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Science  24 Oct 2014:
Vol. 346, Issue 6208, pp. 463-466
DOI: 10.1126/science.1257008

Making adjustments for a new neighborhood

Competition between species drives the acquisition of diversity. Stuart et al. introduced a non-native anole lizard to natural experimental islands. In response, the original inhabitants adopted higher perches in the trees, where the larger invader was at a disadvantage. Within about 3 years—or 20 generations—the shift led to inherited morphological changes in the native lizards, including their growing larger toepads.

Science, this issue p. 463

Abstract

In recent years, biologists have increasingly recognized that evolutionary change can occur rapidly when natural selection is strong; thus, real-time studies of evolution can be used to test classic evolutionary hypotheses directly. One such hypothesis is that negative interactions between closely related species can drive phenotypic divergence. Such divergence is thought to be ubiquitous, though well-documented cases are surprisingly rare. On small islands in Florida, we found that the lizard Anolis carolinensis moved to higher perches following invasion by Anolis sagrei and, in response, adaptively evolved larger toepads after only 20 generations. These results illustrate that interspecific interactions between closely related species can drive evolutionary change on observable time scales.

In their classic paper, Brown and Wilson (1) proposed that mutually negative interactions between closely related species could lead to evolutionary divergence when those species co-occurred. In the six decades since, this idea has been debated vigorously, with support that has vacillated, depending on the latest set of theoretical treatments and comparative studies [reviewed in (25)]. However, tests of interaction-driven evolutionary divergence have been slow to capitalize on the growing recognition that evolutionary change can occur rapidly in response to strong divergent natural selection [but see (69)]; thus, evolutionary hypotheses about phenomena once thought to transpire on time scales too long for direct observation can be tested in real time while using replicated statistical designs.

An opportunity to study such real-time divergence between negatively interacting species has been provided by the recent invasion of the Cuban brown anole lizard, Anolis sagrei, into the southeastern United States, where Anolis carolinensis is the sole native anole. These species have potential to interact strongly [e.g., (10)], being very similar in habitat use and ecology (11). We investigated the eco-evolutionary consequences of this interaction on islands in Florida (12) using an A. sagrei introduction experiment, well-documented natural invasions by A. sagrei, genomic analyses of population structure, and a common garden experiment. This multifaceted approach can rule against several of the most difficult alternative hypotheses [e.g., plasticity, ecological sorting, environmental gradients (2, 5)] while directly testing two predictions for how A. carolinensis responds to its congeneric competitor.

Typical of solitary anoles (13), A. carolinensis habitat use spans ground to tree crown (14). However, where A. carolinensis and A. sagrei (or their close relatives) co-occur elsewhere, A. carolinensis perches higher than A. sagrei (1316). Thus, we used an introduction experiment to test Collette’s prediction (14) that competitive interactions with A. sagrei should drive an increase in A. carolinensis perch height. In early May 1995, we chose six islands that contained resident populations of A. carolinensis and collected pre-introduction perch height data from undisturbed lizards (12). Later that month, we introduced small populations of A. sagrei to three treatment islands, leaving three control islands containing only A. carolinensis (12). From May to August 1995–1998, we measured perch heights for both species. The A. sagrei populations grew rapidly [table S1; (17)], and by August 1995, A. carolinensis on treatment islands already showed a significant perch height increase relative to controls, which was maintained through the study [Fig. 1, fig. S1, and table S2; (12)].

Fig. 1 Perch height shift by A. carolinensis after the experimental introduction of A. sagrei.

We introduced A. sagrei to one small, one medium, and one large island (treatment; closed symbols) in 1995, keeping three similarly sized control islands (open symbols). Island means (±1 SE) are shown for perch height. Anolis sagrei introduction corresponds with a significant perch height increase by A. carolinensis (linear mixed models: treatment × time interactions, all P < 0.001 [(12)]; tables S1 and S2].

We next predicted, following (14), that this arboreal shift by A. carolinensis would drive the evolution of larger toepads with more lamellae (adhesive, setae-laden, subdigital scales). Toepad area and lamella number (body-size corrected) correlate positively with perch height among anole species (14, 1820), and larger and better-developed toepads improve clinging ability (20), permitting anoles to better grasp unstable, narrow, and smooth arboreal perches. We tested the prediction in 2010 on a set of islands partially overlapping those used in 1995–1998 (12). We surveyed 30 islands and found that A. sagrei had colonized all but five (12). We compared A. carolinensis populations on these five islands without the invader (hereafter “un-invaded”) to A. carolinensis populations on six islands that, on the basis of 1994 surveys, were colonized by A. sagrei sometime between 1995 and 2010 (hereafter “invaded”) [Fig. 2; (12)].

