Many thanks to Luke, Melissa and everyone else involved in organizing this interesting and valuable blog. I have just learned about it, and am stimulated to offer some comments that seem extensive enough to merit a separate posting.
To begin, I discuss Jonathan Losos’ comparison of the Galapagos finch radiation with the Antillean anole radiation, as reported in his post of Dec. 19. In the book chapter he refers to, Jonathan offers a beautifully written summary of the biology of these radiations. On p. 325 he concludes that “Overall, adaptive radiation in Darwin’s finches and Greater Antillean anoles has occurred in very much the same way. Interspecific competition appears to have been the driving force leading to resource partitioning and subsequently adaptation to different niches, and speciation is probably primarily allopatric and may be promoted as an incidental consequence of adaptation to different environments. Differences exist as well, such as the extent of hybridization and of independent evolution on different islands; many of these differences probably result because the radiations differ in age and aspects of natural history.” While I tend to agree with this conclusion, I would develop a alternative list of differences and similarities between Galapagos finches and Caribbean anoles.
Specifically, I agree that for both finches and anoles interspecific competition is connected somehow with resource partitioning, that speciation is allopatric, and that speciation is an incidental consequence of adaptation to different environments. And I agree that in both groups morphological differences nicely correspond to differences in habitat and behavior.
From my perspective though, I would not, at least initially, compare the very diverse Greater Antillean anoles with all the Galapagos finches combined. To do so invites viewing the anole ecomorphs as a counterpart somehow to the distinct genera of finches that occupy ground and trees, Geospiza and Camarhynchus respectively, as well as other finch genera in distinct habitats. We would need to consider rather carefully whether, and in what sense, to view the trunk-ground, trunk, crown, twig and giants as distinct genera corresponding to what is apparently done with the Galapagos finches. Rather, I would compare the less diverse Lesser Antillean anoles with each particular finch genus separately. The number of species on a Lesser Antillean island is similar to the number of species in each finch genus on a Galapagos island. For example, the number of anoles per island in the Lesser Antilles is one or two, and the number for the Geospiza (ground) finches is one, two, or three.
On p. 315 Jonathan mentions that “The primary difference is the extent of evolutionary independence between islands. In the Galapagos, the theater of evolution has been the entire archipelago, and adaptive radiation has not proceeded independently on different islands. In other words, similar niches on different islands are occupied by closely related taxa. By contrast, in anoles, adaptive radiation has occurred independently on each island in the Greater Antilles.” Here I demur. In the Northern Lesser Antilles the wattsi group supplies a trunk-ground anole and the bimaculatus group supplies an arboreal anole for all the islands. In the Southern Lesser Antilles, only on St Vincent are the two endemic anoles each other’s closest relative, whereas on Grenada the larger lizard is most closely related to the larger lizard on St Vincent. So, in both the Galapagos and Lesser Antilles, the archipelago is, for the most part, the theater of evolution; that is, the radiations are inter-island not intra-island, and both the Galapagos finches and Lesser Antillean anoles are similar in this regard, not different.
Despite this similarity in the geographic extent of the evolutionary theater, the Galapagos finches and Lesser Antilles anoles have not acted out the same script. The difference in scripts is evident in the absence of exceptions to the biogeographic “size rules” in Galapagos finches in contrast with the Lesser Antillean anoles. As David Lack’s famous diagram of the histograms of beak depths from ten islands in the Galapagos for G. fuliginosa, G. fortis, and G. magnirostris illustrated, every finch species alone on an island has a certain beak depth whereas finch species coexisting with another finch species have beak depths equally displaced above and below the beak depth of a solitary finch species.
As Ernest Williams was the first to point out, the analogous size rules for anoles in the Lesser Antilles are not so straight forward and instead have exceptions, namely, a solitary anole that is too big on Marie Galante, and two anoles on St. Martin, the larger of which is the solitary size. The smaller anole on St. Martin has a restricted distribution, occurring only in the central hills, and this smaller species on Anguilla, from the same bank as St. Martin, has already become extinct in historical times. Ernest Williams was also the first to recognize how serious these exceptions are to any neat story of traditional character displacement as underlying the radiation of anoles in the Caribbean. And Williams also thought that the Lesser Antilles needed to be understood first before extrapolating to the Greater Antilles.
Because of these exceptions to the size rule, Ernest proposed certain workarounds—that repeated invasion by failed propagules from Guadeloupe to Marie Galante was “nudging” the Marie Galante anole to be “too big”, and that the near-extinct status of the smaller anole on St. Martin implied it could have no evolutionary impact on the body size of the solitary-sized anole it co-occurred with in restricted locales. That left unexplained however, why the smaller anole was near extinction there to begin with.
So, the Galapagos finches and Lesser Antilles anoles show different biogeographic patterns of body size, patterns that presage differences in how competition between finches and competition between anoles plays out. In that context I offered an alternative archipelago-wide explanation that could more or less account for both the regularities and exceptions to the body size rules in the Lesser Antilles. My idea rests on the assumption of asymmetric competition between anoles of different body sizes—a larger lizard exerts a much stronger competitive effect against a smaller lizard than vice versa. The bases for this assumption are that the energetics of body size imply that a larger lizard consumes more food than a smaller lizard and so a larger lizard takes more food away from a smaller lizard than vice versa. This is asymmetric exploitative competition. Furthermore, and perhaps more importantly, as Jonathan notes, a larger lizard can eat a smaller lizard—intra-guild predation. This is asymmetric interference competition. Anyone who dissects stomachs from a series of collected anoles encounters several specimens whose stomaches contain the bodies of other Anolis lizards. And, my students and I have occasionally directly witnessed predation by one anole species on another. Indeed the smaller lizard perching near the base of a tree is always keeping a look out for a larger lizard near the canopy who might prey on it—a large anole is likely as much a danger to a small anole as is a pearly-eyed thrasher or other avian predator. Because of this overall asymmetric competition, which presumably does not occur between finches of differing bill depth, the evolutionary consequences of competition appear to play out quite differently in finches and anoles.
