et al (2013), allows us to estimate an increased in return rate on harvested rice, with just this mutation of about +50%. This actually implies that awns were selected for during earliest phases of cultivation, but would have lost selection advantages (in terms of harvest) once non-shattering became dominant.  Thus, as concluded by Amarasinghe et al 2020,  after domestication it became reasonable to selected for reduced awns. Without awns harvested spikelets take or less space and plant would not have needed the same degree of metabolic investment in producing awns. The reduction of awns is also common in many varieties of wheats, barley, oat, but I suspect it was not actually part of the initial domestication in these either. Thus the conclusion of Svizzero et al (2019) may well have relevance to many cereals beyond rice.

However, Swizzero et al are wrong that this trait can not be studied archaeologically, even if it really hasn;t been so far.  We are able nor to recover lemma apex remains and determine these as awned or awnless (as in the example at left from work by Cristina Castillo at Khao Sam Kaeo, Thailand). In recent years work by Castillo, myself, and others has increasingly recovered these from flotation samples. They are lightly smaller than spikelet bases, less common than spikelet bases but nevertheless can be reognized as either complete apices (with a beak like end) or torn (like the one at left) indicating that they were awned. Thus there is potential to study this archaeologically. The example shown here is part of a dataset that indicates the predominance of awned japonica rice in Thailand upto at least the Iron Age. In waterlogged material from the Lower Yangtze it is clear that early rice, even non-shattering ones are awned. More work to be done on recognizing when and where awnless rices became common. Reduced awn or awnless rices appear to be present at Roman era sites on the Red Sea soast of Egypt (at Berenike and Quseir al-Qadim), at which time they are presumably being imported from somewhere in southern or western India (published in the books by Rene Cappers, and Marijke van der Veen).

Rice domestication was slow, and post-domestication varietal diversification, including the reduction of awns in some varieties, took even longer. And there is much we still don't know about this history-- but a history of varietal and geographical diversification starting to be unravelled in part through genomic history (but that should be a post for another time).

Citrus diversity in Roman Naples: pollen evidence for tangerines

The early history of Citrus fruits in the Mediterranean has been an active area of discussion amongst archaeobotanists, historians and palynologists in recent years. It has been well-established that citrons (Citrus medica) and lemons (Citrus limon) were known. For one thing they appear distinctively in Roman art, and for another their seeds are well known from Pompeii (e.g. Celant and Fiorentino 2018). What has been less clear is whether anything that we would call an orange today was known. Despite plausible textual sources, it is always hard to translate ancient terms into botanical species, especially in Citrus fruits that are so variety-rich, prone to both hybridization and frequent somatic mutations. So I have tended to think that some of the few orange-like seeds from Pompeii and from Rome, might just be outliers in the range of variation of early lemons (which are likely to have some pomelo and orange related ancestry in their South Asian origins (see, e.g. Fuller et al 2018). But an important new morphometric investigation of pollen of several Citrus species and archaeological pollen from Oplontis (near Pompeii) seems to have cleared this up. 

Lumaga et al. (2020) in a recent Vegetation History and Archaeobotany article, demonstrate the clear distinction in exine form, especially the cell or lumen size, that differentiates oranges (C. reticulata- the more primitive species, or less hybridized, of mandarin oranges or tangerines and similar small, sweet fruits). Much larger lumens characterize lemons. So I stand corrected on the Citrus diversity of Roman Italy: at least citrons, lemons and mandarins were grown.

This raises interesting questions about how these got to Rome. While these oranges were certainly known in China prior to the Han Dynasty, I have previously deduced that early orange in India-- known from Prakrit and Pali sources of the First Millennium BC-- naranga-- were perhaps most likely bitter oranges (Citrus aurantium), with sweet fruits coming later. Long distance transport of fruits from China to Rome strikes me as unlikely, so perhaps then there was more fruit diversity in northern Indian after all included under the rubrice of naranga, or other less obvious terms. Early South Dravidian languages (precursor to Old Tamil and Kannada) do seem to have two different kinds of oranges. This highlights all the more need for archaeobotanical investigations of early citrus (hidden in flots as charred rind fragments) throughout South Asia and Middle East in the Iron Age period.

