Genetic neoteny - how delayed genes separate human brains from chimps

Blogging on Peer-Reviewed ResearchBe it in sports or comedy, they say that timing is everything. In evolution, it's no different. Many of the innovations that have separated us from other apes may have arisen not through creating new genetic material, but by subtly shifting how the existing lot is used.

i-4ef823392f2015cb912d0c7a0d0768c6-Babychimp.jpgTake our brains, for example. In the brains of humans, chimps and many other mammals, the genes that are switched on in the brain change dramatically in the first few years of life. But Mehmet Somel from the Max Planck Institute for Evolutionary Anthropology has found that a small but select squad of genes, involved in the development of nerve cells, are activated much later in our brains than in those of other primates.

This genetic delay mirrors other physical shifts in timing that separate humans from other apes. Chimpanzees, for example, become sexually mature by the age of 8 or 9; we take five more years to reach the same point of development.

These delays are signs of an evolutionary process called "neoteny", where a species' growth slows down to the point where adults retain many of the features previously seen juveniles. You can see neoteny at work in some domestic dog breeds, which are remarkably similar to baby wolves, or the axolotl salamander, which keeps the gills of a larva even as it becomes a sexually mature adult. And some scientists, like the late Stephen Jay Gould, have suggested that neoteny has played a major role in human evolution too.

As adults, we share many of the physical features of immature chimps. Our bone structures, including flat faces and small jaws, are similar to those of juvenile chimps, as is our patchy distribution of hair. A slower rate of development may even have shaped our vaunted intelligence, by stretching out the time when we are most receptive to new skills and knowledge. Somel's research supports this idea by showing that since our evolutionary split from chimpanzees, the activation of some important brain genes has been delayed to the very start of adolescence.

Somel collected samples of brain matter from 39 humans, 14 chimps and 9 macaques, all of whom had recently passed away and who represented a wide range of ages. He focused on almost 8,000 genes and analysed when they became activated in a part of the brain called the dorsolateral prefrontal cortex (DLPFC).

i-fed24122d9c81833f1ac19bf2d237633-Neotenygenes.jpgOn a broad level, all three species showed similar patterns. The majority of these 8,000 genes were expressed in different ways as the animals age and most of these changes happened very early on.  In both chimps and humans, half of these shifts take place within the first year of  life. The same thing happens in the brains of mice, which suggests that this is a general pattern of brain development that is common to most, if not all, mammals.

But these superficial similarities mask subtler differences. Somel looked at each gene individually and focused on those that are activated differently as the brain matures; he found that half of these follow different journeys in humans compared to chimps. Some were switched on at an earlier point in time but a much higher proportion were delayed in their timing. These genes were neotenic - in the brains of humans, their use matches that of much younger chimps.

To work out the proportion of neotenic genes in the human DLPFC, Somel compared brain samples taken from 14 humans and 14 chimps, who were matched as closely as possible for both age and sex. He considered 300 genes whose timings had shifted in humans or chimps, and worked out whether each was activated earlier (accelerated) or later (neotenic) in either species. He found that the neotenic human genes were in the majority and outnumbered the other groups by a factor of two.

This isn't just a property of the DLPFC; Somel found the same pattern by looking at another part of the brain - the superior frontal gyrus - in 9 other humans, chimps and macaques. Here, the dominance of neotenic human genes was even more pronounced and they comprised half of the total sample.

i-008bc24a40769a8430db4e508dce6cef-Humanneotenic.jpg

So clearly, some genes in the human brain have come to be activated at a later point in time than their counterparts in chimps. These are still in the minority - it's not the case that the development of the human brain as a whole has been drawn out. This mirrors the use of neoteny in explaining the evolution of human anatomy too - those who first proposed the idea of humans as neotenic apes applied the idea with broad brushstrokes to our entire bodies; now it's restricted to specific parts.

Finding out exactly what these genes do is the next big step. For starters, Somel has found that many of the neotenic genes are activated in our grey matter (the bodies of nerve cells, as opposed to white matter, which is the cabling that connects them).

