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Rapid Temporal Reversal in Predator-Driven Natural Selection

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Science  17 Nov 2006:
Vol. 314, Issue 5802, pp. 1111
DOI: 10.1126/science.1133584

Abstract

As the environment changes, will species be able to adapt? By conducting experiments in natural environments, biologists can study how evolutionary processes such as natural selection operate through time. We predicted that the introduction of a terrestrial predator would first select for longer-legged lizards, which are faster, but as the lizards shifted onto high twigs to avoid the predator, selection would reverse toward favoring the shorter-legged individuals better able to locomote there. Our experimental studies on 12 islets confirmed these predictions within a single generation, thus demonstrating the rapidity with which evolutionary forces can change during times of environmental flux.

Because of its potentially epochal scope, evolutionary biology is often caricatured as a strictly descriptive science, but recent years have shown that evolution can be studied on short time scales and that evolutionary biology can be both experimental and predictive (1, 2). Here, we report just such an example by demonstrating the occurrence of a predicted reversal in the direction of natural selection on limb length in Anolis sagrei, a common Bahamian lizard often found on the ground in the absence of terrestrial predators.

Previous research showed that, when a larger and entirely terrestrial predatory lizard, Leiocephalus carinatus, invades, A. sagrei becomes more arboreal and that the extent of this habitat shift broadens through time (3). Hence, we predicted that the direction of selection operating on limb length in A. sagrei would change through time in the presence of L. carinatus (4): Initially A. sagrei occurs mostly on the ground, so individuals with relatively longer legs, being faster (5), would be better able to elude the predators and thereby be favored. As A. sagrei becomes more arboreal, however, we predicted that selection would favor the reverse because shorter limbs are better suited for movement on the narrow and irregular surfaces A. sagrei would use to avoid the terrestrial predator (5).

To test this hypothesis, we introduced L. carinatus to six small Bahamian islands that naturally contained A. sagrei, randomly choosing six others to serve as controls (L. carinatus occurs on nearby larger islands and is known to colonize smaller islands); the number of L. carinatus introduced (all adults) was proportional to the number of A. sagrei resident on the island. Before introduction of L. carinatus, A. sagrei individuals on each island were measured and individually marked. Islands were exhaustively censused after 6 and 12 months to determine survival (6).

All predictions were confirmed. A. sagrei on introduction islands became increasingly arboreal, whereas use of the ground remained unchanged in controls (Fig. 1A); differences in perch diameter between lizards on experimental and control islands also increased through time (Fig. 1B). These trends are the same if comparisons are restricted to only those individuals surviving to the end of the experiment, indicating that differences between treatments resulted from individual shifts in behavior, rather than selection among individuals differing in habitat use [see also (4)]. In the first 6 months, longer legs were more strongly favored on introduction islands than on controls, but in the second 6 months, selection was reversed and more strongly favored shorter legs on introduction islands [repeated-measures analysis of covariance (ANCOVA), time*treatment interaction, F1,2 = 59.04, P = 0.017 (Fig. 1C)]. This reversal was accompanied by an especially great divergence in perch diameter during the second six months (repeated-measures analysis of variance, time*treatment interaction, F1,10 = 11.38, P = 0.007).

Fig. 1.

Changes in habitat use and pattern of natural selection. For use of the ground (top) and perch diameter (middle), data from May 2003 represents habitat use before the initiation of the experiment. All data are for individuals initially measured and marked in May 2003. Lizards grew throughout the experiment, probably explaining the increase in perch diameter on control islands (an intraspecific relationship between body size and perch diameter is well established in Anolis lizards). (Bottom) Selection gradients were calculated for two time periods, May 2003 to November 2003 and November 2003 to May 2004. Selection gradients in the figure were adjusted for log-transformed island area (included in the repeated-measures analysis as a covariate) by using least squares means from the ANCOVA. Open symbols indicate control islands; filled symbols, introduction islands. Error bars are ± 1 standard error.

Thus, we showed that selection dramatically changed direction over a very short time, within a single generation, favoring first longer and then shorter hindlimbs. The behavioral shift from the ground to higher perches of smaller diameter apparently caused this remarkable reversal; behavioral flexibility, indeed, may often be the key in driving extremely rapid reversals in evolution (4). Our experiment also illustrates the complexity of measuring natural selection in the field (7). For example, had we waited 12 months to first measure selection, we could have concluded that the predator's presence had little if any effect on selection, and we certainly would have failed to detect the transitory selection for longer hind limbs over the first 6-month period (table S1).

Nonetheless, over the much longer term, we expect that in the continued presence of L. carinatus the initially long-legged A. sagrei would remain on high, thin perches, eventually evolving substantially shorter legs. We base this expectation both on functional studies of locomotion (5) and on the observation that twig specialists have arisen four times on Caribbean islands, in each case evolving very short hind legs (8). Evolutionary biology is by its nature an historical science, but the combination of microevolutionary experimentation and macroevolutionary historical analysis can provide a rich understanding about the genesis of biological diversity.

Supporting Online Material

www.sciencemag.org/cgi/content/full/314/5802/1111/DC1

Materials and Methods

Fig. S1

Table S1

References

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