Contingency and Determinism in Replicated Adaptive Radiations of Island Lizards

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Science  27 Mar 1998:
Vol. 279, Issue 5359, pp. 2115-2118
DOI: 10.1126/science.279.5359.2115


The vagaries of history lead to the prediction that repeated instances of evolutionary diversification will lead to disparate outcomes even if starting conditions are similar. We tested this proposition by examining the evolutionary radiation ofAnolis lizards on the four islands of the Greater Antilles. Morphometric analyses indicate that the same set of habitat specialists, termed ecomorphs, occurs on all four islands. Although these similar assemblages could result from a single evolutionary origin of each ecomorph, followed by dispersal or vicariance, phylogenetic analysis indicates that the ecomorphs originated independently on each island. Thus, adaptive radiation in similar environments can overcome historical contingencies to produce strikingly similar evolutionary outcomes.

The theory of historical contingency proposes that unique past events have a large influence on subsequent evolution (1-3). A corollary is that repeated occurrences of an evolutionary event would result in radically different outcomes (4). Indeed, faunas and floras that have evolved in similar environments often exhibit more differences than similarities (5-7). These differences in evolutionary outcome probably result from clade-specific factors that cause taxa to respond to similar selective factors in different ways, as well as from unique historical events and subtle environmental differences in the different areas (2, 8). Here we show that such factors will not always lead to disparate outcomes.

Anolis lizards are a dominant element of the Caribbean fauna. On each of the islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico), lizard assemblages are composed of species that differ in habitat use. The same set of “ecomorphs”—species specialized to use particular structural microhabitats—occurs on each island, except that two ecomorphs are absent from Jamaica and one from Puerto Rico (9).

We measured six morphometric characteristics that are closely linked to habitat use (10, 11) for members of each ecomorph class from each island to investigate whether the ecomorphs constitute objectively recognizable classes (12). Our analyses reveal distinct ecomorph classes; members of an ecomorph class are more similar to other members of that class from different islands than they are to members of different ecomorph classes from their own island (Fig. 1A) (13).

Figure 1

(A) UPGMA phenogram showing that members of the same ecomorph class cluster in morphological space regardless of geographic affinities. Branch lengths are proportional to the distance separating species or clusters in morphological space. Letters indicate the island on which a species is found (C, Cuba; H, Hispaniola; J, Jamaica; P, Puerto Rico). The shading of the branches connecting the ecomorph classes has no significance. (B) The most parsimonious tree derived from the molecular data indicates frequent transitions among ecomorph classes. The lengths of the branches have no significance. (C) Topology of the four ecomorphs common to all islands, extracted for each island separately from the most parsimonious phylogeny.

The presence of the same set of ecomorphs on each island suggests that either ecomorphs evolved only once and then, by colonization or vicariance, occupied all four islands, or that each ecomorph evolved independently on all four islands. Because six ecomorph classes exist (crown-giant, grass-bush, trunk, trunk-crown, trunk-ground, and twig; the classes are named for the microhabitat that constituent species normally use), the single-evolution hypothesis predicts that only five instances of the evolution of new ecomorphs have occurred (assuming that one ecomorph is ancestral). By contrast, the recurring evolution hypothesis (9) predicts that none of the ecomorph classes form a monophyletic group and that 17 to 19 evolutionary transitions between ecomorph classes have occurred (14).

Phylogenetic analysis based on mitochondrial DNA sequences (15, 16) for 55 species (17) indicates that, with two exceptions, members of the same ecomorph class from different islands are not closely related (Fig.1B). Statistical analyses (18) indicate that none of the ecomorph classes constitutes a monophyletic group relative to members of the other classes and that at least 17 evolutionary transitions among ecomorph classes have occurred (Table1) (19, 20). Although similar sets of ecomorphs have evolved independently on each island, the sequence by which they have evolved differs among islands (Fig. 1C) (21).

Table 1

Hypotheses tested with DNA sequence data. A significant result denotes rejection of the stated hypothesis. D is the difference in length between the most parsimonious tree (8889 steps) and the tree constrained to conform to the stated hypothesis. T s is the test statistic for the Wilcoxon signed-ranks test. n is the number of characters that differed in numbers of changes on the two trees. Z is the normal approximation when n > 100 (25). “Difference” is the difference in negative log likelihoods between the maximum likelihood tree (–ln L = 41,059.9) and the tree constrained to conform to the stated hypothesis. t is the Student‘s t test statistic.

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One hypothesis to explain the repeated evolution of the same ecomorph types is that the diversity of morphological variants that can be produced by anoles is constrained to these ecomorphs. However, the existence of several Greater Antillean species, usually restricted to montane areas (9), and many mainland species (22) that are not members of any of the ecomorph classes shows that morphological diversification among anoles is not constrained to produce only members of these ecomorph classes. Rather, the recurring evolution of ecologically and morphologically similar species in these replicate adaptive radiations suggests that adaptation, rather than constraint, is responsible for the predictable evolutionary responses of Anolis lizards.

The phylogenetic analysis reveals only two cases in which an ecomorph has evolved more than once on a single island. Interspecific competition, which is intense among anoles (23) and may drive their adaptive radiation (9, 24), is probably responsible; once an ecomorph niche is filled on an island, other species are excluded from utilizing that niche. Thus, the importance of historical contingency depends on the frame of reference: Among islands, it has little discernible effect in that the same ecomorphs evolve on each island, whereas within each island, prior evolutionary events limit the options available to particular species and thus determine the directions in which evolution can proceed.

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