I was recently interviewed about the history of Citrus fruits, especially oranges, in Europe in relation to how we can understand their use and symbolism in the writings of William Shakespeare: find the podcast here: That Shakespeare Life.

On the Anti-Neolithic of Cyprus

Cyprus is the first place that we know that crops and livestock were spread to by human action. This even took place before domestication. Morphologically wild wheat and barley, cattle, sheep and goat that appear wild. Cats that were presumably following mice that were stow-aways with grain stores on those early boats; early meaning ~9000 BC. But despite this very early start on the path to agriculture, Cyprus throughout the Neolithic and into the Bronze Age appears decidely unagricultural, what I might dub an anti-Neolithic. This is evident due to the accumulation of archaeobotanical and zooarchaeological evidence, that my colleague Leilani Lucas has been compiling and analyzing for several years, and which is summarized and discussed in our new Journal of World Prehistory article.

Long-term Cypriot trends  in cereals (vs. wild plants)
 Cyprus (black squares) vs. the
mainland (above). Below: proportion of deer
out of  consumed meat (below) 

Cyprus is perhaps quintessentially an island, in the sense of demonstrating evolutionary patterns that work differently from the large land areas and populations of the mainland. So years ago her work demonstrated that in terms of morphological change, domestication processes seem to be happening faster on Cyprus, with much higher rates of grain size increase in wheat. But this does not mean that wheat became quickly important or even that the overall economy was especially agricultural. Instead it appears that cereals (and other crops) remain a minor, rather than dominant, part of the economy for millennia (see left). This is in contrast to the mainland Fertile Crescent where increasingly morphological features of domestication are accompanied by a trend towards increasing use of cereals and dominance of wheats and barley out of all plant remains. If agriculture as an economic change is properly decoupled from domestication (and genetic change), then these trends clearly do not go together on Cyprus. The same is clear in the faunal record. Despite the early translocation of mammals, including livestock or potential livestock (like cattle) but also wild game (like boars and deer), it is hunted game, especially deer, that dominate bone assemblages. Cattle even plausibly go extinct and get reintroduced to Cyprus. For fully agricultural economic systems one perhaps needs to look at transformations from the Middle to Late Bronze Age, driven by Cyprus getting more central to a world system of trade, in which cultivation of "cash crop" fruits became important. In this context continued hunter-gatherer economic activities  lost ground to the food and economic production activities that transformed the wild fringes to investment agriculture.

Thus despite material culture that we class as Neolithic (and Bronze Age) the economy looks rather anti-Neolithic.

Structured diversity in tea does not mean multiple domestications

Genetic population structure of tea.

When and where were tea domesticated? And how many times? This is a question I get asked sometimes, and a paper published a few years ago was just brought to my attention that claims to have genetic evidence for three separate domestications, by Meegahakumbura et al. (2016) in PLOSone. I disagree. The paper convinced me of quite the opposite. It remains entirely likely that tea was domesticated only once in ancient times, even if there were widespread use of wild tea leaves across their wild range by people who encountered them-- but a key problem remains determining what that wild range was. The Meegahakumbara paper is an interesting one in terms of raising the question as to how much underlying geographical structure there is in the genetic diversity of tea, and how this relates to different cultural traditions of use, and which (if any) can be regarded to evolving into domesticated forms. But in the end there are severe limitations to their study. Despite some sampling from "wild" populations in India and China, as well as cultivars, there is a lack of samples from in between (northern Vietnam, Myanmar and presumably Laos, which are all presumably within the range of wild teas. What is really at issue is whether or not the large tree forms of tea are primarily wild (and recently managed or cultivated) or represents a distinct domesticated form, and this in turn raises the issues of what is "domestication" in tea. Domestication implies morphological adaptations, underpinned by genetics, which have been favoured through the propagation over generations by people. We know full well what this entails in cereals and seed crops (see, e.g. this Annals of Botany article); we can propose what is involved in tree fruits (which are harvested for fruits and presumably early on cultivated from seed: see "long and attenuated"); and we can also propose what is common about domestication in tubers and other vegecultural crops (see this recent Annals of botany article). But what about tea? Since tea can be propagated by seed or by cuttings it might share some similarities with either tree fruit or vegecultural domestications, but its use for leaf harvesting makes it quite different. Characteristics that might fit in the vegecultural domestication syndrome, include increased proportion of edible (leaf) to inedible (trunk) parts, and more asynchronous production of those. In developmental terms there appear to be selection for dwarfism-- smaller leaves, smaller stature, and more compact growth, which together with human management give teas their very trimmed hedge look (below).

