The sequencing of the genome of the green anole (Anolis carolinensis) is a landmark in the age of genomics, and a highpoint in the annals of anole studies. It is the first complete genome sequence of a reptile, and a great step forward in the development of comparative genomics. Results are already coming in: Matthew Fujita, Scott Edwards and Chris Ponting have a paper in press in Genome Biology and Evolution, using an earlier release of the anole genome, showing that the green anole genome lacks the large guanine-cytosine rich regions (called isochores) that are characteristic of birds and mammals. Is this lack unique to the green anole, or a feature of some larger group? We don’t know, of course, because the green anole is the first non-avian/non-mammalian amniote to be sequenced, but it is a hint of new things to come. As Rich Glor put it in his commentary here at Anole Annals,
Fujita et al.’s work is a good example of the insight offered by comparative genome sequencing; as the number of available genomes expands, this work is sure to continue to challenge overly simplistic assumptions about genome architecture and evolution derived from biased sampling of the tree of life.
So why was an anole chosen to be the first reptile sequenced? The short answer is that, among a small group of candidate species of reptiles announced by the NIH in May of 2005, the response of the biological community favored the green anole over the garter snake. But the longer answer includes why the community preferred the green anole: it has long been the subject of diverse physiological, behavioral, ecological, and other studies (a “model” organism in the functional biology sense), and, more importantly, anoles in general have been favored and favorable materials for a diverse array of physiological, behavioral, ecological, evolutionary, and zoogeographic studies over many decades. The goal of this post is to review a bit of the rich history of anole studies to provide some background on why so many researchers have found anoles to be vastly interesting animals.
What’s in a name?
Among anolologists, anole is almost invariably pronounced “uh-nole” or “an-ole”, but the etymologically correct pronunciation is probably “a-no-lee”. The word “anolis” is a French West Indian word, still used on some French (or Creole) speaking islands, and on currently English-speaking islands which were previously French. In Haitian Creole, Wade Davis (1983) rendered the word as “zanolite” (he pronounced it with stresses on the first and third syllables), while Allsop (1996) gives it as “zandoli” on St. Lucia. (In both these forms, the ‘z’ is a common addition to Creole nouns, as in “zwazo”, from French “oiseau”.) It is most plausibly derived from a Carib word, but claims for an African origin have also been made. So, pretty much every anole biologist you meet (including me!) will be saying “anole” wrong.
Who are the anoles?
Part of what makes anoles interesting is their great species diversity. There are about 400 species, more or less equally divided between the West Indian islands and the mainland. Many anole workers (e.g. Losos, 2009) place all the species in a single genus, Anolis. Until the last decade or so, anoles were commonly divided into four genera, three of which (Chamaeleolis, Chamelinorops, and Phenacosaurus) had few species but were structurally distinctive (Chamelinorops, for example, having broad, plate-like processes on its vertebrae), while the fourth, Anolis, comprised all the remaining hundreds of species. Recent phylogenetic work has tended to show that the non-Anolis anoles, rather than being early branches of the anole phylogenetic tree, are actually nested well within Anolis (i.e. twigs, rather than trunks), and this has led to these genera being sunk within Anolis by most workers.
Although anoles can be fairly described as being, in general, diurnal, arboreal insectivores, they nevertheless present a great diversity of form, physiology, behavior, and ecology. Some species are terrestrial, while others are aquatic; most eat insects, but some eat fruit and small vertebrates; some live in rainforests, others in deserts; some sit and wait for their prey, others pursue it; and some live at the edges of tree crowns, some in the centers, and others at the base of the trunk. The most characteristic structural features of anoles are their dewlaps and subdigital toepads. The dewlap, a flap of skin on the throat most highly developed in males, is usually retracted, but is extended by cartilaginous rods in a variety of situations, especially courtship and territorial defense. The size, color, and pattern of movement varies greatly among species, and tends to be species-specific. The expanded pads on the bottom of anole toes are crossed by lamellar scales covered with microscopic setae that help anoles climb. Even these most characteristic features of anoles, their dewlaps and expanded subdigital lamellae, are lacking in some.
Why are anoles studied so much?
What is it about anoles that has made them such useful objects of study? It is because of their diversity, in several respects. I have already mentioned two features of this diversity—the great number of species, and their diversity of form, physiology, behavior and ecology. There is next their great diversity of individuals, the vast numbers in which they occur in certain localities, particularly in the West indies. Thomas Barbour (1884-1946), long time director of Harvard’s Museum of Comparative Zoology, wrote (1930):
Some species of Anolis simply swarm; no mainland species of this genus approach in abundance Anolis sagrei in Cuba or Anolis ordinatus in the Bahamas. At times these may be seen literally on every fence post, tree trunk and hut wall.
James D. “Skip” Lazell expressed this well in his remark that anoles aren’t really abundant unless you can catch ten without having to move your feet!
