by Greg Mayer
At the Anolis Symposium at Fairchild Tropical Botanic Garden in March, one of the stars of the show was Colin Donihue of Harvard University, who gave a talk on the effect of last fall’s Hurricane Irma on Anolis scriptus, the endemic (and only native) anole of the Turks and Caicos. Colin and collaborators had chanced to visit and measure the morphology of the lizards just before the hurricane struck, and were able to return within weeks to see what had happened.
And something had happened. After Irma, the lizards had bigger toepads, longer arms, and shorter hind legs. The first two changes made sense—bigger toepads and longer arms are known to increase clinging ability in anoles– but the third seemed contrary to the first two. Longer legs would help them cling to the vegetation, and thus prevent them from being blown against the rocks or out to sea– so why did the ones with shorter legs survive better?
It was Colin’s exploration of this last question that made his talk one of the hits of the Symposium. In order to see the effect of Irma on the lizards, they used a garden leaf blower to simulate high winds, and recorded it all on video!
The video above is from Nature (not what Colin showed us in March), where the paper by Colin and colleagues will soon appear (already available online; there’s also a nice account of the field work by Colin at his website). What they have surmised, based on their leaf blower experiments, is that the hind legs of the lizards, once they’ve lost their grip on a perch, act as ‘sails’, catching the wind, and thus carrying the poor lizard away. “Yarr, ’tis an ill wind that blows a man out to sea.”
What surprised me was that the lizards held on to the last with their arms—I would have thought that they would grasp with all fours, and that the hind legs, having a greater toepad surface area, would give out last. Perhaps the wind caught their (larger) hind legs around the perch, and forced them off first, presaging the eventual cause of blowing away altogether. As expected during a round of directional selection, the variances of traits generally decreased. Also, the body condition of the lizards was good—they weren’t starving after the hurricane, supporting the idea that the differential mortality occurred at the time of the storm.
So, what we have here is a nice demonstration of natural selection, and a plausible, experimentally supported cause of the differential survival. But it is important to note that this is not a demonstration of evolution by natural selection, and the reason for that is interesting, and relates to the fact that evolutionary biologists use the term ‘natural selection’ in a number of contexts.
While natural selection is a major cause of evolution, as Fisher noted in the first sentence of his Genetical Theory of Natural Selection, “Natural Selection is not Evolution.” A short definition of natural selection, and one that I have used in classes and in print is that natural selection is “consistent differential survival and reproduction of heritable variants.” That this does not equate to evolution by natural selection can be readily seen in the case of heterozygote advantage, such as sickle cell hemoglobin in malarial environments. In such cases, the result of natural selection is that the genetic composition of the population doesn’t change—rather, it reaches an equilibrium, and stays there. There’s no evolution.
But there’s another sense in which natural selection does not imply evolution, and that is the sense used in quantitative genetics, and also very often in studies of changes in quantitative phenotypic traits (such as the study under discussion). Quantitative genetics derives from the work of plant and animal breeders (which was an important source of facts and inspiration for Darwin), and one of its key results has long been summarized in the ‘breeder’s equation‘:
Response to selection is equal to the selection differential times the heritability (h²)
What this means is that the evolutionary change due to natural selection depends on both how much the selected organisms differ from the mean of the population (the selection differential), and what proportion of that difference is passed on the offspring (the heritability). The heritability is where genetics comes in—the variants that are hereditary have a (non-zero) heritability.
The structure of the breeder’s equation flows naturally from how breeders work. First, they pick an animal to breed from, based on its possession of desirable variation (e.g., having larger breast muscles than average for a turkey). Then, they breed it. Finally, they check to see how much of the desirable variation is present in the offspring. If the offspring are exactly like the parent in the selected trait (i.e. desirable), then heritability is 100% or 1.0. If the offspring have only half the desirable advantage of the parent (say, being 4 ozs. larger than average, as opposed to 8 ozs. larger in the selected parents), then the heritability is 50% or .5. So in these two cases, selection leads to evolution. So where’s the problem?
