Why Evolution is True is a blog written by Jerry Coyne, centered on evolution and biology but also dealing with diverse topics like politics, culture, and cats.
A correspondent who visited Hawaii in December, 2019, sends in the following from Haleiwa, on the north shore of Oahu. I believe these are from Waimea Valley, where there is a botanical garden.
First up is a Hawaiian Gallinule, Gallinula galeata sandvicensis. This is an endemic subspecies of a widespread species. On remote islands, land and freshwater birds, like the gallinule, have higher levels of endemism than sea or shore birds. The latter are accustomed to flying great distances, and thus have higher levels of interbreeding among populations, which retards differentiation.
Gallinula galeata sandvicensis, Haleiwa, Oahu, Hawaii, December 2019
Remote islands are also very vulnerable to establishment by introduced species, and here’s a combo. That’s a giant day gecko, Phelsuma madagascariensis, from Madagascar, on top of a sign for a neotropical orchid, Myrmecophila tibicinis. The orchid has a mutualistic relationship with ants. (Its generic name means “ant lover”.) The gecko, brought in with the pet trade, is well established in Oahu. The orchid may not be established, but just a specimen in the botanical garden.
Phelsuma madagascariensis, Haleiwa, Oahu, Hawaii, December 2019
And finally, high up on a palm, is an anole. This is probably Anolis sagrei. This species was introduced from the U.S. mainland. It was introduced to the U.S. mainland from Cuba. So it’s on the second leg of its travels!
Anolis sagrei, Haleiwa, Oahu, Hawaii, December 2019
A corespondent from Florida sends the following photos from Fort Myers. First up, a giant or marine or cane toad (Bufo marinus) that is living under a beehive. In this first photo, you can see that the variegated coloring is fairly cryptic against the leaf litter background.
Bufo marinus, Fort Myers, Florida, 3 November 2019.
Getting a little closer, a few things are notable. First, from the body shape (which I am tempted to describe as “jowly”, despite the fact that it’s her abdomen that’s distended), I can tell this is a fairly large individual. My correspondent, unprompted, stated it was about 15 cm long, which sounds about right for a big one. The biggest ones are in the Guianas, where they get to about 25 cm.
Bufo marinus, Fort Myers, Florida, 3 November 2019.
Second, as the preceding sentence implies, she is a female. Females are larger, and retain the brown/black/tan blotching and spotting of the juveniles. This coloration is typical of many species of toads at all ages, and in both sexes. Adult males of marinus are distinctive in becoming uni-colored in some olive drab-like shade (see a male here). And finally, note the large parotoid gland extending from above the arm towards the eye. This gland can secrete a milky toxin, which is part of the toad’s defenses.
These toads, native from the lower Rio Grande down into South America, have been introduced into Florida, and to many other places, including islands in the West Indies and the Pacific, and Australia, where they picked up the moniker “cane toad”, which is rapidly becoming the vernacular name throughout the English-speaking world. I always called them “marine toads”, from their scientific name. They are not marine (although they can be found in brackish situations), and it’s just a coincidence that U.S. Marines have landed in so many of the places that the toads were introduced (e.g. Hispaniola, Puerto Rico, New Guinea, the Philippines, etc.).
Next up a brown anole (Anolis sagrei). This species and its close relatives are widespread in the West Indies, including Cuba and the Bahamas, and have, like the toad, been introduced in to Florida and many other places. The green anole, Anolis carolinensis, native to Florida, is now perhaps less abundant than prior to the arrival of sagrei, but the native is not threatened by the invader. In Cuba, the two species (or close relatives) live side by side, with the green anole higher in the vegetation, the brown anole lower, and this ecological situation has now been replicated in Florida; the two species were “preadapted” for coexistence by their long joint history in Cuba.
Anolis sagrei, Fort Myers, Florida, 31 October 2019.
Last but not least, something higher on the scala naturae, an anhinga, Anhinga anhinga, drying its feathers. These diving birds, which stab their piscine prey with their bills, do not have waterproof feathers.
