Here’s an evolutionist’s dream: 10,000 planet Earths, starting from the same point at the same time, and left to their own devices for four and a half billion years. What would happen? Could you go on safari from one planet to the next seeing an endless procession of wildly different organisms? Or would many of the planets be home to life forms that are broadly similar?
The conventional answer to this question — the one championed by the late Stephen Jay Gould, for example — is that chance events, from mutations to asteroids, play such a large role in evolution that each of the planets would be totally different. And probably, after four and a half billion years, they would be. I wish we could do the experiment, though. It might hold some surprises.
Looking around the Earth, it’s striking how often similar traits evolve in similar environments. So: birds living on remote islands typically lose the power of flight. Males in species (be they chimpanzees or yellow dung flies) where females are promiscuous tend to evolve high sperm counts and large testes. Animals that live in caves lose their eyes and their color: whether they live in Rwanda or Romania, they’re a pallid, blind lot, the troglodytes. Mammals that specialize on eating leaves — be they cows or langurs (that’s a monkey) — have evolved foreguts where bacteria break down the leaves, as well as special enzymes to help with digestion. Amazingly, the same phenomena are also seen in the hoatzin, a leaf-eating bird from South America. In short, evolution has a remarkable tendency to repeat itself.
That this happens has been known for decades. But now we’re unpicking the genetic basis for the repetitions. And the startling thing is, evolution often repeats itself at the genetic level, too.
Alizarin Red stained sticklebacks. Credit: Pamela Colosimo and David Kingsley, Stanford University.As an example, take three-spine sticklebacks (Gasterosteus aculeatus). These little fish usually live in the ocean, but like salmon, they come into rivers to spawn. As the glaciers retreated at the end of the last ice age — a process that went on between ten and twenty thousand years ago — a series of lakes began to form in the northern hemisphere, and the sticklebacks moved into them. Initially, the lakes would have been linked to the oceans by streams and rivers, but as the glaciers retreated, the land rose up (ice is heavy), and the exits to the lakes closed, leaving the sticklebacks in each lake marooned and isolated. And so the animals stuck there began evolving to live exclusively in freshwater.
Which is a real-life version of the evolutionist’s dream: each lake is an evolutionary experiment, a natural laboratory. Because there are so many lakes, the experiment has been repeated many times; and because we know the ages of the lakes, we know roughly how long each experiment has been going on. And sure enough, fish in different lakes have evolved a variety of similar features, repeatedly and independently.
Drawing of marine sticklebacks. Credit: David Kingsley, Stanford University (based on Cuvier & Valenciennes, 1829).
Marine sticklebacks, for example, boast body armor: from head to tail, they are covered in rows of bony plates. Many freshwater sticklebacks have lost these. In marine sticklebacks, the pelvis is a complicated affair that comes complete with a pair of long spines. In some freshwater populations, individuals have a much reduced, lopsided pelvic structure. In others, they have just a remnant, a small, lopsided bone: the ghost of pelvis past.
Drawing of freshwater sticklebacks. Credit: David Kingsley, Stanford University (based on Cuvier & Valenciennes, 1829).Mutations to a gene called Ectodysplasin have been implicated as the major culprit in loss of armor; another gene, Pitx1, has been fingered as the main agent of pelvis reduction. Yet the means by which the two genes have effected their changes are different.
Take Ectodysplasin first. In this case, a rare version of the gene exists at a low frequency in marine sticklebacks. Two copies of the rare version (you inherit one from each of your parents), and you have no plates. Two copies of the regular version, and you have all the plates. But if you have one of each, the sort of armor you have can vary. Some individuals will have all their plates. Others will have a sort of half-armor.
What seems to have happened is that when sticklebacks invaded each lake, some of the invaders carried this rare version with them. In the ocean, being without body armor is deadly: it makes you vulnerable to predators. But lakes don’t have the same dangers as the ocean — and armor is heavy and makes you less agile. Thus, in these new environments, being without body armor conferred a significant advantage, and so in lake after lake, the rare variant of the gene swept through the population.
Let’s turn now to the ghostly pelvis. Pelvic loss is much less common than armor loss. But if you find sticklebacks that lack a pelvis, you can bet that they came from large, shallow lakes where the water is soft, there are no large fish that might act as predators, and the vegetation is dense. Soft water has little calcium, and you need calcium to make the pelvic spines. Shallow lakes that are thick with weeds are home to predators like dragonflies, which enjoy having a stickleback for breakfast. And whereas the spines are a defense against being eaten by other fish — trout, say, or pike — and can actually induce the predator to spit out the stickleback instead of trying to swallow it, insect predators catch sticklebacks by grabbing the spines.
The difference between having a spiky pelvis or not is influenced by the expression of several genes, but as I said earlier, the main agent seems to be a gene called Pitx1. In sticklebacks with a proper pelvis, this gene is turned on at several different places in the developing fish, including the head, the pituitary and the spots on the side of the body where the pelvis should form. In those without, Pitx1 is switched on everywhere except the pelvic region, and the pelvis doesn’t grow.