Fig. 2 2010 study islands along the Intracoastal Waterway.

Anolis carolinensis inhabits all study islands. Six study islands were invaded by A. sagrei sometime between 1995 and 2010 (closed circles), and five study islands remain un-invaded today (open circles). Nineteen additional non–study islands were surveyed [“x”; (12)]; 17 of these contained A. carolinensis and were invaded by A. sagrei; and two were empty of both species.

From May to August 2010, we measured perch height for undisturbed lizards and found that, as in the 1995 introduction experiment, A. carolinensis perch height was significantly higher on invaded islands [fig. S2 and table S3; (12)]. We then tested whether the perch height shift had driven toepad evolution by measuring toepad area and lamella number of the fourth toe of each hindleg for every A. carolinensis captured (12). We found that A. carolinensis on invaded islands indeed had larger toepads and more lamellae [traits corrected for body size; Fig. 3, A and C, and table S3; (12)]).

Fig. 3 Divergence in wild-caught and common garden A. carolinensis.

Mean-of-island-means size-corrected residuals (±1 SE) are shown. The invasion of A. sagrei corresponds to a significant increase in both traits for wild-caught lizards (A and C) in 2010 [five islands un-invaded, six invaded; linear mixed models (LMM); (A) toepad area, βinvaded = 0.15, t9 = 2.7, P = 0.012; (C) lamella number, βinvaded = 0.54, t9 = 3.1, P = 0.009]. (B and D) Common garden offspring from invaded islands had significantly larger toepad characteristics [four un-invaded islands; four invaded; LMM; (B) toepad area, βinvaded = 0.14, t6 = 2.1, P = 0.043; (D) lamella number, βinvaded = 1.45, t6 = 3.6, P = 0.006]. All P values are one-tailed.

This morphological change occurred quickly. Assuming, conservatively, that A. sagrei reached all six invaded islands in 1995, A. carolinensis populations on invaded and un-invaded islands have diverged at mean rates of 0.091 (toepad area) and 0.077 (lamellae) standard deviations per generation [haldanes (21); rates > zero, each one-tailed P < 0.02; (12)], comparable to other examples of rapid evolution (21) such as soapberry bug beak length (22) or guppy life history (23).

We tested several alternative processes that could have generated the observed divergence. First, we used a common garden experiment to investigate possible posthatching, developmental responses to physical challenges imposed by arboreality during growth (i.e., phenotypic plasticity). We took gravid A. carolinensis females from four invaded and four un-invaded islands in July 2011, collected their eggs in the laboratory, and raised the offspring in identical conditions (12). The effect of A. sagrei invasion on A. carolinensis toepad characteristics persisted in the common garden [Fig. 3, B and D, and table S4; (12)], suggesting genetically based divergence in nature (though we cannot rule out transgenerational plasticity).

Second, observed divergence in A. carolinensis could have arisen through nonrandom migration of individuals with large toepads among invaded islands, instead of arising independently on each island. Thus, we tested whether relatedness among A. carolinensis populations is independent of A. sagrei invasion. In 379 A. carolinensis individuals from four un-invaded and five invaded islands, we genotyped 121,973 single-nucleotide polymorphisms across the genome [table S5, (12)]. Individuals from the same island were closely related, and islands were largely genetically independent (pairwise-FST 0.09–0.16; table S6). We found no evidence that population relatedness in A. carolinensis was correlated with whether an island had been colonized by A. sagrei [Fig. 4; (12)] or with distance between islands (Mantel test; P > 0.25), suggesting that gene flow is relatively limited among islands and that island populations were independently founded from the mainland.

Fig. 4 Neighbor-net analysis of genetic distance for A. carolinensis individuals from invaded (red) and un-invaded (blue) islands (12).

Small shaded areas enclose individuals that do not cluster with their own island; the color of these areas represents invasion status of their home islands.

