Repeatable Evolution: Lizard Diversification On Different Islands Produces Similar Outcomes

Convergent evolution in cichlid fish from Lake Tanganyika (left) and Lake Malawi (right). Image from Stiassny and Meyer, Scientific American, 1999).

For years, evolutionary biologists have debated the predictability of evolution. Stephen Jay Gould famously said that if the tape of life could be rewound to the same starting point, it would replay with a very different outcome. On the other hand, many evolutionary biologists have pointed to the ubiquity of adaptive convergent evolution–when species facing similar environmental pressures evolve in highly similar ways–as evidence that evolution is deterministic.

A particularly interesting example of repeated convergent evolution occurs when two groups evolving in different places diversify to produce similar sets of descendant species. The existence of such “replicated adaptive radiations” would seem to be strong evidence for evolutionary determinism. For example, the cichlid fishes of the African Rift lakes have become an iconic textbook example, illustrated by diagrams matching up pairs of species from two lakes  that are morphologically convergent (see figure on right). The problem is that there are hundreds of fish species in each lake—the example illustrates a number of cases of convergent evolution between the lakes, but does not demonstrate that the lake radiations themselves are overall more similar than one might expect; another possibility is that there are some cases of convergence embedded in a larger pool of non-convergent evolution.

 This figure illustrates pairs of Anolis species from different Greater Antillean islands that have independently evolved matching morphologies. Anoles diversifying on four islands repeatedly colonized the same adaptive peaks on a shared evolutionary landscape, resulting not just in convergence among a few species pairs, such as those shown here, but in the convergence of entire island anole faunas. From left to right, the top row depicts giant tree crown specialists Anolis cuvieri (Puerto Rico; photo by J. Losos) and A. garmani (Jamaica); second row depicts the twig specialists A. garridoi (Cuba) and A. occultus (Puerto Rico); third row depicts trunk and ground specialists A. cybotes (Hispaniola; photo by B. Falk) and A. lineatopus (Jamaica); fourth row depicts grass specialists A. alumina (Hispaniola; photo by M. Landestoy) and A. alutaceus (Cuba). Images not otherwise marked are by L. Mahler.

Examples of convergent evolution in Greater Antillean Anolis lizards. From the top: Giant tree crown specialists from Puerto Rico and Jamaica (photo J. Losos); twig specialists from Cuba and Puerto Rico; tree trunk near ground specialists from Hispaniola (photo by B. Falk) and Jamaica; and  grass specialists from Hispaniola (photo by M. Landestoy) and Cuba. Uncredited photos by L. Mahler.
Anolis barbouri, a leaf-litter specialist from Hispaniola. Nothing like it has evolved on any of the other Greater Antillean islands.
Anolis barbouri, a leaf-litter specialist from Hispaniola. Nothing like it has evolved on any of the other Greater Antillean islands.

Another classic case of replicated adaptive radiation is the lizards of the genus Anolis, which have diversified mostly independently across the four islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico). As with the cichlids, sets of similar species have evolved convergently on each island; for example, short-legged, camouflaged species have evolved on each island to adapt to living on twigs, and green species with large toepads have evolved to live in the canopy. But also as with the cichlids, some types are ecologically and morphologically unique to a single island; for example, Hispaniola has an anatomically distinctive leaf litter-dwelling species that has no counterpart on the other islands.

Given the considerable amount of research on the evolution of these lizards, including a well worked out evolutionary tree, they would seem to be a perfect group in which to investigate whether entire radiations are truly replicated. Luke Mahler of the University of California at Davis and colleagues (including me!) have done just that in a paper published in this week’s issue of Science. By taking anatomical measurements on the species on the four islands, the paper demonstrates that, although the set of species that have evolved on each island is not identical, they are very similar, much more so than would be expected by chance. In other words, despite evolutionarily radiating independently on each island, the outcome has been deterministic—species diversifying independently in similar environments do, indeed, produce highly similar evolutionary outcomes.

George Gaylord Simpson

But why does this occur? Years ago, the great paleontologist George Gaylord Simpson proposed what is now called the “macroevolutionary landscape.” Analogous to a topology map, Simpson suggested that there are “adaptive peaks,” particular combinations of features that natural selection would favor. A corollary of this idea is that similar environments should have similar adaptive peaks, and thus should lead to evolutionarily similar radiations. The idea, though intuitive and widely-discussed, has never previously been tested in the context of replicated adaptive radiations.

Using a powerful new analytical method, Mahler et al. showed that, indeed, the adaptive landscapes have been highly similar for the diversifying island groups. Not only does this study demonstrate that similar evolutionary diversification is the result of similar underlying natural selection pressures, but, given the antiquity of these lizards (which began to radiate more than 40 million years ago), it also reveals that evolutionary pressures can remain relatively constant over long periods of time. Ironically, even while disproving the idea that replays of the same evolutionary tape will not produce similar outcomes, this study finds support for another of Stephen Jay Gould’s ideas, the existence of long term evolutionary stasis.


Changing Planet

Meet the Author
Jonathan Losos is a professor in the Department of Organismic and Evolutionary Biology at Harvard University and Curator of Herpetology at the Museum of Comparative Zoology. He is also a member of the National Geographic Committee for Research and Exploration. The focus of Dr. Losos’s research is biological diversity, how it originates evolutionarily and how it is maintained in ecological communities. Answering these questions requires synthesis of ecological, behavioral, functional, and evolutionary data, requiring work both in the laboratory and the field. The organisms of choice in these studies are lizards, and Dr. Losos’s research has taken him throughout the world, conducting studies in the Caribbean, Central and South America, Africa, Madagascar, and Australia. Dr. Losos is the former editor of the American Naturalist, a leading interdisciplinary journal in the fields of ecology and evolutionary biology, and has authored or edited two books, two textbooks and more than 100 scientific papers. He is the recipient of the Theodosius Dobzhansky Prize, the David Starr Jordan Prize, and a John Simon Guggenheim Fellowship. Dr Losos is also a regular contributor to Anole Annals, a blog written and edited by scientists who study Anolis lizards.