Perhaps most important are two intertwined aspects of their diversity: their diversity of geographic occurrence, and their diversity of lineage. They occur from Mexico through Central America and down into the South American mainland, and throughout the West Indian Archipelago into the southeastern United States, and on a few scattered islands in the eastern Pacific. This range provides a wealth of habitats and geographic circumstances, and, crucially a large series of islands, which have long been recognized as providing replicated circumstances for the investigation of ecological and evolutionary phenomena (Losos and Ricklefs, 2009) . Their diversity of lineage consists of the many subgroups within the anoles; these many subgroups, combined with their wide distribution, allow hypotheses based on particular lineages or locations to be tested by the “natural experiments” of other lineages and other locations (especially islands). Overall, the rich diversity of anoles allows for the recognition of repeated patterns and the testing of evolutionary hypotheses. It is through this style of investigation that the most striking evolutionary aspect of anole biology, the convergence of community structure, involving convergence in ecology, morphology, and behavior, of the anoles of the Greater Antilles (Cuba, Hispaniola, Puerto Rico, Jamaica). (For a somewhat longer take on why anoles are interesting, see Jonathan Losos and Christopher Schneider‘s 2009 primer in Current Biology.)
The discovery of anoles
Anoles were of course known to the Indian inhabitants of the Americas, as reflected in the probably Carib origin of the word “anolis” itself. They became known to Western science beginning in the colonial period. Hans Sloane (1661-1753), whose collections founded the British Museum, noted and illustrated two species of anoles in his account of Jamaican natural history. The artist and scientist Mark Catesby (1683-1749), during his explorations in America and the West Indies, painted both the North American green anole and a Jamaican one. Although these early naturalists recognized multiple species of anoles, anoles themselves were not recognized as a genus distinct from other lizards until 1802, when F.M. Daudin (1774-1804) named the new genus Anolis, attesting to its Carib origin, in his monumental Histoire naturelle generale et particuliere des reptiles.
Throughout the 19th century, new species were described from throughout the range of anoles, with A.M.C. Dumeril (1774-1860) and G. Bibron (1806-1848) in France, and G.A. Boulenger (1858-1937) in England, being prominent contributors and synthesizers. American scientists became more active later in the century, notably E.D. Cope (1840-1897) of dinosaur hunting fame, and Samuel Garman (1843-1927) at the Museum of Comparative Zoology. Boulenger’s monumental Catalogue of 1885, summarizing the state of knowledge near the close of the 19th century, recognized 112 species of anoles in five genera (all but six in the genus Anolis).
In the 20th century, Barbour took up where Garman had left off and made the Museum of Comparative Zoology (MCZ) a center of anole studies. Barbour was the first of the great describers to be a field worker, and to know the anoles in life. This was crucial for developing an understanding of anole diversity, as workers using museum specimens alone could not always figure out what was the true nature of variation within and among anole species. This knowledge of the animals in life led Barbour to recognize more species than his purely museum-working predecessors. He wrote (1932):
It seems, I confess, to be a wicked and sinful affection to describe more Anoles.
In his compilations of 1930 and 1934, he recorded 188 species of anoles. Four years after Barbour’s death, Ernest E. Williams came to the MCZ, becoming curator of reptiles in 1957. When he arrived, he was most interested in turtles, but field work in the West Indies excited his interest in anoles; he published his first paper on them, with Max Hecht, in 1955. They soon came to dominate his research program, and a large group of students, colleagues, and collaborators gathered around him made the MCZ the center of anole studies for four decades. Williams’ own work was informed by an even closer acquaintance with anoles in life and the field than Barbour had. Although he made numerous contributions to the description of anole diversity, his greatest achievements were in bringing together workers of diverse interests in anole ecology, behavior, physiology, zoogeography, and evolution, and in synthesizing all the diverse strands of anole biology, developing the concepts of ecomorphs and community convergence.
Ecomorphs and community convergence
Leonhard Stejneger (1851-1943), the great herpetological systematist of the U.S. National Museum, was perhaps the first to begin thinking about the ecological structure of anole communities. There were clearly many species: how did they all live together in the same place? Stejneger (1904), based on his field investigations in Puerto Rico, called attention to the vertical zonation of the distribution of anoles. Some were confined to the lowlands, some extended to mid elevations, while others were more characteristic of high elevations. K.P. Schmidt (1928), also working in Puerto Rico, realized that the distinctions among species were not altitudinal, but climatic or thermal: some species preferred sun, others shade, but where the two conditions were juxtaposed, anoles might be found in close proximity regardless of altitude.
Bruce Collette (1961) noted “Correlations between ecology and morphology in anoline lizards from Havana, Cuba and southern Florida,” establishing that ecological differences among species were reflected in the species’ morphology. A. Stanley Rand (1932-2005) pursued this further in the context of the entire Puerto Rican anole fauna (1964), coining a series of terms for the characteristic position of a species within the structure of the vegetation (e.g. “trunk ground”, “trunk crown”). Rand established that local communities of anoles accommodated increased species richness in two ways: some differed in position in the vegetation (structural habitat), while others, sharing the same structural habitat, differed in their thermal and insolation preferences (climatic habitat). Thomas Schoener, and others, extended these studies of habitat partitioning in anoles to other islands, where similar patterns were evident.