The differences in timing between humans and chimps are particularly pronounced when we reach the start of adolescence. At this point, our brains become dramatically reorganised and our grey matter actually starts to shrink, as unused connections between neurons are trimmed in a bid for efficiency. Somel thinks that delaying the point at which this happens may have given us extra invaluable time with which to pick up knowledge and skills.

[PS I'm not sure I like the headline. For some reason, I had a total mental block about it; better suggestions welcome - Ed]

Reference: PNAS 10.1073/pnas.0900544106 to be published this week

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Great summary of our paper! It is not common to see such precise and understandable description of a scientific study. next time we are writing a paper, we should ask you to help.

Michael Lachmann & Philipp Khaitovich

By Michael Lachmann (not verified) on 24 Mar 2009 #permalink

"Many of the innovations that have separated us from other apes may have arisen not through creating new genetic material, but by subtly shifting how the existing lot is used."

boy that's vague. Tell that to Richard gene-king, Richard Dawkins. Is there any wonder people don't believe in evolution?... Evolutionists have no idea what makes a human different than a chimp or a fly or a mouse. Absolutely, completely, totally clueless. Funny how they've lied to the public to make them think otherwise. Losers. ToE is stupid.

Evolutionists have no idea what makes a human different than a chimp or a fly or a mouse.

It's the spelling.

I know chuck's just trollin' for jebus, but I'll bite nonetheless.

What exactly is vague about that statement, chuck? And how does it contradict the principles of modern evolutionary theory? I'm sure even you could name a few ways in which we're different from chimps, chuck, and the important bit about this research is that it sheds some light on why this particular bit (the brain) is different, and how it came to be that way.

And Ed, at least the headline is difficult to misunderstand and/or turn into a creationist weapon, unlike for example: "Humans are just retarded (or "developmentally challenged" if someone prefers the pc version) chimps". I could totally see the Discovery Institute or some other paragon of scientific (and journalistic) integrity having their wicked way with a paper as interesting as this.

You can see neoteny at work in some domestic dog breeds, which are remarkably similar to baby wolves, ...

And cats will act as kittens toward humans if they're imprinted to humans at the right time.

We probably became human by domesticating ourselves.

But perhaps we got help, from the dogs. Kids easily bond with animals. Having a dog partner could help a young human survive early in life.

[Recent news suggests that dog and man have been living together much longer than was assumed before. Must dig up that reference.]

So, I kinda wonder what a neotenized h. erectus would look like and wonder what kind of conditions would select for that. Would a neotenized chimp express its genes in such a way that it would appear to be more like a bonobo in morphological structure, less sexual dimorphism and maybe increased socialfamilial cohesion instincts?

Very interesting article.

How did the researchers determine whether which genes were activated in the tissue they sampled was a constant feature of the age of the animal; or just a transient activation phase captured at the time of death?

Thanks!

I've been wondering for some time whether or not pedophilia was an evolutionary driver for human neoteny. It's certainly plausible, and possibly testable using shorter-lived organisms as proxies. David Brin has an essay where he argues the connection goes the other way, i.e. neoteny enables pedophilia, but that seems less plausible to me.

Of course, this line of reasoning and experiment might not be terribly desirable to follow through on, because so many people think that just because something WAS so at one point in our evolutionary history then this makes it desirable or natural to BE so now. This is the "You can't get an ought from an is (or was)" fallacy. And, while some places have gone overboard in the fight against pedophilia (one young man is serving a *ten year* jail sentence for having had sex with a 15 year old girl --- when he was 17) it is absolutely clear that sex with people who cannot reasonably consent is fundamentally wrong. So, we don't want to enable people to argue for pedophilia.

Still, I find I'd like to know the answer to this. Was, at some point in our history, pedophilia an important driver in making us neotenous apes? Some of the items on Stephen Jay Gould's list of neotenous characteristics (from the work of Bolk) would seem to support the idea (vide 2, 9, and 12); others, not so much. Ed, do you know of any research on this idea? I doubt I'm the first to think of it.

