In our textbook, Evolution, my coauthor Carl Bergstrom and I start our chapter on evo-devo with a vignette of William Bateson. Young Bateson had announced to family and friends that he intended to be a naturalist. If he was not talented enough, he added, “I suppose I shall have to be a doctor.” He was more than talented enough, and became not just a natural historian, but a geneticist, entomologist, evolutionary biologist and developmental biologist.
While studying at Cambridge University, Bateson came to observe a number of bizarre abnormalities in insects and vertebrates, including instances, during the process of development, in which one body part had replaced another. Perhaps most famously were insects with legs that developed where antenna should (Figure 1).
Figure 1. The Antennapedia mutation in fruit flies leads to legs developing where antennae should be. From: https://en.wikipedia.org/wiki/Antennapedia#/media/File:Antennapedia2.jpg
Over time, Bateson began to see patterns. These oddities seemed to pop up in body parts that were repeated and/or segmented. He called them homeotic transformations, and with that, he arguably got the modern version of evo-devo up and running (though there were certainly others that had tinkered with these sorts of things earlier).
When he was more seasoned and grey, Bateson, looking back, wrote, “If I may throw out a word of counsel to beginners it is: Treasure your exceptions!… Exceptions are like the rough brickwork of a growing building which tells that there is more to come and shows where the next construction is to be.”
If all that the readers get from this first of my blogs is exposure to that quote, and if they pass it on to others – their mentors, students, friends and family – I will consider this post a success.
When I thought about Bateson’s words of wisdom, they made me think about an episode from my own past. Starting as a graduate student back in the late 1980s, I ran a long series of experiments on whether female guppies copy the mate choice of others in their populations, and if they do, how such cultural transmission of information might interact with the genetic transmission of traits associated with sexual selection in this species. I tried to cover all my bases. Not just running controls, but looking at every possible variable that might play a role in female mate-choice copying (age, resource abundance, threat of predation and so on). Across more than half a dozen different published experiments, one thing was clear – females were copying the mate choice of others. Virtually every experiment my colleagues and I ran found approximately 80% of the females tested copied the mate choice of others. And females were consistent about it.
I thought about those mate-copying females. A lot. Too much. I designed and implemented more experiments. Then twenty years after starting this work, something hit me out of the blue. I was overly focused on the mate copiers. I was ignoring the 20% of the females that were not copying the mate choice of others. My exceptions. What about them, I thought? I wonder if they consistently don’t copy? When I looked, I found they were consistent. They ignored culturally transmitted information from others. These lovely, little, strong-willed exceptions suggested a new line of inquiry. Perhaps the tendency to use culturally transmitted information was itself a heritable trait? Wouldn’t that be something? And so I started to look. The initial work was more of a pilot run than a full-blown experiment. It wasn’t clean and I don’t make too much of it, but there are hints that the tendency to use information acquired from others may be heritable. More work – much more — is needed, but maybe, just maybe it is.
Bateson knew what he was talking about – “Exceptions are like the rough brickwork of a growing building which tells that there is more to come and shows where the next construction is to be.”
 Bergstrom, C. T., and L. A. Dugatkin. 2016. Evolution. 2nd edition. W.W. Norton, New York.
 Cock, A., and D. Forsdyke. 2008. “Treasure Your Exceptions”: The Science and Life of William Bateson. Springer.
 Bateson, W. 1894. Materials for the Study of variation. Macmillan.
 Bateson, W. 1908. The Methods and Scope of Genetics. Cambridge University Press.
An interesting story. Perhaps the strong-willed female guppies were really making a random mate choice. But you say they consistently chose something ‘different’, so random may not be it.
Lee, your elegant essay brings me back to the days when you, Beren Robinson, Kris Coleman and Ted Dearstyne were grad students working with me,with adaptive individual differences within populations a major theme. Shyness and boldness. Body morphologies adapted to different habitats. And now tendencies to copy others. If I am not mistaken, models of social learning predict such a polymorphism, right? If everyone copies others, then the blind are leading the blind.
DSW, Thanks! I have such fond memories of those times! Indeed, shyness and boldness, body morphologies and, as you say, now copying. It is no coincidence that I started this work while under your wings. You made me think – about everything. I love you for that.
And yes, all models predict a polymorphism of copiers and noncopiers.
Your student forever, Lee