Anhinga anhinga, Fort Myers, Florida, 31 October 2019.
Although Jerry has been receiving fresh wildlife photos from readers, I thought I’d chip in with a few of mine and my correspondents from San Diego. We begin with a wild inhabitant of the San Diego Zoo, the introduced green anole, Anolis carolinensis. Native to the southeastern United States, they became established at the Zoo many years ago, probably by escapees.
Anolis carolinensis, female, in West Indian rock iguana exhibit at San Diego Zoo, September 1, 2018.
They are now scattered through several southern California counties, although it’s not clear if they are established and reproducing in all locations from which they have been reported. Another anole, the brown anole, Anolis sagrei, is also in southern California. Greg Pauly, of the LA County Museum, is studying these very interesting introductions. Much can be learned about ecological and evolutionary processes from study of populations confronted by, and confronting, new biotic and physical environments for the first time.
Next we have a western fence lizard, Sceloporus occidentalis, a native species, from Point Loma, San Diego.
Sceloporus occidentalis, Point Loma, San Diego, California, March 22, 2019.
Old Point Loma Lighthouse, San Diego, March 22, 2019.
We’ll finish off with two inhabitants of Murphy Canyon, a suburban neighborhood within the city of San Diego. First a snail on the sidewalk– I’ve no clue on the ID.
Snail, Murphy Canyon, San Diego, March 22, 2019.
And last, but certainly not least– in fact I think it’s the best in this set– a southern alligator lizard, Elgaria multicarinata. It was just strolling along through a lawn.
Southern alligator lizard (Elgaria multicarinata), Murphy Canyon, San Diego, California, March 15, 2019.
The lizard, of course, is not breathing water; rather, it is breathing air that is trapped around it’s body, which it then visibly exhales in a bubble, and then “rebreathes”. I could not tell from how far around the body air was being drawn to the nostrils, but it seems to include at least the head. The longest she has seen them stay down is 16 minutes. It has long been noticed that air can be trapped around an anole’s body when it’s placed in water, and I’ve wondered whether that air might enable an anole to float longer or higher in the water (perhaps aiding “occasional transport”). But Lindsey has placed these casual observations on a much firmer basis, and recorded, for the first time to my knowledge, that the lizards are breathing; that’s something I never suspected. She proposes a “scuba tank” explanation for the behavior– that the lizard is getting oxygen from the recycled air.
Many species of anoles, both on the main and on the islands, are semiaquatic; aquaticus occurs in Costa Rica and Panama, and the ones filmed were in southern Costa Rica. These semiaquatic anoles inhabit the vegetation alongside streams, and jump into the water when approached. As Lindsey notes, it is an effective anti-predator behavior. Many times I have seen anoles of these species flee from my approach into the water; I think I may once have seen aquaticus myself, in southern Costa Rica.
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!
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 (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. Naturein 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.
I’ve previously noted a recent paper about fruit eating lizards that wind up as bird fodder. Fortunately, the cases I’m about to relate here don’t end tragically in an avian maw. The lizards that I study, anoles, are primarily insectivorous, but eat a modest amount of meat and fruit as well. I’ve seen the Jamaican Anolis opalinus eat runny banana (the banana had been sliced and left out to attract birds), Puerto Rican Anolis cristatellus pursue round, red fruits (pursue because the fruit kept rolling away as the lizard tried to grab it), and Virgin Island A. cristatellus defecate purplish feces with small black seeds (perhaps from Turk’s cap cactus, Melocactus).
Anoles are the neatest of all animals, and if you don’t believe me, take it up with my friend here– she’ll set you right!