Tea (C. sinensis sinensis) cultivation in Zhejiang
(Photo: DQ Fuller, 2004)

So what did Meegahakumbara et al. find? They demonstrated 3 distinct populations, and a 4th (lasiocalyx) that looks admixed between the Indian and Chinese tree teas (Figure at top). Truly domesticated tea (C. sinensis sinesis) looks to a be a strong clade. That is (in my view) the only really domesticated form. It has distinctive morphology (dwarfism).  It could already be distinct by the Han period, or at least under selection, since small, immature leaves are among the grave goods in the Yangling tomb of a Han Dynasty queen in Shaanxi, indicating trade from distance Yunnan already by 2200 years ago (see this Scientific Report). While it could be that tea was still a wild utilized plant, it might make sense that by this period experiments with cultivation had begun with an ancestral form of C. sinensis sinensis. It is also plausible that some cultivation developed in parallel with the distinct species C. taliensis, but its cultivation never spread beyond the Myanmar-Yunnan border regions (see, this paper on taliensis tea), so it is less relevant to the main domestication story of tea.

But is there any reason to assume that the distinct populations of large tea forms of tea, which they refer to as Assam tea (C. sinensis assamica). They divide this tall tree tea (see left) into two geographical groups (Indian assamica and Yunnan assamica, which leads to the somewhat oxymoronic terminology of "Chinese assam tea"). I do not see any reason in these data, or rationale provided, to not assume that Chinese tea is a domestication bottleneck from the Yunnan tree tea (assamica sensu  lato). The Assam and Yunnan populations of tree teas are distinct as one would expect of any geographically distant populations of a wild species. Trees of this assamica tea are also wild through large parts of northern Vietnam (see Zhao et al. 2017), and I would expect them also in Laos and parts of Myanmar.  In India these tree teas were used from the wild by a few local minority tribes prior to the British introduction of tea drinking and Chinese domesticated tea to India. But these were presumably only ever gathered wild. These Assam tree teas only came into cultivation (equivalent to pre-domestication cultivation) in the colonial era.  though they have now been cultivated by ~200 years, there seems no basis to assign them to domesticated status.

The Yunnan tree teas (What they call Chinese Assam tea) are presumably also native to the forests of parts of Yunnan, where they were also used by indigenous people. In this region their cultivation and management has continued while perhaps unmanaged populations went extinct in the wild. They could still be also the source of domesticated C. sinensis Chinese tea, or related to that source.

Tree (assamica) tea, leaves and fruits
(after a photo in the Hangzhou Tea museum)

The Cambod teas (C. lasiocalyx) look to me like part of the structured variation of a wild species that included geographical populations: i.e that the tea trees of Yunnan, India and adjacent Northern SE Asia (Vietnam, etc) borderlands should probably all be C. assamica (or  C., sinensis assamica, as taxonmically described by Zhao et al. 2017).  In their K=3 structure analysis these are grouped with Indian Assam wild tea trees, so it may be that lasiocalyx is just a northerly somewhat smaller variant of wild tea trees. It is plausible that domesticated Chinese tea came from this Cambod end of the wild range, i.e. further east, like SE Yunnan and is more distance from the Assam end of the geographical variation. It is a pity their is no geographical information on the assamica and lasiocalyx populations-- in terms of where and what habitats they come from. Although with a species like this it is not really surprising if wild populations have been completely lost. One is hard pressed to identify truly wild populations of some of the world's more popular nuts, whether chestnuts or walnuts, as these trees have been so heavily anthropogenically influenced in terms of where they grow.

So the origins of tea cultivation: southwest China, some place and time still to be determined. But the use of wild tea leaves by local peoples, widespread from Northeast India through Vietnam.

On the history of tea, see especially this magnum opus by Van Driem, reviewed here.