Sunday 28 June 2020

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 1st 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).


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