Deep history impacts present-day ecology and biodiversity Laurie J. Vitt*† and Eric R. Pianka‡ *Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, Norman, OK 73072; and ‡Section of Integrative Biology (C0930), School of Biological Sciences, University of Texas, 1 University Station, Austin, TX 78712-0253 Edited by David B. Wake, University of California, Berkeley, CA, and approved April 4, 2005 (received for review February 9, 2005) Lizards and snakes putatively arose between the early Jurassic and correlate with phylogenetic similarity in Amazonian lizards (7) late Triassic; they diversified worldwide and now occupy many and (ii) consistency of diets within South American xenodontine different ecological niches, making them ideal for testing theories snakes independent of the assemblages in which they occur (11). on the origin of ecological traits. We propose and test the ‘‘deep Although most organismal biologists would expect trophic in- history hypothesis,’’ which claims that differences in ecological teractions to have a deep historical basis, our analysis ties one traits among species arose early in evolutionary history of major component of niche partitioning (diet) to cladogenic events in clades, and that present-day assemblages are structured largely the Mesozoic. because of ancient, preexisting differences. We combine phyloge- In an earlier analysis, we and our colleagues suggested an netic data with ecological data collected over nearly 40 years to association between ingestion of specific insects and a combi- reconstruct the evolution of dietary shifts in squamate reptiles. nation of feeding mechanisms and prey discrimination modes Data on diets of 184 lizard species in 12 families from 4 continents (7). Here, we use the best available data on lizard diets (184 reveal significant dietary shifts at 6 major divergence points, species in 12 families from 4 continents) and alternate phyloge- reducing variation by 79.8%. The most striking dietary divergence netic hypotheses of their relationships to quantitatively test two (27.6%) occurred in the late Triassic, when Iguania and Scleroglossa predictions of the deep history hypothesis: (i) a strong relation- split. These two clades occupy different regions of dietary niche ship between diet and evolutionary relationships of squamate space. Acquisition of chemical prey discrimination, jaw prehension, reptiles should exist and (ii) nodes at which major dietary shifts and wide foraging provided scleroglossans access to sedentary and occurred can be identified. hidden prey that are unavailable to iguanians. This cladogenic We chose lizard diets to test the deep history hypothesis event may have profoundly influenced subsequent evolutionary because food is a major niche axis on which lizards separate in history and diversification. We suggest the hypothesis that ancient contemporary assemblages (5, 6) and because data we have events in squamate cladogenesis, rather than present-day compe- collected over the past 35 years cut across both the evolutionary tition, caused dietary shifts in major clades such that some lizard history of lizards and their global distribution. clades gained access to new resources, which in turn led to much of the biodiversity observed today. Materials and Methods Diets. During the past four decades, we have collected dietary data cladogenesis ͉ community ecology ͉ historical ecology ͉ squamate on 184 lizard species, including 91 Neotropical and 93 desert species evolution from southwestern deserts of the United States; tropical rainforests of Nicaragua, Ecuador, and Brazil; semiarid regions of northeastern quamate reptiles are ideal for testing theories on the origin Brazil (Caatinga); Australian deserts; and the Kalahari Desert of Sof ecological traits. Their evolutionary history dates back to Africa. Detailed methods for collection of lizards and identification the early Jurassic or late Triassic (1–3), they have diversified on and measurements of prey appear elsewhere (5, 6, 13, 14). All all major continents (4), and they occupy a remarkable diversity lizards were treated in accordance with federal, state, and university of ecological niches (4–7). One theory claims that ecological regulations (Animal Care Assurance 73-R-100, approved Novem- differences result from recent factors such as shifts in availability ber 8, 1994, University of Oklahoma). Initial prey categories for of different prey types or interspecific competition (competition desert and Neotropical lizards were nearly identical, which allowed hypothesis) in which species interactions for harvesting limited us to reanalyze our data at various taxonomic levels. The original resources cause divergence in niche characteristics [food, time, Neotropical