Specifically, I hypothesized that an island with a solitary-sized species is more easily invaded by a larger species than a smaller species. Once the larger species does invade however, the stage is set for the original solitary-sized species to evolve to be smaller. Meanwhile, the large invader evolves to be smaller itself, entering the niche space being vacated by the original species. Thus, both species evolve in parallel to become smaller, and the difference in body size they possess is not the result of in situ character displacement, but reflects the difference the invading species had to have from the original resident for it to have successfully invaded. This overall scheme was termed a “taxon loop” or “taxon cycle”, following the jargon of the time.
In principle, this scheme more or less could account for the biogeographic size patterns in the Lesser Antilles. St Martin is an island where the larger species has converged upon the solitary size nearly driving the smaller species to extinction, and Anguilla is where it has already gone extinct. But Marie Galante continues to be problematic unless the remains of a smaller now-extinct species is discovered there, making it approximately comparable to Anguilla. Alternatively, a possible ad-hoc explanation for Marie Galante notes that the size dimorphism between males and females there is exceptionally large. Perhaps the species on Marie Galante could be viewed as having each sex occupy the niche that on standard two-species islands is occupied by different species. That would leave unexplained why this situation exists however.
Now, I don’t know of course, whether the taxon loop or some amended version of this same idea is true. It is consistent with lots but not all of the data. I did excavate fossil lizard bones on Anguilla, and the solitary-sized species now there once was larger and has evidently evolved downwards in size, as expected by the taxon loop hypothesis.
I don’t know where the first instance of the size differences between the anoles developed. My thought is that the source for the Northern Lesser Antillean anoles is the Guadeloupe cluster of islands because the central Lesser Antilles are the oldest of the Lesser Antillean islands, with Jurassic basement exposed on the Guadeloupean isle of La Desirade. The central islands also possess, along with the extensive sub-speciation that Jonathan notes, geographic variation in body size so that a dry-lowland form and a mesic-forest form of the same species differ quite a bit in body size. Thus, propagules of the same species from different places on Guadeloupe can supply different body sizes to invade other islands.
These suggested biogeographic scenarios remain conjectural, and the entire story can change in light of new findings from fossil excavations, analysis of fossil DNA, and molecular phylogenetic analysis. Still, the facts as we now know them, in my judgement, point to considerable differences between the radiations of the finches in the Galapagos the anoles of the Caribbean. These differences trace to a difference in competitive symmetry—competition is asymmetric with respect to body size in anoles, and competition is relatively symmetric with respect to bill depth in finches.
I should add that the role of micro-plate tectonics in the distribution and radiation of anoles also differs considerably between anoles and finches, a point to which Jonathan alludes when he mentions the great difference in historical age between the anole and finch radiations. The Barahona peninsula is a distinct fragment from the rest of Hispaniola and there is a faunal boundary between them. The story is not simply an ecological one, even though the Barahona region is remarkably desert-like.
I now turn to a miscellany of other matters. I’ve personally not had the opportunity to work in the field with anoles for the last five years or so. My recent students working with Anolis have studied behavioral or community questions: Roman Dial studied community structure in canopy anoles in Puerto Rican rain forest, and incidentally showed that the canopy anoles there rely on insects wafting up from the ground where they had been feeding as part of the decomposer community; Sharoni Shafir experimentally studied decision-making by foraging anoles in Anguilla, and incidentally showed that anoles on Tortola can be trained using operant conditioning techniques; Henrique Pereira studied anole territoriality on St. Martin; and most recently Lauren Buckley studied the contrasting beta-diversity patterns in the Northern and Southern Lesser Antilles, and incidentally worked on Montserrat immediately after the recent volcanic eruption there.
My own research is now almost exclusively directed toward social behavior. I would love to pursue this with anoles. Specifically, I would love to study the transition from a basically monogamous social structure in lowland xeric sites to a social structure at mesic locations consisting of one male possessing a territory containing the territories of several females perhaps surrounded by floating or satellite males. This transition in social structure is continuous along any transect from low-land sites up an elevation gradient to mesic higher elevation sites, as easily witnessed on an island such as Dominica. I would like to model this transition in social structure using the techniques and approaches from cooperative game theory and industrial economics that my lab has been developing, as summarized in my recent book, The Genial Gene. If anyone is interested in these issues, I’d love to collaborate, so let’s talk.
For anyone in the New York area on April 9, I will be participating in a symposium on sexual selection at Columbia University. I’ll be talking about modeling family dynamics using cooperative game theory and the economic theory of the firm.
By the way, my former name has been obsolete for over a dozen years and its use is discouraged.
Finally, on a personal note, I am now retiring from Stanford and will become Professor Emerita in a couple of months. I was just married in May, and in June my husband, Rick, and I moved to Kauai where we are now busily trying to get settled. I am founding an organization called The Kauai Institute and am in the midst of figuring out exactly what it will do, but in any event, it will foster basic research in ecology and evolution stressing the intersection of theory with field study.
Best wishes for everyone’s continued efforts with Anolis, a truly wonderful creature.
January 8, 2011