Hangin’ on in the wind: Natural selection, hurricanes, and lizards

by Greg Mayer

Colin Donihue at the Anolis Symposium, 17 March 2018.

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‘:

R=sh²; or

Response to selection is equal to the selection differential times the heritability ()

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.

27 Comments

  1. GBJames
    Posted July 27, 2018 at 3:38 pm | Permalink

    sub

  2. freiner
    Posted July 27, 2018 at 3:40 pm | Permalink

    Thank you very much for this, Greg — I especially appreciate these explanations of scientific topics that appear here. And while I know I’ll have to go over the subtleties of the natural selection, evolution, and heritability section again to get it firmer in mind, I really appreciate the way your exposition goes from the particular case of the windblown lizards, to the general concepts and then back to the lizards (and Grants’ finches)to illustrate those concepts. The last paragraphs seemed especially helpful to me (provided, of course that I’m not completely misunderstanding the whole thing, anyway).
    Again, thanks very much.

    • Randall Schenck
      Posted July 27, 2018 at 3:53 pm | Permalink

      I would have said the same but you beat me to it. Very interesting and a little confusing at the same time. A great place to study the lizards would be Typhoon Alley during season. Go to Okinawa from July to December.

      • Angel
        Posted July 27, 2018 at 4:39 pm | Permalink

        Ditto!!

      • Posted July 27, 2018 at 4:47 pm | Permalink

        I’m with freiner, it’s a puzzle well worth dissecting for a lay person like me.

  3. Barry Lyons
    Posted July 27, 2018 at 3:53 pm | Permalink

    Hey, Greg. I occasionally send emails to Jerry when there are things that need to be corrected (he welcomes these notes). I just sent an email to him regarding this piece. It mainly has to do with your distracting use of hyphens when they should be em dashes. For example, that should be an em dash with no spaces in the headline. Right now you’ve got that weird hyphen space thing happening.

    Ask Jerry to forward the email to you! Or, you can contact me directly.

    • Posted July 27, 2018 at 4:02 pm | Permalink

      When I use double hyphens (which word processors often convert to dashes), the WordPress editor converts them to single hyphens– sorry!

      GCM

  4. BJ
    Posted July 27, 2018 at 4:31 pm | Permalink

    That equation is very interesting. I had no idea equations have been worked out for such things.

  5. Posted July 27, 2018 at 4:57 pm | Permalink

    Fascinating – both the Anole work itself and your analysis. I’ve learnt a lot from this.

  6. Mark Sturtevant
    Posted July 27, 2018 at 5:20 pm | Permalink

    Great stuff! I suspect that a reason for why the hind legs loose their grip first is b/c the tail is at that end. The flying tail should create a powerful pulling force that causes the hind legs to also be pulled away.

    • infiniteimprobabilit
      Posted July 27, 2018 at 7:28 pm | Permalink

      I’d agree with that hypothesis. And also, it just seems more ‘natural’ to try to stay head-into-wind – notice how the lizards manage to hang on with their front feet for quite a while. In that position they’re probably experiencing less total wind force on their bodies than they did in the all-four-feet-hanging-on, broadside** position.

      If they let go with their front legs first, they would then be doubled back in an unnatural shape but still broadside** to the wind, so I imagine they would lose their hind feet grip very quickly. They probably know this, which is why they devote most effort to their front-feet grip.

      ** Well, not really broadside, more like broad-bottom, but I can’t think of a succinct word for it.

      cr

  7. Posted July 27, 2018 at 5:32 pm | Permalink

    Gould would’ve had a field day with this data, constructing a straw man of ‘Hurricane-ists’ to bash, forcing the rest of the scientific community to divert time & energy to refute him.

    I do not miss him.

  8. urthmothr
    Posted July 27, 2018 at 5:36 pm | Permalink

    This is why I want to read this blog! Some of the jargon went over my head, but it makes sense to me that survival of one generation does not necessarily mean the traits will be passed on to the next generation – right?

    • Posted July 27, 2018 at 7:23 pm | Permalink

      Right. They are passed on in proportion to the heritability.

      GCM

    • Michael Fisher
      Posted July 27, 2018 at 8:01 pm | Permalink

      That’s right. Here’s my very, very amateur explanation – others please improve!

      If you [or nature] went on sprees of culling wild long-legged anoles it doesn’t follow that the short-legged anole becomes the standard lizard in future populations.

      There are all sorts of reasons why a selected short legged trait may not ‘breed true’ such as…

      Long legs are advantageous in
      mate selection or
      foraging or
      escaping predators

      Long legs may link to a whole system of other traits that are advantageous [eg long-legged anoles are brainier or better at smelling]

      The genetics of short legs may not be a simple gene or set of simple genes [there isn’t an allele for it] & thus it doesn’t breed true. As an example the traits that make some animals ‘domesticable’ can’t always be selected for – e.g. attempts to farm & produce a tamer zebra are a good way to get your head kicked in & similarly ‘guard leopards’ are not the way to go. Producing heritable behavioural changes in an animal is luckily, very, very hard – a good thing or imagine the consequences.

