The role of habitat shift in the evolution of lizard morphology: evidence from tropical Tropidurus

  • Vitt L
  • Caldwell J
  • Zani P
 et al. 
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Abstract

We compared morphology of two geographically close populations of the tropical lizard Tropidurus hispidus to test the hypothesis that habitat structure influences the evolution of morphology and ecology at the population level. T. hispidus isolated on a rock outcrop surrounded by tropical forest use rock crevices for refuge and appear dorsoventrally compressed compared with those in open savanna. A principal components analysis revealed that the populations were differentially distributed along an axis representing primarily three components of shape: body width, body height, and hind-leg length. Morphological diver-gence was supported by a principal components analysis of size-free morphological variables. Mitochondrial DNA se-quences of ATPase 6 indicate that these populations are closely related relative to other T. hispidus, the rock outcrop morphology and ecology are derived within T. hispidus, and morphological and ecological divergence has occurred more rapidly than genetic divergence. This suggests that natural selection can rapidly adjust morphology and ecology in response to a recent history of exposure to habitats differing in structure, a result heretofore implied from comparative stud-ies among lizard species. There has been a recent upsurge of interest in innovative tech-niques to account for evolutionary relationships in comparative analyses (1–4). Phylogenetic analyses provide the opportunity to polarize the direction of character change and to estimate the time over which divergence has occurred. With respect to lizards, numerous techniques have been used to compare ecology and morphology among closely related species (5, 6). These studies and others (7–13) suggest that morphology can be adjusted by adaptation to differing structural characteristics of habitats. How-ever, there have been few ecomorphological studies comparing populations within species (14, 15) and none directly integrating morphological change at the population level with recent change in structural habitat in lizards. One underlying assumption of the ecomorphology paradigm (16) is that morphology differs among species as a result of competition (17, 18) or habitat shift (6). We demonstrate that morphological evolution has occurred at the population level as an adaptation to rock dwelling in South American lizards in the genus Tropidurus (19, 20), a clade that is much less speciose than Caribbean and Central American Anolis lizards in which most ecomorphology studies have been done (7–9, 21). Species of Tropidurus occur in savanna, cerrado, caatinga, and lowland forest habitats of South America (20). All are insectivores (22–26) with a tendency toward ant specialization in arboreal species (23, 25). A recent study (26) found that species that inhabited isolated rock outcrops in the southern Amazon region and used narrow crevices for escape were more compressed dorsoventrally than a widespread species (Tropidurus hispidus) that used a diversity of habitats and microhabitats. However, because a phylogeny for those populations did not exist (they comprise at least two undescribed taxa; ref. 27), it was not possible to polarize the direction of character change. T. hispidus, which is widespread north and south of the Amazon River in South America, is the only ''open formation'' species (see ref. 23 for discussion of Tropidurus taxonomy) occurring north of the Amazon. During a field expedition to the Brazilian state of Roraima in 1993, we discovered a population of T. hispidus isolated on a granitic rock outcrop within approximately 40 km of a large savanna area known locally as lavrado (28). T. hispidus is widespread in the savanna and uses a variety of microhabitats (29, 30). It does not occur in terra firme tropical forest habitats except on isolated granitic outcrops. Populations on outcrops within tropical forest are isolated from savanna populations and from other rock outcrop populations. The structure of savanna and rock outcrop habitats is very different, and the occurrence of populations in each habitat offered a unique opportunity to directly test the hypothesis that adaptation to rock outcrops causes morphological change in lizards over relatively short time periods. Based on the observa-tion that other rock outcrop Tropidurus appear dorsoventrally compressed in morphology (23), we predicted that the rock outcrop population of T. hispidus would be relatively more compressed in morphology than the savanna population. Because the rock surfaces provide a much more open microhabitat for lizards than the grassy savanna, we predicted that the rock outcrop population would have relatively longer hind limbs as shown in other lizards (31, 32). Because the isolated rock outcrop in which we studied Tropidurus was part of a continuous savanna habitat until recently (33–39), we also predicted that the rock outcrop population was derived from the savanna population and that divergence had been a relatively recent event. We used morphological comparisons to demonstrate morphological divergence and molecular data to polarize the direction of change and examine the degree of genetic divergence.

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Authors

  • Laurie J. Vitt

  • Janalee P Caldwell

  • Peter A Zani

  • Tom A Titus

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