I recently attended a symposium at the Salk Institute on “Domestication and Human Evolution.” The symposium was organized by CARTA, the Center for Academic Research and Training in Anthropogeny, whose charter is “to explore and explain the origins of the human phenomenon.” As the name indicates, the focus of this symposium was on how domestication affected the evolution of humans as well as other species.
In his opening remarks, co-chair Robert Kluender explained why domestication is important in the study of evolution: it is one of the few known mechanisms for rapid change (or “saltation”). The theory of evolution as proposed by Darwin predicts only slow changes, which occur as a result of tiny changes in each generation accumulating over long time periods (“gradualism”). However, there are examples of changes occurring in species more rapidly than could be explained by gradualism. Domestication has been shown to be a mechanism for causing some of these rapid changes. For example, in the famous silver fox domestication study in Siberia beginning in the 1950s (and still ongoing), Soviet scientist Dmitri Belyaev and his successor Lyudmila Trut were able to tame wild foxes in a surprisingly small number of generations: “By the tenth generation, 18 percent of fox pups were elite [very tame]; by the 20th, the figure had reached 35 percent. Today elite foxes make up 70 to 80 percent of our experimentally selected population.” [reference]
The symposium featured eight 20-minute presentations which covered the domestication of a variety of animals, including dogs, foxes, birds, apes, and humans. Most of the examples presented were of species that self-domesticated (in contrast to species that humans domesticated). All of the talks shared some fascinating common themes, which I will attempt to summarize in the next couple of sections.
The “Domestication Syndrome”
In domestication, the selecting for one trait, tameness, results in a number of other “unselected byproducts.” Many different domesticated animals exhibit the following traits in addition to tameness:
- cranial feminization: facial retraction (shortened snout), smaller teeth.
Below: front and side views of adult chimpanzee (left) and adult human (right) skulls [reference].
- floppy ears (a bit of trivia: the only wild animal with naturally floppy ears is the elephant!)
- piebald pigmentation (large black and white spotting)
- more variation (e.g., dwarfism and giantism) – result of relaxation of selection (more on this idea later in the Case Study)
- reduced sexual dimorphism (e.g., Australopithecus vs. Homo sapiens: In Australopithecus, males were on average 44% larger than females [reference], compared to 15% in humans) – indicates less physical competition for females
- paedomorphism (more on this in following section)
- smaller brains (35% smaller in pigs, 16% smaller in horses; no size difference seen in domesticated mice or fox)
- reduced size of olfactory structure/number of olfactory receptor genes (humans have ‘lost’ 50% of olfactory receptor genes, old-world monkeys 30%, new-world monkeys 20%; even dogs, who we think of as having such good senses of smell, have significantly smaller olfactory structures than wolves do)
- neurotransmitter concentrations: elevated serotonin and tryptophan, lower cortisol (less stress!)
- reduced violence (e.g., finches vs. munia, red colobus monkey of Zanzibar vs. Uganda; more on both these pairs of species in later sections)
- reduced neophobia (e.g., finches vs. munia, domesticated vs. wild foxes)
So what the heck is going on here? Why do all these other traits happen to tag along with tameness?
One speaker, Tecumseh Fitch, proposed a hypothesis that could account for most of these byproducts (excluding brain size) involving the “neural crest,” a layer of cells that exists early in the development of the vertebrate embryo. The cells that form the neural crest eventually migrate to other parts of the body where they produce “not only facial skeletal and connective tissues, teeth and external ears but also pigment cells, nerves and adrenal glands, which mediate the ‘fight or flight’ response.” So the hypothesis goes that “the domestication process selects for pre-existing variants in a number of genes that affect neural crest development. This causes a modest reduction in neural crest cell number or activity. This in turn affects the broad range of structures derived from the neural crest, giving rise to domestication syndrome.” [reference]
Neotony and paedomorphism
A common phenomenon in domestication is for traits that are found only in young members of the wild species to be retained in adulthood in the domesticated species. This often results in the domesticated animal appearing “cuter” to humans.
Some visible examples of this include:
- Adult human skulls resemble infant chimp skulls much more than they do adult chimp skulls, as shown in the photos below. [photo reference]
- The Zanzibar red colobus monkey (below, left) originates from the Uganda red colobus monkey (below, right). Isolated on the island of Zanzibar, the species self-domesticated, and developed a variety of neotenic traits, including paedomorphic coloring (see the pink lips and nose, big eyes, and fuzzy hair in the photo below) and smaller males. They further exhibit the neotenic behavior of late suckling (into adulthood!−you can’t get more neotenic than that!).
- Humans also retain pink lips in adulthood.
Some physiological examples include:
- The myelination process of neurons continues into adulthood for humans, but only occurs in young chimps.
- Gene expression. The patterns of activity over time for certain genes in humans resemble shifted versions of the pattens in macaque monkeys and chimps. For certain genes, the activity peaks during gestation or around birth for monkeys and chimps, while the peak occurs well into childhood for humans.
Some behavioral examples include:
- Wild wolves and foxes bark only as pups; dogs retain this behavior in adulthood.
- Adolescent chimps display homosexual behavior; humans retain this behavior in adulthood. (I swear this was used as an example!!)
Case study: The Bengalese finch
The presentation by Kazuo Okanoya on “Domestication and Vocal Behavior in Finches” was so interesting it deserves its own section here. The speaker began his talk by joking(?) that he will explain how we can learn more about human evolution by studying birds than by studying apes. Okanoya researches Bengalese finches (below, left), a species that was domesticated from the white-rumped munia (below, right) about 250 years, or 500 generations, ago. It is known that the song of the Bengalese finch is much more complicated than that of its wild progenitor. (He noted that there are no records indicating that the finches were ever artificially selected based on song.)
In one experiment, Okanoya swapped out the eggs in two bird cages, giving the munia’s eggs to the Bengalese finch and the finch’s eggs to the munia. He found that song learnability was wider in the Bengalese finch: the baby Bengalese finch was able to learn the munia’s simple song, but the baby munia was not able to learn the more complicated Bengalese finch’s song. They found that the Bengalese finches were able to learn from multiple (2-4) tutors, whereas munias could only learn from their own fathers. Physiological studies showed that the brain nuclei responsible for song control were smaller in munias, and that munias had fewer glutamate receptors, which are important for plasticity (learning). They also found that females prefer the more complex song over the simple version containing the same syllables.
It turns out that the song complexity is positively correlated with the body size of the male. Since females preferred larger, healthier males, they were inadvertently selecting for song complexity. The theory is that song complexity evolved due to female selection under relaxed-constraint environments. That is, in captivity where there are no predators, the birds no longer needed to dedicate so much energy to pure survival, so they were able to dedicate more resources to developing complex songs.
The theory that Okanoya came to based on these studies was that the evolution of song complexity in domesticated finches could be a mirror for the evolution of language complexity in (self-)domesticated humans. Like the Bengalese finches, early humans had virtually no predators, and had lower stress levels than their primate counterparts, which led to enhanced learning.
There were many more details in these presentations that I have not captured in this blog post, but these are the ideas that were most salient for me personally. For a complete list of speakers and titles (and, eventually, videos of the talks), refer to this webpage.