@Stephan
Thanks for raising this point. We indeed (have to) use brain tissue from dead individuals, so you are right to wonder how much gene expression in dead brains represents those in live brains. Previous work form our lab showed that the correlation is actually quite good (http://genomebiology.com/2005/6/13/R112).
In addition, the patterns of expression change we find with age also relate to specific biological functions, such as developmental processes, which gives us more confidence. Also note that, we are studying changes with development, so any expression pattern that occurs at or after death would need to occur in different ways between children and adults (as well as between humans and chimps). This could be the case if types of death (quick or slow) among individuals correlated with age. But that was not the case among the subjects in our study.
Hope this was clear.
And Ed, thanks for covering our work!
Mehmet Somel

By Mehmet Somel (not verified) on 25 Mar 2009 #permalink

Assuming you're the real Dr. Somel,

Wow, thanks for taking the time to answer my question! It's very interesting research.

Stefan

@Rob C.

Hmm ... that's a fascinating idea. I'm not sure how plausible it is, though. What benefit would attraction to sexually immature mates have?

The issue of paedophilia and neotony is interesting though recognizing/differentiating the sociopathic variety such as sometimes seen in certain genetic conditions (Kleinfelters syndrom) from the instinctual desire to mate with younger and presumably more fertile partners, would be essential if it's to be considered at all. As to what advantage neotony might confer in our ancestors, questions of paedophilia aside, perhaps neotony would have helped early humans in overcoming some instinctual resistance to large and complex social structures and concomitant issues of dominance and aggressoion, which in turn allow for longer infant and adolescent stages and great degree of cooperative behaviors and instincts to become more prominent and integral to what makes us so social and so human.

@Paper Hand

"What benefit would attraction to sexually immature mates have?"

None that I can think of offhand (perhaps one could invent some plausible just-so stories). It might arise accidentally as an extreme of a gradual shift towards younger (looking) mates (which I now realize is closer to Brin's point), and the shift towards younger (looking) mates would be a self-reinforcing generational loop as per the standard theory of sexual selection (except in this case it's a bit self-referential as the sexual selection would be for sexual preference itself).

The possible replacement of younger mates by younger "looking" mates would be the driver for neoteny that I was wondering about.

@doug

"younger and presumably more fertile"

Many species have clear markers as to when individuals become fertile. We do too, but they're a bit blurry compared to many, I think. It's just not true that younger = more fertile. The world's youngest mother was 5 when she gave birth (! according to my old Guinness Book of Records) but that's the absurd (and horrible) early end of the frequency distribution---one sees a ramp-up to higher fertility rates starting at near-zero when normal puberty begins, through a peak (the age of which depends strongly on individual life-history) and gradual diminishing till menopause. (Oldest mother, same Guinness Book, gave birth at age 69).

What I was wondering about was what role, if any, pedophilia, or its cousin ephebophilia, played in the gradual neotenization of ancestral apes to humans. It now seems to me that all you'd need for neoteny to arise was a slight preference, on average, for "younger than optimal" mates.

Why such a preference could arise, or what benefit it could have (or lack of penalty), is a different question. One could, again, imagine "just-so" stories for that, but I'd prefer first to see if it could happen that way at all.

I think the Vila et al dog genetics study has been superseded by these papers:
Leonard, J. A., R. K. Wayne, J. Wheeler, R. Valadez, S. Guillen, and C. Vila. 2002. Ancient DNA evidence for Old World origin of New World dogs. Science 298:1613-1616.
Savolainen, P., Y.-p. Zhang, J. Luo, J. Lundeberg, and T. Leitner. 2002. Genetic Evidence for an East Asian Origin of Domestic Dogs. Science 298:1610-1613.
and the Aurigancian dog story can be found at:
Germonpré, M., M. V. Sablin, R. E. Stevens, R. E. M. Hedges, M. Hofreiter, M. Stiller, and V. R. Després. 2009. Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. Journal of Archaeological Science 36:473-490.

Of course these tend to depend on an assumption that the relationship between the humans and the dogs can be defined by either the genes or the morphology. Whereas (I think) the implication of the paper that is the subject of this blog is that there may be some subtler processes involved.