      • Posted July 28, 2018 at 9:08 am | Permalink

        The reasons you give are indeed plausible reasons why selection may be ineffective in producing a response. The reasons fall into two distinct classes, though. The reasons that invoke selection for some other feature (foraging, smelling, etc.) prevent selection from being effective not due to lack of heritability, but due to the existence of other, countervailing, selective forces. The last reason, in which selection doesn’t work because there are no genes for the trait which vary, would be lack of heritability. Only in the latter case would we say that the selected animals do not breed true.

        GCM

        • Michael Fisher
          Posted July 28, 2018 at 9:28 am | Permalink

          Thank you GCM – I though I’d take the risk of being wrong 🙂

  9. Posted July 27, 2018 at 5:47 pm | Permalink

    I also thank you very much for this article that informs this particular non-scientist in clearly constructed non-arcane language. More!

  10. CAS
    Posted July 27, 2018 at 6:16 pm | Permalink

    Nice post! I had not thought about the heritability factor in evolution, though it makes perfect sense. The h squared is also obvious when you think about it. Thanks

  11. ThyroidPlanet
    Posted July 27, 2018 at 6:17 pm | Permalink

    Sub

  12. Mark R.
    Posted July 27, 2018 at 7:49 pm | Permalink

    When I read the title, I thought this post might be about how lizards (and other ‘largish’ animals) can be carried off by hurricanes and land on distant lands and multiply.

    That would have been cool. But this post was even more engaging and interesting. Thanks.

  13. Adam Felton
    Posted July 28, 2018 at 2:55 am | Permalink

    What struck me while reading this was the similarity between their approach to dealing with high winds, and the depower / emergency depower systems used in kitesurfing. The more tension on the back lines of a kite, the more the back of the kite is pulled downwards, which increases the power of the kite (simple drawing in the link below). The point being that just as the fastest way for us to depower our kites is to drop the tension in the back lines, it seems these lizards are likewise dropping wind resistance by releasing the grip on their back legs.
    https://kiteboardschool.nl/en/theory-kitesurfing/how-to-control-a-4-or-5-line-kite/

  14. Hempenstein
    Posted July 28, 2018 at 7:52 am | Permalink

    Now I’m semantically confused.

    With sickle-cell, that Glu –> Val substitution at position 6 in the beta chain must’ve come from a founder mutation that was advantageous according to the now well-known explanation, but the homozygous state is also equally well-known to be deleterious. So heterozygous for HbS is where the advantage lies. Surely the precursor state was no HbS, so isn’t the existence of HbS an example both of selection and evolution? Or would HbB have to be completely replaced by HbS to qualify as evolution?

    • Posted July 28, 2018 at 8:59 am | Permalink

      When HbS is introduced into a population in a malarial environment (by either immigration or mutation), it will increase in frequency, until it reaches its equilibrium. (This frequency is the ratio of the fitness decrement of the HbA homozygote to the sum of the fitness decrements of both homozygotes.) That would be evolution by natural selection. At equilibrium, natural selection continues–there are consistent differences in survival and reproduction of the hereditary variants–but there’s no evolution. Of course, if the environment changes (e.g., malaria is suppressed), then the fitnesses might well change, and then evolution by natural selection might occur.

      GCM

      • Hempenstein
        Posted July 28, 2018 at 11:51 am | Permalink

        OK, thx, I thought you were saying that the first part – from introduction to steady state – was selection but not evolution.

        Separately, HbS must have arisen from a spontaneous mutation, with incorporation through selection likely not long after the origin of the malarial parasite’s ability to target humans or predecessors. Myriads of Hb variants have been described, but are you aware of any studies on the prevalence of Hb (or any other protein or enzyme) variant genes of neutral or previously unrecognized significance in the general population from DNA sequencing studies of large numbers of individuals? It would seem that that would be fairly easy to do, just to get an idea of existing general mutation rates, but I’ve never heard of any such studies.

  15. Posted July 30, 2018 at 7:15 am | Permalink

    I suggest that the hind limbs are pulled from the support first due to the huge sail area of the tail, which wrenches them off quickly.

    Then the lizard sort of forms a “banner” or streamer which shows a smaller cross-section to the wind.

  16. Posted August 9, 2018 at 1:23 pm | Permalink

    Archosaurs may have evolved in a windy climate and may have clunged with their hindlegs to have them grown so out of proportion! (Sorry, I am now struggling with some archosaurs extinct and modern and couldn’t resist a little joke.)


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