Third, toepad changes could have been generated by adaptation to environmental differences among islands that are confounded with the presence of A. sagrei [e.g., (24)]. However, invaded and un-invaded islands do not differ in characteristics important to perching or arboreal locomotion [e.g., vegetated area, plant species richness, or available tree heights; table S7; (12)]. Fourth, toepad changes could have arisen through ecological sorting, wherein A. sagrei was only able to colonize those islands on which the existing A. carolinensis population was already sufficiently different. However, A. sagrei seems capable of successfully colonizing every island it reaches, regardless of resident A. carolinensis ecology or morphology: All 10 A. sagrei populations introduced in 1994–1995 are still extant (12), and A. sagrei inhabits nearly every other island surveyed in the lagoon (Fig. 2). Finally, toepad changes observed in A. carolinensis in 2010 could be unrelated to interactions with A. sagrei if the latter’s invasion merely missed the five islands with the lowest A. carolinensis perch heights (fig. S2) by chance; however, this would occur only one time in 462. In sum, alternative hypotheses of phenotypic plasticity, environmental heterogeneity, ecological sorting, nonrandom migration, and chance are not supported; our data suggest strongly that interactions with A. sagrei have led to evolution of adaptive toepad divergence in A. carolinensis.

Brown and Wilson called evolutionary divergence between closely related, sympatric species “character displacement” (1), and our data constitute a clear example of this. Resource competition has been the interaction suggested most often as the source of divergent selection during character displacement [sometimes specifically called “ecological character displacement” (13)]. For A. carolinensis and A. sagrei, resource competition for space likely is important: Allopatric A. carolinensis and A. sagrei overlap in their use of the habitat (1214, 16); moreover, when they co-occur, the two species interact agonistically (10), and our experimental data show a rapid spatial shift by A. carolinensis following A. sagrei introduction. The two species also overlap in diet and thus may compete for food (17). Competition for food is strong among co-occurring Anolis and has been shown to be mitigated by differences in perch height (11). Evolutionary divergence may also arise, however, from selection to reduce interspecific hybridization; yet, such “reproductive character displacement” (4) seems an unlikely explanation for our results, as A. carolinensis and A. sagrei already differ markedly in species-recognition characteristics, males of both species nearly exclusively ignore heterospecific females in staged encounters (25), and the species have never been reported to successfully produce hybrids. We note, finally, that other mutually negative interactions such as apparent competition (26) and intraguild predation (27) could also produce divergence among overlapping species. These remain to be explored in this system, though some evidence exists for at least the latter (17).

Here, we have provided evidence from a replicated, natural system to support the long-held idea (4) that interspecific interactions between closely related species are an important force for evolutionary diversification (2). Moreover, we show that evolutionary hypotheses such as character displacement can be rigorously tested in real time following human-caused environmental change. Our results also demonstrate that native species may be able to respond evolutionarily to strong selective forces wrought by invaders. The extent to which the costs of invasions can be mitigated by evolutionary response remains to be determined (28), but studies such as this demonstrate the ongoing relevance of evolutionary biology to contemporary environmental issues.

Supplementary Materials

www.sciencemag.org/content/346/6208/463/suppl/DC1

Materials and Methods

Supplementary Acknowledgments

Figs. S1 and S2

Tables S1 to S7

References (2945)

References and Notes

  1. Information on materials and methods is available on Science Online.
  2. Acknowledgments: We thank A. Kamath, C. Gilman, A. Algar, J. Allen, E. Boates, A. Echternacht, A. Harrison, H. Lyons-Galante, T. Max, J. McCrae, J. Newman, J. Rifkin, M. Stimola, P. VanMiddlesworth, K. Winchell, C. Wiench, K. Wollenberg, and three reviewers; M. Legare and J. Lyon (Merritt Island National Wildlife Refuge), J. Stiner and C. Carter (Canaveral National Seashore); and Harvard University, Museum of Comparative Zoology, University of Massachusetts Boston, University of Tennessee Knoxville, University of Tampa, NSF (DEB-1110521), and NIH (P30GM103324) for funding. Y.E.S., T.S.C., and J.B.L. designed the study; Y.E.S., T.S.C., P.A.H., L.J.R, and R.G.R. collected the data; Y.E.S., T.S.C., and P.A.H. analyzed the data; all authors contributed to the manuscript. Data are accessioned on datadryad.org: doi:10.5061/dryad.96g44.
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