Natural historians have known for a long time that islands often harbour an extraordinary amount of biodiversity. One reason is that lineages that colonize islands can exploit open ecological niches and therefore diversify along new evolutionary trajectories. So did Anolis lizards following their arrival to the Caribbean. A range of habitat specialists has evolved repeatedly on different islands, creating a structured diversity of morphologies. Since one Anolis clade has remained on the mainland, and one clade has returned the mainland, this group of lizards presents a kind of before/after ‘island evolution’ experimental setting that can help us understand how evolution works.
Our new study, published in Nature Communications, took advantage of this setting to find out if morphological diversification proceeded in a different way following colonization of the Caribbean islands compared to the lizards that stayed on the mainland. This would be predicted if there were lots of ecological opportunities on islands. Furthermore, we wanted to know if the clade that returned to the mainland evolved along similar trajectories as their distant mainland relatives, or if they followed more closely their Caribbean relatives. Finally, we also wanted to test if evolution on the Caribbean islands was faster, more punctuated, and led to higher morphological diversity than on the mainland, again expected if lizards encountered a lot of empty niches on islands. To answer these questions, Nathalie and Illiam travelled to the Nanoscale Research Facility at the University of Florida to collect CT-scans of more than 700 individuals of 271 Anolis species. Back home they quantified the morphology of the parts of the skeleton that determine how the lizards navigate their habitat – limb bones, hip and shoulder girdles. Interestingly, we found that the evolutionary modularity – the covariation of parts of the locomotor skeleton across the evolutionary tree – was different between the clades: while the lizards whose ancestors had never set foot on an island showed a tight covariation between the fore- and hindlimbs, Anolis evolution on islands followed a trajectory with much tighter covariation between limbs and their respective girdles (forming a front and a hind module). What is more, the evolutionary modularity that was seen across island lizards was also seen in the mainland re-colonizers.
What does this mean? The answers are hidden in the past, of course, but we speculate that the exploitation of ecological opportunities following colonization of the islands led to a profound change in how limbs and girdles develop and grow together during ontogeny. That is, adaptation on islands may have changed how limbs and girdles vary together, and this change persisted even after lizards recolonized the mainland. This meant that lizards in the clade that recolonized the mainland produced very similar morphologies to those seen on the islands, but failed to explore some parts of the morphospace occupied by their other mainland relatives. If we compare the island lizards with the clade that returned to the mainland, we find that a general prediction from island biogeography holds true – island lizards show faster and more variable evolutionary rates and greater morphological variation. That is, while the patterns of diversification of the locomotor skeleton is similar, the mainland lizards produce only a subset of the morphologies seen on the islands. The same is not true, however, if we compare the morphology of island lizards to the morphology of lizards in the ‘primary’ mainland clade. This mainland clade is equally diverse as the lizards on islands, and it contains morphologies that are not seen on the islands. Perhaps this means that comparing diversification patterns of island and mainland groups is only ‘fair’ if the two groups share the same variability. Or perhaps it reflects historical differences in the ecological opportunities for adaptive diversification in the two mainland clades.
We do not yet have all the answers, and many will forever remain unknown. However, we do suggest that these macroevolutionary trends of the locomotor skeleton in Anolis illustrate that adaptation to ecological opportunities on islands can have profound effects on trait development, with lasting effects on patterns of morphological diversification. To put this hypothesis to the test, we need to study how the parts of the locomotor skeleton vary together within species, and do this for several species across the different clades. A big task, but not impossible.