What domestication can and can't tell us about evolution

Domestication is the harnessing of one species by and for the benefit of another, usually via selective breeding. Humans are master domesticators, but we're not the only ones.  There are ants that farm fungi, and milk aphids, but it has also been suggested that the Melissotarsus ant in continental Africa and Madagascar has domesticated a scale insect for its meat but if not for meat, some other nutritional benefit such as of waxy secretions from the scale insect. Whether these ant/domesticate relationships depend on genetic changes is not clear, at least to us.

Two key differences are, first, that humans work teleologically, or so we assume!  That is, the 'artificial selection' that the domesticators had some end in mind--more yield, more easy harvestability, drought resistance, and so on.  Secondly, we presume that in the past, as now, this process involved not just purposive breeding, but strong selection -- much faster and more directed than natural selection.  If domestication was slow or inadvertent, then the resulting genetic picture may differ.

Humans appear to have begun to domesticate plants and animals ~12,000 years ago, and a new review in Nature Reviews Genetics ("Evolution of crop species: genetics of domestication and diversification," Meyer and Purugganan, online 18 Nov 2013) reports that recent work has identified genetic signatures of that artificial selection in plants, and of subsequent diversification of these crops.  These studies "reveal the functions of genes that are involved in the evolution of crops that are under domestication, the types of mutations that occur during this process and the parallelism of mutations that occur in the same pathways and proteins, as well as the selective forces that are acting on these mutations and that are associated with geographical adaptation of crop species."

Charles Darwin, of course, based much of his argument about evolution and natural selection in The Origin of Species on observations about artificial selection from the breeding of plants and animals for food.  He writes of this explicitly in these frequently quoted words from his autobiography:

..After my return to England it appeared to me that by following the example of Lyell in Geology, and by collecting all facts which bore in any way on the variation of animals and plants under domestication and nature, some light might perhaps be thrown on the whole subject. My first note-book was opened in July 1837. I worked on true Baconian principles, and without any theory collected facts on a wholesale scale, more especially with respect to domesticated productions, by printed enquiries, by conversation with skilful breeders and gardeners, and by extensive reading. When I see the list of books of all kinds which I read and abstracted, including whole series of Journals and Transactions, I am surprised at my industry. I soon perceived that selection was the keystone of man's success in making useful races of animals and plants. But how selection could be applied to organisms living in a state of nature remained for some time a mystery to me.

Fifteen months after I had begun my systematic enquiry, I happened to read for amusement Malthus on Population, and being well prepared to appreciate the struggle for existence which everywhere goes on from long-continued observation of the habits of animals and plants, it at once struck me that under these circumstances favourable variations would tend to be preserved, and unfavourable ones to be destroyed. The result of this would be the formation of a new species.

Here, then, I had at last got a theory by which to work; but I was so anxious to avoid prejudice, that I determined not for some time to write even the briefest sketch of it.   

Indeed, after the Origin, Darwin published two hefty volumes of the effects of artifical selection on plants and animals.

Now, in a modern parallel, Meyer and Purugganan argue that understanding of the genetic underpinnings of domestication can shed light on evolutionary processes, in general, specifically because domesticated crops are recent, selection was strong, and (presumably) consistently directional, and there is good archaeological and historic evidence of the origin, spread and diversification of domesticated crops.

Humans first began to domesticate plants about 12,000 years ago in the Middle East and Fertile Crescent, but plants were also domesticated elsewhere, in China, Mesoamerica, South America, sub-Saharan Africa, and North America from 10,000 to 6000 years ago as well.  Many of these were independent of each other, and involved totally different species, providing, in principle at least, multiple independent views of the genomic aspect of the process.  Artificial selection often involves genetic changes that reduce a plant's fitness in the wild, and species that are completely domesticated cannot survive without human intervention in their reproduction and growth. The process may be rapid, or may take thousands of years.

After domestication, in the "improvement phase", the species can diversify and spread, involving genetic and phenotypic changes that allow adaptation to different ecosystems and climates, generally as a response to selection pressure on chosen traits.  Many such traits have been selected for, but generally they have to do with increasing quality, yield and ease of farming.  Milk yield in dairy animals, tameness or ability to reproduce under domestication, for example.  Or, in grasses, the evolution of larger seeds than in wild grasses, and crucially, a non-shattering rachis.

Commonly observed traits accompanying domestication and diversification; Table 1, Meyer and Purugganan, 2013

When wild wheat is ripe, for example, the rachis (the stem on which the wheat shafts grow) easily shatters, allowing seeds to disperse in a wind or when otherwise disturbed.  This wouldn't be desirable in a crop plant, which the farmer wants to be able to harvest at his or her chosen time, and domesticated wheat has a history of selection for a less brittle rachis so that the seed remains in situ until ready for harvest.
 

