Recurrent Evolution of Herbivory in Small, Cold-Climate Lizards
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Recurrent evolution of herbivory in small, SEE COMMENTARY cold-climate lizards: Breaking the ecophysiological rules of reptilian herbivory Robert E. Espinoza†‡, John J. Wiens§, and C. Richard Tracy¶ †Department of Biology, California State University, Northridge, CA 91330-8303; §Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11794-5245; and ¶Ecology, Evolution, and Conservation Biology and Biological Resources Research Center, MS 314, University of Nevada, Reno, NV 89557 Edited by David B. Wake, University of California, Berkeley, CA, and approved October 2, 2004 (received for review February 23, 2004) Herbivory has evolved in many groups of vertebrates, but it is rare body temperatures (7–14). These widely reported ‘‘rules’’ of among both extinct and extant nonavian reptiles. Among squa- herbivory have been proposed as explanations for the paucity of mate reptiles, (lizards, snakes, and their relatives), <2% of the herbivorous reptiles (i.e., herbivory should not evolve in lineages >7,800 species are considered to be herbivorous, and herbivory is that are small bodied, live in cool climates, or maintain low body restricted to lizards. Here, we show that within a group of South temperatures; refs. 2, 7, 8, 11, 13, and 14). These traits may be American lizards (Liolaemidae, Ϸ170 species), herbivory has associated with physiological constraints imposed by herbivory. evolved more frequently than in all other squamates combined and For example, because most plant tissues are relatively low in at a rate estimated to be >65 times faster. Furthermore, in contrast digestible energy, large body size is favorable because it affords to other herbivorous lizards and to existing theory, most herbiv- a low mass-specific rate of energy expenditure (7, 13–16). A large orous liolaemids are small bodied and live in cool climates. Her- body can also support a voluminous gut that will increase bivory is generally thought to evolve only in reptile species that are digestive efficiency by increasing the time that food is fermented large bodied, live in warm climates, and maintain high body and assimilated (8, 9, 17, 18). Likewise, high body temperatures temperatures. These three well known ‘‘rules’’ of herbivory are may be necessary for microbial fermentation of plant tissues (9, EVOLUTION considered to form the bases of physiological constraints that 12, 18, 19), given that herbivorous vertebrates lack endogenous explain the paucity of herbivorous reptile species. We suggest that cellulases and must rely on gut endosymbionts (bacteria and the recurrent and paradoxical evolution of herbivory in liolaemids protozoa) to release the energy bound in plant cell walls (17, 18, is explained by a combination of environmental conditions (pro- 20). The need to maintain high body temperatures may explain moting independent origins of herbivory in isolated cool-climate why herbivorous reptiles are largely confined to the tropics or regions), ecophysiological constraints (requiring small body size in warm deserts (9, 11, 12). Given that these ecophysiological rules cool climates, yet high body temperatures for herbivores), and may explain the scarcity of herbivory in reptiles, changes in one phylogenetic history. More generally, our study demonstrates how or more of these three apparent constraints might allow for a integrating information from ecophysiology and phylogeny can dramatic increase in the rate at which herbivory evolves in a help to explain macroevolutionary trends. given clade. Liolaemidae consists of three genera, Ctenoblepharys, Liolae- ecophysiology ͉ macroevolution mus, and Phymaturus, and 168 species (European Molecular Biology Laboratory reptile database) of small-bodied iguanian iet is a fundamental aspect of an organism’s biology, and the lizards that are distributed primarily in southern South America Devolution of dietary strategies may have important conse- (21–24). The monotypic Ctenoblepharys is insectivorous (23) and quences for both lineages and ecosystems (1–5). Although is the sister taxon of the clade Liolaemus plus Phymaturus (25). herbivory is common in some groups of animals, it is rare among Liolaemus contains 157 species, including insectivores, omni- both extinct and extant nonavian reptiles (2, 3, 6–8). Among vores, and herbivores (9, 21–24). Phymaturus contains 10 species, squamate reptiles (lizards, snakes, and their relatives), Ͻ2% (9) all of which are herbivorous (9, 21–24). Although some research- of the Ͼ7,800 currently recognized species (European Molecular ers have suggested or provided evidence that small lizards Biology Laboratory reptile database, www.embl-heidelberg.de͞ (including some liolaemids) eat