An agitated anole
But rather than tangle with her, you can convince yourself by reading my friend and colleague Jonathan Losos’s new book, Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles, which was published at the end of July. Anoles are a group of 300 or so species found in the southeastern US, Central and South America, and throughout the West Indies. Although they may be fairly described as, on average, diurnal, arboreal insectivores, they exhibit a great range in behavior, structure, and ecology: some are aquatic, some terrestrial, some engage in carnivory and frugivory, and some live in deserts, and others in rainforests. They are perhaps most remarkable for the evolution of convergent multi-species communities on the islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, Puerto Rico). This is not just the usual (but still remarkable) convergence in features between, say sabertoothed tigers and sabertoothed marsupial tigers, or dolphins and icthyosaurs. It is convergence in the whole set of species living together in a community. Thus each of the four Greater Antilles has a large, green anole that lives in the canopy of trees, a medium green anole with short legs that lives in the tree crown and on the trunk, a whitish, very short-legged anole which lives on twigs in the crown, and a medium brown anole with long legs that lives on the trunks and bases of trees; and there are several other inter-island correspondences among species. The corresponding species, however, are not, in general, related to one another; rather, on each island a more or less independent adaptive radiation has produced similar ecological sets of species. There are lots of other neat things about anoles, but I’ll leave you to read about them in Jon’s book, which you need to add to your summer reading lists.
Many anoles are marvelously colored, and the book is beautifully illustrated and well-produced. My pictures here are of anoles from my trip earlier this summer to Estacion Biologica La Suerte, Costa Rica, where I taught a field course in tropical herpetology.
Anolis capito, Estacion Biologica La Suerte, Costa RicaAnolis oxylophus, Estacion Biologica La Suerte, Costa Rica
The terrifyingly threatening predator on the left (which closely resembles my first cat, Kitty Cat) appears ready to enjoy a quick snack at the expense of the anole on the right (which closely resembles my first lizards, Gilbert and Ignatius). What’s that, you say? An anole? Not a gecko?
(via icanhascheezburger.com)
Our endangered friend is not a gecko, a type of lizard that has been popularized by commercial ventures ranging from Hawaiian tourism to insurance, but rather an anole, a member of a quite distinct family of lizards. In particular, it is Anolis carolinensis, the green or Carolina anole. They are native to the southeastern United States, and have long been popular in the pet trade. Jamaican acquaintances have told me of how the arrival of a house cat can clear out the anoles in their garden, but I don’t greatly fear for our friend here: I’ve seen an anole on Grand Cayman, faced in a similar manner by a predatory bird, dash between the bird’s legs and make good its escape.
Anoles are the neatest of all lizards, with about 300 species ranging from the US to South America and all over the West Indies, and showing a great diversity of morphology, ecology, and behavior. One of the neat things about anoles is that they are great natural colonizers. The species group to which Anolis carolinensis belongs originated on Cuba, and has colonized the southern US, the Bahamas, Little Cayman, Navassa, and Half Moon Cay and the Bay Islands off the coast of Central America. Through human introduction, Anolis carolinensis is now widespread on islands in the Pacific, including Hawaii. The populations on the West Indian islands are variously considered endemic species or subspecies, and are a good example of geographic speciation, discussed by Jerry in chapter 7 of WEIT.
Studies of the colonizing abilities of anoles, and many other neat things about them, were pioneered by E.E. Williams. Anole studies have been carried to new levels by my friend and colleague Jonathan Losos, and he has a book on anoles coming out this summer, which everyone should read to find out more about their evolution, ecology, and biogeography.
some engage in carnivory and frugivory, and some live in deserts, and others in rainforests. They are perhaps most remarkable for the evolution of convergent multi-species communities on the islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, Puerto Rico). This is not just the usual (but still remarkable) convergence in features between, say sabertoothed tigers and sabertoothed marsupial tigers, or dolphins and icthyosaurs. It is convergence in the whole set of species living together in a community. Thus each of the four Greater Antilles has a large, green anole that lives in the canopy of trees, a medium green anole with short legs that lives in the tree crown and on the trunk, a whitish, very short-legged anole which lives on twigs in the crown, and a medium brown anole with long legs that lives on the trunks and bases of trees; and there are several other inter-island correspondences among species. The corresponding species, however, are not, in general, related to one another; rather, on each island a more or less independent adaptive radiation has produced similar ecological sets of species. There are lots of other neat things about anoles, but I’ll leave you to read about them in Jon’s book, which you need to add to your summer reading lists.