The problem, or rather conceptual subtlety, is that the heritability may be 0—the offspring of the selected parents may not differ at all from the general mean of the population. Thus we can have selection, but no response to selection, and thus no evolution. So, although natural selection is often defined as I did above (consistent differential survival and reproduction of heritable variants), it is often the case that we can measure the differential survival before we know whether or not the variation is hereditary. And that’s what the breeder’s equation captures—the two-step nature of differential first, inheritance second.
The same two-step sequence of observation often applies in nature as well as on the farm or in the lab, and thus, ‘natural selection’ is often used in the sense of the differential, with the heritability evaluated separately (as it usually must be, since the observation of a phenotypic difference does not generally imply anything, one way or the other, about heritability).
As regards the measurement of selection differentials, Colin’s study has the very nice feature that the measurements were taken within the same generation; i.e. no reproduction had occurred—the second set of measurements were taken on lizards that had lived through the hurricane. This allows them to exclude certain other possible explanations—e.g., phenotypic plasticity—for the change in average morphology. A similar advantage accrued to the classic studies of natural selection in Darwin’s finches by the Grants and their collaborators. The Grants had the additional advantage that their birds were individually marked, so that the individual identities of surviving birds were known; on the Turks and Caicos, the same generation of adult lizards was sampled before and after the hurricane, and some individuals might indeed have been measured both times, but as the lizards were unmarked, individuals cannot be followed over time.
The next step for Colin is to return to the Turks and Caicos, to see if the morphological shifts persist into the next generation, thus supporting that evolution by natural selection has occurred—i.e., that the offspring resemble the selected (=surviving) parents. This could be complicated by the fact that, with the selective environmental force (Irma) now gone, there may be directional natural selection back toward the previous trait means. Thus, measuring the persistence of the observed change may be confounded by further changes occurring. As in the Darwin’s finches studies, a multi-year approach is called for.
The lizard traits that were studied are likely to be at least moderately heritable, as morphological features such as these are usually found to be so. There have been few studies of heritability in anoles, and there have been conflicting results. Using common garden experiments, Shane Campbell-Staton has found that critical thermal maximum, a physiological trait, is heritable in Anolis carolinensis; but Mike Logan has recently reported that heritability was low for other thermally-related traits in Anolis sagrei. Studies of the heritability of morphological traits in anoles should be a fruitful area of inquiry. One advantage the Grants had is that, using the information on pedigrees provided by individual marking, they measured the heritabilities of a number of quantitative phenotypic traits in the populations of Darwin’s finches they have studied.
Campbell-Staton, S.C., S.V. Edwards, and J B. Losos. 2016.Climate-mediated adaptation after mainland colonization of an ancestrally subtropical island lizard, Anolis carolinensis. Journal of Evolutionary Biology 29:2168-2180. link (links marked ‘link’ may not be to full text)
Donihue, C.M., A. Herrel, A.-C. Fabre, A. Kamath, A.J. Geneva, T.W. Schoener, J.J. Kolbe and J.B. Losos. 2018. Hurricane-induced selection on the morphology of an island lizard. Nature in press. link
Fisher, R.A. 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford. full text
Grant, P.R. and B.R. Grant. 2014. 40 Years of Evolution: Darwin’s Finches on Daphne Major Island. Princeton University Press, Princeton, New Jersey.
Logan, M.L., J.D. Curlis, A.L. Gilbert, D.B. Miles, A.K. Chung, J.W. McGlothlin, and R.M. Cox. 2018. Thermal physiology and thermoregulatory behaviour exhibit low heritability despite genetic divergence between lizard populations. Proceedings of the Royal Society B 285 (1878): 20180697. link
Mayer, G.C. and C.L. Craig. 2013. Theory of evolution. pp. 392-400 in S.A. Levin, ed. Encyclopedia of Biodiversity, 2nd ed., volume 3, Academic Press, Waltham, Mass.