Williams synthesized these strands in his 1972 “On the Origin of Faunas,” coining in it the term “ecomorph” for
Species with the same structural habitat/niche, similar in morphology and behavior, but not necessarily close phyletically.
And, crucially, the same ecomorphs occurred across the Greater Antilles, displaying the pattern of community-wide convergence that is perhaps the most distinctive aspect of anole biology. Barbour and Schmidt had thought that species of the same ecomorph from different islandswere phyletically related; but, in fact, their similarities are convergent– similar responses to similar conditions of existence. Williams expanded his ecomorph analysis in an important 1983 paper. In making his synthesis, Williams drew on not just his and Rand’s work, but that of many contributors, including, to name a few, Richard Etheridge, Thomas Schoener, George Gorman, Ray Huey, Joan Roughgarden, and Paul Hertz.
Much subsequent ecological, morphological, and phylogenetic work has been directed toward elucidating the concepts of ecomorphs and community convergence, and Jonathan Losos’s (2009) Lizards in an Evolutionary Tree is largely an explication and exploration of these concepts, finding that, indeed, the ecomorphs and community convergence are real phenomena that suggest a greater deterministic aspect to evolution than some might have expected.
In tracing the 19th century work on describing species, through to community convergence, I have followed an important, but by no means the only, strand of research within anole studies. Anoles have been the subject of studies on the behavioral and physiological control of reproduction, the effects of competition on community structure, the comparative demography of island and mainland populations, the correlation of habitat use with thermal physiology, the ecological factors promoting colonization, the evolutionary consequences of such colonization, historical zoogeography, the structuring of populations by territories, and the signaling behaviors used to maintain these territories, to mention but a small sample of the problems for which anoles have been found useful study organisms. They range from questions of the proximate causes of individual behavior and physiology, to the ultimate causes of adaptive radiation. Indeed, there is scarcely a problem in organismic, evolutionary, and, now, genomic biology to the solution of which anoles have not, or will not, contribute. Not all threads can be mentioned, but there are a few about which more must be said.
First, the work of Albert Schwartz (1923-1992) must be mentioned. Schwartz was a tireless field worker in the West Indies, who, while interested in all reptiles and amphibians, paid close attention to anoles. In particular he elucidated patterns of intra- and interspecific variation in many species groups, naming many species and subspecies in the process. Noted briefly earlier in its connection to community structure, thermal physiology has been an important thread of research on anoles in its own right, and some of the chief workers (e.g. Huey, Hertz) have been mentioned.
Alongside the work done in the West Indies, there has been a parallel track of work on mainland, especially Central American, anoles, led by such luminaries as Henry Fitch (1909-2009) and Jay M. Savage. Anoles do not form as conspicuous an element of the mainland fauna as they do on the islands, but there are many species, and much has been learned about their ecology and habits; a currently active area of research is comparing the mainland and island forms, an endeavor pioneered by Robin Andrews (1979). The Central American work has been largely summarized in Jay Savage’s magnificent The Amphibians and Reptiles of Costa Rica. Central American workers have tended to favor a more split generic classification, and often recognize several anole genera, including Norops, which is especially species rich in Central America.
Another rich research tradition in anole studies is that of behavioral and physiological studies. Some of these trace to Barbour and the Harvard field station in Cuba, where color change was an object of study, but an important impetus was G.K. Noble’s work at the American Museum (Greenberg and Noble, 1944). Important contributions have been made by Gordon Burghardt and David Crews.
And finally, phylogenetic studies on the relationships of the anoles have been a crucial component of anole studies in general, and community convergence in particular. Richard Etheridge pioneered studies of anole relationships in his now classic thesis, “The relationships of the anoles.” Recent phylogenetic work, now including molecular data, have tested and extended the estimate of phylogeny made by Etheridge. The work of Kirsten Nicholson (2002; Nicholson et al. 2005) and Steve Poe (2004) should be especially noted in this regard.
All of these approaches to anole biology are usefully thought of as threads within a single fabric, because there is frequent reciprocal interaction and illumination provided by the various strands to one another.
Under the editorship of E.E. Williams, three editions of the Anolis Newsletter were produced from 1972 to 1978. After a fallow period, Losos and the present author, undergraduate and graduate students of Williams, respectively, revived the series in 1991, and Losos has continued co-editing the series, and there have now been three issued, each produced in conjunction with a symposium on anole biology, the latest held at the MCZ in 2009. The talks at this symposium reflect the vital state of anole studies today, now expanding into evolutionary developmental biology, conservation (under the leadership of Ross Kiester and Luke Mahler), and, the occasion for this review, genomics. With Losos now the curator of reptiles at the MCZ, that museum is once more a center of anole studies, with his students and collaborators, many now running their own labs, contributing to a new flowering of anolology.
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