Hulled wheat vs free-threshing wheat (wild vs domesticated); Wikimedia

Genes associated with domestication and diversification have been identified with fine-mapping or GWAS, primarily in maize and rice, although, say Meyer and Parugganan, identifying causal mutations has been difficult, although some functional studies have been done.  In addition, they point out, it can be difficult to distinguish mere correlation with domestication and diversification with causation. 

The first "domestication gene" identified was teosinte branched1 (tb1) which is responsible for differences in the shoot of wild and domesticated maize.  Not all changes can be traced to a single gene, however.  Hundreds of domestication genes and loci have been identified in other plants as well, largely in cereal crops, although, for many of the same reasons that genes 'for' disease and other traits can be hard to identify, the specific genes responsible and their functions are often difficult to narrow down--just as we have trouble finding 'the' gene or genes 'for' human traits. 

Architecture of domesticated maize vs wild teosinte; Doesbley, 2003

Even with complications, however, Murray and Parugganan evaluate the role in domestication or diversification of 60 specific genes that have been functionally validated and/or included in population genetic studies.  They note that many of these are regulatory genes that control the timing, amount, or cell-context of the gene's usage.  And, many of the genetic changes correlated with domestication and diversification are nonsense mutations or frameshift indels that alter the protein coded for by a gene, and result in the "large phenotypic effects that are observed during crop evolution."

Among the genes the authors identify with domestication are those involved in regulation of inflorescence development (an inflorescence is the cluster of flowers on a stem that will become seeds; see image above), vegetative growth habit and height, seed pigment, size, casing, nitrogen access and efficiency, and fruit flavor in strawberry, and so forth. Diversification genes include those involved in fruit shape and size, inflorescence architecture, color, starch composition, dwarfism, flowering time, and more. 

It is difficult to know whether a mutation is a precursor to domestication or diversification, or simply happened to arise at around the same time.  People might have noticed a precursor and chosen to breed it, for example.  Some are present in the wild plant but at much lower frequency than in the cultivated plant, which suggests that it, in conjunction with other genetic changes, may be associated with domestication. 

It's possible that because domestication is selection on a trait not a gene, the underlying genetic architecture of a trait is different in different species.  This is certainly true for many phenotypes not related to domestication, so wouldn't be unexpected.  Murray and Parugganan suggest that finding such parallelisms can explain the genetic basis for Darwin's idea of "analogous variations" and for Russian botanist and geneticist of the early 20th century, Nikolay Vavilov's idea of the Law of Homologous Series (I can't resist noting here that Gary Nabhan writes beautifully about Vavilov's life and work in his 2009 book, "Where Our Food Comes From: Retracing Nikolay Vivilov's Quest to End Famine").  This can happen by phenogenetic drift, or by parallel evolution.

This paper is an excellent reprise of the state of knowledge of crop domestication -- with one quibble. Murray and Parugganan write that "Domestication provides a fascinating model for the study of evolution..."  Darwin thought so, too, but artificial selection, the basis for domestication, is directed, strong, and often fast.  Not only is natural selection generally much weaker, but it is not directed and evolution by natural selection is typically slow.  With complex causation, strong selection should often have very different genomic consequences compared to weak selection -- the former being more single-gene or at least simpler in nature.  But even with relatively simple causation that could be picked out at a specific gene level by artificial selection, slow natural selection may not be so gene-specific.

In addition, much of evolution seems not to happen by natural selection but instead by genetic drift or other forms of selection (organismal selection, niche selection, and so forth), while domestication is due to strong, directed artificial selection.  Thus, the lessons of domestication aren't always a good model for evolution in general.

Indeed, while Darwin thought of domestication as a good model, Alfred Wallace, the co-discoverer of evolution did not.  He noted, in his letter read to the Linnean Society ("On the Tendency of Varieties to depart indefinitely from the Original Type"), in 1858 along with Darwin's, announcing their co-discovery,

     One of the strongest arguments which have been adduced to prove the original and permanent distinctness of species is, that varieties produced in a state of domesticity are more or less unstable, and often have a tendency, if left to themselves, to return to the normal form of the parent species; and this instability is considered to be a distinctive peculiarity of all varieities, even of those occurring among wild animals in a state of nature, and to constitute a provision for preserving unchanged the originally created distinct species....

     It will be observed that this argument rests entirely on the assumption, that varieties occurring in a state of nature are in all respects analogous to or even identical with those of domestic animals, and are governed by the same laws as regards their permanence or further variation.  But it is the object of the present paper to show that this assumption is altogether false, that there is a general principle in nature which will cause many varieties to survive the parent species, and to give rise to successive variations departing further and further from the original type, and which also produces, in domesticated animals, the tendency of varieties to return to the parent form.

Selection is a far more curious phenomenon than it is typically given credit for being.  It is too easy for us to compress time in our minds and think of natural selection as if it were artificial, strong and directed.   But the beasts and foliage of nature may, like a Rousseau painting, be a thicket of meandering change, sometimes for inscrutable reasons.