primarily plants (17, 21, 22, ϳuetz͞livingreptiles.html) are considered to be herbivorous, 26–32), reviews of herbivory in reptiles have overlooked or and herbivory is confined entirely to lizards (2, 7–9, 10). The dismissed reports of herbivory in liolaemids (2, 3, 7, 8, 18) or paucity of plant-eating reptiles suggests that there are constraints were unaware of the extent of herbivory and its unexpected limiting the evolution herbivory in this group. correlates in these lizards (10, 17, 26–32). In this study, we find that herbivory has evolved repeatedly in a clade of South American lizards (Liolaemidae with nearly 170 Materials and Methods species), likely more times than are known for all other squa- Definition and Coding of Herbivory. After a review of herbivory in mates combined, and at a rate that is Ͼ65 times faster. We also lizards (10), which found that diets are more discrete than find that herbivores in this clade have converged repeatedly on previously recognized (figure 2 in ref. 10), we adopted the a unique combination of morphological, ecological, and physi- following definitions: insectivore ϭ 0–10%, omnivore ϭ 11– ological characteristics that are strikingly different from those reported for other Recent herbivorous reptiles. We combine data on phylogeny, diet, ecology, and physiology to document This paper was submitted directly (Track II) to the PNAS office. and explain the seemingly paradoxical evolution of herbivory in Abbreviations: ND2, NADH dehydrogenase subunit II; SVL, snout–vent length. liolaemid lizards. More generally, our study suggests how the Data deposition: The sequences reported in this paper have been deposited in the GenBank interplay of ecophysiology and phylogenetic history may lead to database (accession nos. AY661892–AY661908 and AY662050–AY662079). remarkable shifts in macroevolutionary trends in diet. See Commentary on page 16713. Many researchers have noted that herbivorous lizards are ‡To whom correspondence should be addressed. E-mail: [email protected]. generally large bodied, live in warm climates, and maintain high © 2004 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0401226101 PNAS ͉ November 30, 2004 ͉ vol. 101 ͉ no. 48 ͉ 16819–16824 Downloaded by guest on September 29, 2021 50%, and herbivore ϭ 70–100%, where the percentage corre- sponds to the volumetric proportion of plant matter in the diet (Data Set 1, which is published as supporting information on the PNAS web site). Each taxon was assigned to a diet based on data from the literature or volumetric estimates of gut contents or freshly deposited feces (means of individuals for each taxon). Phylogeny Reconstruction. Phylogenetic analyses (performed with parsimony and Bayesian methods) were based on combined data matrices consisting of published (23, 33, 34) morphological data (23 characters; Data Set 2, which is published as supporting information on the PNAS web site), reproductive mode (Data Set 1), and published (35, 36) and previously unreported mito- chondrial DNA sequences (Data Set 3, which is published as supporting information on the PNAS web site), totaling 1,026 parsimony informative characters (pic). Parsimony analyses were performed by using PAUP* 4.0B10 (37) and Bayesian analyses were performed by using MRBAYES 3.0B4 (38). Sequence data for 61 liolaemid taxa and four outgroup species from a 1.7-kb fragment [referred to as NADH dehydrogenase subunit II (ND2) here- after, but consisting of eight tRNAs, the ND2 gene, and a portion of NADH dehydrogenase subunit I; 852 pic] were taken from refs. 25, 35, and 36. Two additional Liolaemus sequences were provided by J. A. Schulte (U.S. National Museum, Smithsonian Institution, Washington, D.C.) (personal communication). Se- quences from 17 additional taxa for an overlapping 1.4-kb fragment were obtained by using methods described in ref. 36. An additional 685-bp fragment (139 pic) of the 12S (small) ribosomal subunit was obtained for 30 taxa (emphasizing mem- bers of the alticolor–bibronii and elongatus–kriegi species groups of Liolaemus) by using methods described in ref. 39. Details of the phylogenetic analyses are provided in Supporting Methods, which is published as supporting information on the PNAS web site. The majority-rule consensus tree from the first Bayesian analysis of the combined data was used as the preferred topology (Fig. 1), and results from comparative analyses (described below) are based primarily on this tree. However, to address the sensitivity of these results to alternative topologies, comparative analyses were repeated on the two shortest trees from the combined data parsimony analysis, the majority-rule consensus tree from a second Bayesian analysis, and five trees from each Bayesian analysis having the highest posterior probabilities. Results were