lizard data set included 30 broad prey types (13), or place (microhabitat)] (6, 8). This theory predicts that niche whereas the original desert lizard data set included 20 broad prey differences arose within a relatively recent ecological time types (6). Most differences in prey categories resulted from prey frame. Evidence supporting this theory is of two types: (i) specific to each area. Mollusks and earthworms, for example were demonstrations that assemblages containing evolutionarily dif- not found in desert lizard stomachs. We used an expanded data set ferent species separate on at least one of three major niche axes of volumetric dietary data (27 categories) for all of our combined (6), and (ii) demonstrations that species (e.g., Anolis lizards on species to construct an all-species dietary matrix. Although this islands) respond in predictable manners to introduction of procedure enters zero values for prey taxa missing in each data set, ecologically and evolutionarily similar species, shifting micro- such taxa were generally rare in all other lizard diets. Consequently, habitats and͞or diets (9, 10). Shifts in availability of different effects of differences in prey availability among sites were minimal. prey types for reasons other than competition could also stim- Diets of pooled lizard samples at all sites were dominated by 7–12 EVOLUTION ulate diet shift under such a model (adaptation to current abundant prey categories. The most common 12 prey categories conditions). Such changes would be considered ‘‘shallow’’ in a accounted for 90% of all lizards’ diets, and the first 7 categories phylogenetic sense because they occurred within an ecological accounted for 76% of all lizards’ diets. time framework. Another theory claims that differences in ecological traits among species arose early in the evolutionary history of major clades (‘‘deep history hypothesis’’) such that This paper was submitted directly (Track II) to the PNAS office. present-day assemblages may coexist largely because of ancient Abbreviation: CCA, canonical correspondence analysis. preexisting differences (7, 11, 12). Evidence supporting this †To whom correspondence should be addressed. E-mail: [email protected]. theory includes (i) demonstrations that dietary niche overlaps © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0501104102 PNAS ͉ May 31, 2005 ͉ vol. 102 ͉ no. 22 ͉ 7877–7881 Downloaded by guest on September 27, 2021 Phylogenetic Reconstruction. We constructed a composite phylo- and morphological differences heretofore attributed to foraging genetic hypothesis for the 184 lizard species based on 23 different mode (4, 7, 42, 43). Our results suggest that long ago acquisition studies (15–37) (Fig. 1), thus presenting a consensus view of of chemical prey discrimination, jaw prehension, and wide lizard evolutionary history. For the present analysis, we consider foraging opened up a new food resource base for scleroglossans, species’ membership in every clade at the family level or above. providing them access to sedentary and hidden prey that were We also consider a recent competing phylogenetic hypothesis of unavailable to iguanians. Moreover, these dietary differences squamate evolutionary history based on a combination of nu- have persisted to the present day. This quantitative result is clear (RAG-1 and c-mos) and mitochondrial (ND2 region) genes, identical to the qualitative result reported earlier (7). Whether which suggests a nontraditional relationship among the three prey discrimination by chemical cues resulted in dropping many major clades, Iguania, Gekkota, and Autarchoglossa (38). insects containing chemical defense mechanisms from lizard diets or simply resulted in selection of more profitable prey Ordination Analysis. To reconstruct the history of dietary change remains unexplored, although experimental evidence demon- in lizards, we used CCA (39), a multivariate ordination proce- strating that scleroglossans discriminate against foods containing dure that directly associates variation in one matrix (lizard diets) alkaloids suggests the former (44, 45). with variation in another (lizard phylogeny). Relationships be- Iguanians occupy a different region in the CCA plot than do tween ecological and phylogenetic characteristics of lizards have scleroglossans (Fig. 3). Iguanians feed on large numbers of ants, been previously examined by using such an analysis (40). Thus, other hymenopterans, and beetles, prey that are detected visually here we ask whether an association exists between dietary and thus available to scleroglossans as well. Scleroglossans not composition and phylogeny, and we identify divergence points in only appear to avoid ants, other hymenopterans, and beetles,