There are a couple of interesting things about this discovery. The first is that the molecular basis of the change from pelvis to no pelvis does not involve a mutation to the protein-coding region of the Pitx1 gene itself. In other words, the protein made from the gene hasn’t changed. What has changed is the way the gene is expressed. This is in contrast to the sorts of mutations one often reads about as being involved in evolution, which typically involve changes to the protein itself.
A second interesting feature of the stickleback pelvis is that — unlike the armor plates — the loss is probably due to mutations having occurred independently in the different populations. What’s more, changes to the use of Pitx1 are also implicated in pelvic loss in nine-spine sticklebacks (Pungitius pungitius) — yet nine-spine and three-spine sticklebacks have been going their own evolutionary ways for at least 10 million years. Mice that have been genetically engineered to lack Pitx1 have a suite of abnormalities, including crushed faces and abnormal pituitaries, that cause them to die young. Intriguingly, they also have a reduced pelvis and hind limbs, and as with the sticklebacks, the reduction is lopsided and shows a greater loss on the right than on the left.
Which makes you wonder. Manatees — those charming marine mammals that cavort in the Florida keys and the West Indies — have also lost their hind legs. All that’s left of their pelvis is a lopsided bone, smaller on the right than on the left. Could Pitx1 have been involved here, too? So far, no one knows for sure. But I’d put money on it.
The idea that the same gene could be involved in mediating evolution of the same trait in creatures as distantly related as mammals and fish is exciting. And — to give one last example — while the relation between Pitx1 and the manatee’s missing hind legs is speculative rather than proven, there is much stronger evidence that a gene called Kit ligand is involved in mediating the evolution of light skin color in both sticklebacks and people.
This gene is by no means the only one that affects human skin color; nonetheless, genetic differences in the regulatory regions of this gene have a significant effect on how light or dark your skin will be, or whether you have blond hair. In sticklebacks, meanwhile, pale skin often evolves in freshwater — perhaps as a disguise — and the change again maps to Kit ligand, and involves alterations in the way Kit ligand is expressed in particular tissues.
Here, I’ve focused on one particular version of the evolutionist’s dream. But there are many others. In northeastern Mexico, for instance, a small fish known as Astyanax has, on a number of occasions, taken up residence in caves: populations of the fish have been found in more than 25 caves, some of them hundreds of miles apart. This system, too, is giving us a glimpse of the genetics of repeated evolution.
And I haven’t even mentioned the hundreds of actual experiments — bacteria or yeasts evolving for generations in the laboratory. Yet all these systems show the same thing: at the genetic level, evolution is, to a remarkable extent, a repeater.
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NOTES:
Gould discussed the role of contingency in evolution in a number of books and articles, but see especially Gould, S. J. 2000. “Wonderful Life.” Vintage.
Examples of similar traits appearing in similar environments are numerous, and can be found in any textbook on evolution; but for details of the hoatzin, see Kornegay, J. R., Schilling, J. W., and Wilson, A. C.. 1994. “Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin.” Molecular Biology and Evolution 11: 921-928.
For an excellent overview of evolution repeating itself at the genetic level, see Wood, T. E., Burke, J. M., and Rieseberg, L. H. 2005. “Parallel genotypic adaptation: when evolution repeats itself.” Genetica 123: 157-170.
For the genetics of armor inheritance, see Colosimo, P. F., Peichel, C. L., Nereng, K., Blackman, B. K., Shapiro, M. D., Schluter, D., and Kingsley, D. M. 2004. “The genetic architecture of parallel armor plate reduction in threespine sticklebacks.” PloS Biology 2: 635-641. For selective sweeps on Ectodysplasin, see Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villareal Jr, G., Dickson, M., Grimwood, J., Schmutz, J., Myers, R. M., Schluter, D., Kingsley, D. M. 2005. “Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.” Science 307: 1928-1933.
The forces that lead to loss of the pelvis in sticklebacks were described to me by Dr David Kingsley, of Stanford University, in a telephone conversation. For the role of Pitx1 in pelvic loss, see Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jonsson, B., Schulter, D., and Kingsley, D. M. 2004. “Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks.” Nature 428: 717-723. For the comparison between three-spine and nine-spine sticklebacks and the manatee, see Shapiro, J. D., Bell, M. A., and Kingsley, D. M. 2006. “Parallel genetic origins of pelvic reduction in vertebrates.” Proceedings of the National Academy of Sciences 103: 13753-13758.
For the evolution of pigmentation in sticklebacks and humans, see Miller, C. T., Beleza, S., Pollen, A. A., Schluter, D., Kittles, R. A., Shriver, M. D., and Kingsley, D. M. 2007. “cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans.” Cell 131: 1179-1189.
For more about the Mexican cave fish Astyanax, see Protas, M. E., Hersey, C., Kochanek, D., Zhou, Y., Wilkens, H., Jeffery, W. R., Zon, L. I., Borowsky, R., and Tabin, C. J. 2006. “Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism.” Nature Genetics 38: 107-111.
*About The Wild Side
Olivia Judson, an evolutionary biologist, is the author of “Dr. Tatiana’s Sex Advice to All Creation: The Definitive Guide to the Evolutionary Biology of Sex,” which was made into a three-part television program. Ms. Judson has been a reporter for The Economist and has written for a number of other publications, including Nature, The Financial Times, The Atlantic and Natural History. She is a research fellow in biology at Imperial College London.
