Harvey, Paul H.; Partridge, Linda
In science, it can be all too easy to provide the public with different take-home messages from the same body of theory and data. Nowhere is that more apparent than from evolution, where different authors have championed different perspectives.
Richard Dawkins, for example, frequently emphasizes evolution by natural selection as a unifying theory for biology: his is a largely deterministic world following from the differential survival and reproductive success of genes within which there is no recombination [1]. By contrast, Stephen Gould concentrates on the evidence for biodiversity resulting from contingency - historical accidents determine disparate courses of evolution [2]. In his metaphor, if the tape of life was repeated, we should always expect a different outcome.
These perspectives leave open the middle ground: if the tape of life was repeated, just how varied would the outcome be? In a paper published in Science last month [3], Jonathan Losos and colleagues describe their studies of Anolis lizard species evolving on the Caribbean islands of the Greater Antilles to provide an illuminating test case.
Four islands constitute the Greater Antilles: Cuba, Hispaniola, Jamaica and Puerto Rico. Each of these islands has its own Anolis community. Working over four decades, Ernest Williams and his students demonstrated that each species on each island has a distinctive niche [4,5] to which it seems to be nicely adapted [6,7]. There are small, short-legged species that live out on fragile twigs, and large-bodied species that inhabit the crowns of trees; and there are others again on the trunk, on the ground and in bushes, and on transitional habitats. Williams called these habitat specialists 'ecomorphs' [8]. Losos has identified six ecomorphs (examples are shown in Figure 1), most of which are present on each island; two are missing from Jamaica and one from Puerto Rico. Some islands have more than one version of a particular ecomorph.
But are the ecomorphs figments of Williams's and Losos's imaginations, or do the same ecomorphs from different islands cluster together in 'morphospace'? In the new study, a variety of morphological characters was measured on several specimens from each ecomorph on the different islands, corrected for body size, and mapped in four-dimensional morphospace, which accounted for more than 95% of variance in the data. The data were then subjected to a hierarchical classification by similarity, and each of 46 species was found to group by ecomorph, independently of its island of origin.
Parsimony arguments based on morphological evolution might lead us to conclude that each ecomorph had a single evolutionary origin, followed by dispersal among the islands. Given six ecomorphs, there would have been five morphological transitions over evolutionary time. Alternatively, similar ecomorphs could have evolved independently on the four islands. Under the conservative assumption that each ecomorph evolved at most once on each island, there would have been between 17 and 19 evolutionary morphological transitions (depending on which was the ancestral phenotype). To distinguish between these two extremes, Losos et al. produced a molecular phylogeny based on mitochondrial DNA sequences relating the various species from the different islands. The most parsimonious tree based on molecular evolution, and all trees within four molecular steps of it, required 17 morphological transitions, as did maximum-likelihood trees.
In fact, the molecular phylogenetic analysis identifies just two cases where the same ecomorph has evolved twice on an island, which makes the occurrence a rare event. Losos et al. suggest that once an ecomorph has evolved on an island it tends to fill the available niche, preventing other species evolving into it. It seems then that as the tape of life has been replayed on the separate islands, there has been a remarkable amount of convergent evolution.
But there remains a role for contingency: the order of evolution of the different ecomorphs seems to differ among the islands. Four ecomorphs are common to each of the four islands, but no phylogenetic tree relating the four ecomorphs is common to any pair of islands (contrary to preliminary evidence reported earlier) [6]. For example, on Puerto Rico the trunk-crown ecomorph's closest relative is the trunk-ground, whereas on Jamaica it is the crown-giant, and on Cuba it is the twig ecomorph. It is not currently possible to distinguish between two extreme causes for these differences. The same end state may have been reached from either similar or different starting conditions, with the same ecomorph or different ecomorphs initially invading each island.
Perhaps evolutionary biologists should not be surprised at such convincing evidence for convergent morphological evolution. After all, the comparative method, which was used so effectively by Darwin and has been a cornerstone of evolutionary investigation ever since, depends for its very existence on repeated instances of convergent evolution [9]. More novel is the finding that the order of evolutionary transitions can differ so markedly-it does not seem to matter what route you take, you'll get there in the end.
1. Dawkins, R. Climbing Mount Improbable (Viking, London, 1996). [Context Link]
2. Gould, S. J. Wonderful Life (Norton, New York, 1989). [Context Link]
3. Losos, J. B., Jackman, T. R., Larson, A., de Queiroz, K. & Rodriguez-Schettino, L. Science 279, 2115-2118 (1998). [Context Link]
4. Rand, A. S. & Williams, E. E. Breviora 327, 1-19 (1969). Bibliographic Links [Context Link]
5. Williams, E. E. in Lizard Ecology: Studies of a Model Organism (eds Huey, R. B., Pianka, E. R. & Schoener, T. W.) 326-370 (Harvard Univ. Press, Cambridge, MA, 1983). [Context Link]
6. Losos, J. B. in New Uses for New Phylogenies (eds Harvey, P. H., Leigh Brown, A. J., Maynard Smith, J. & Nee, S.) 308-321 (Oxford Univ. Press, 1996). [Context Link]
7. Losos, J. B. & Irschick, D. J. Anim. Behav. 51, 593-602 (1996). [Context Link]
8. Williams, E. E. Evol. Biol. 6, 47-89 (1972). [Context Link]
9. Harvey, P. H. & Pagel, M. D. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, 1991). [Context Link]