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Behavioral Ecology Vol. 14 No. 3: 409-416
© 2003 International Society for Behavioral Ecology
Correlated evolution of herbivory and food chemical discrimination in iguanian and ambush foraging lizards
Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, IN 46805, USA
Address correspondence to W.E. Cooper, Jr. E-mail: cooperw{at} ipfw.edu
Received 18 December 2001; revised 7 August 2002; accepted 21 September 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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To efficiently locate and assess foods, animal sensory capacities and behavioral discriminations based on them must be appropriate for the diet and method of hunting. In lizards, actively foraging insectivores identify animal prey using lingually sampled chemical cues, but ambush foragers do not. Among plant eaters derived from active foragers, plant chemical discrimination is added to prey chemical discrimination, resulting in correlated evolution of plant diet and plant chemical discrimination. Here I present comparative evidence on the relationships between plant diet and food chemical discrimination in Iguania, which consists primarily of ambush foragers and is one of two major lizard clades, and for ambushing lizards in general. Comparative analyses conducted using phylogenetic methods show that (1) all but one species of omnivore studied exhibited both prey and plant chemical discrimination, whereas ambush foragers exhibited neither; (2) significant correlated evolution occurred between plant diet and plant chemical discrimination in Iguania and in omnivores and herbivores derived from ambush foragers; and (3) correlated evolution has occurred between prey and plant chemical discrimination in Iguania and, more generally, in taxa derived from ambush foragers. These results are explained by selection on plant eaters to assess the nutritional value and possible toxicity of plants and by continued consumption of some animal prey even in herbivores combined with freedom from factors that select against prey chemical discrimination in ambush foragers.
Key words: behavior, evolution, foraging mode, food chemical discrimination, lizards, Squamata.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Relationships between sensory capacities used to detect and evaluate food and diets and hunting methods provide some spectacular examples of sensory adaptation, among them the extreme light-sensitivity of owls, geckos, and other nocturnal hunters (Walls, 1942
), the impressive visual acuity of raptors (Walls, 1942), infrared detectors of rattlesnakes and pythons (Greene, 1997), ultrasonic detectors of bats (Griffin, 1958) and cetaceans (Kamminga, 1988; Wiersma, 1988), and many others. Although the sensory capacities in these cases very likely evolved at least in part to improve foraging abilities in the face of particular environmental constraints on detecting food, evolutionary relationships between environmental factors and these specialized sensory abilities have not been established in most cases. In some, this is due to lack of study, but in others there may have been insufficient independent origins of the abilities to assess whether correlated evolution has occurred between the environmental factor and the sensory trait.
An exception is the evolutionary dependence of chemosensory responsiveness in squamate reptiles on hunting techniques and diets. In lizards there is a strong relationship between foraging mode and chemosensory location and identification of prey. Prey chemical discrimination evolves in lineages that adopt active foraging and is lost in those that abandon it to become ambushers (Cooper, 1995, 1997, 2000a). Relationships between diet and chemosensory response and even whether they are heritable are known only for garter snakes. In the garter snake Thamnophis elegans, strength of chemosensory responses changes concordantly with dietary preferences over the geographic range, and diet and response are heritable (Arnold, 1981a,b). Although concordance between geographically variable diets and chemosensory response has been observed in a few other snakes (e.g., Burghardt, 1967, 1970a,b; Cooper et al., 2000), correlated evolution between diet and chemosensory behavior has not been established comparatively among snakes or other lizards.
The two major clades of lizards, Iguania and Scleroglossa, exhibit pronounced differences in foraging behavior. Iguania consists of ambush-foraging insectivores and a small percentage of herbivores and omnivores that have been derived from ambush foragers. Scleroglossa primarily includes actively foraging insectivores but also includes many ambush foragers (especially among geckos), as well as a small percentage of omnivores and herbivores (Cooper, 1994a,b; Cooper and Vitt, in press; Perry, 1995, 1999). Lizards that search actively for food tongue-flick to collect chemical cues as they move through the habitat, but ambush foragers wait at fixed posts for prey to approach (Cooper, 1994a,b; Evans, 1961). Although the percentage of time spent moving and the number of movements per minute vary among species within each foraging mode, the majority of lizard species fall into two distinct groupings on the movement spectra, iguanians and gekkonids, almost all falling within the range of ambush foragers (Perry, 1999).
Correlated evolution has occurred between plant consumption and the ability to identify plant foods using chemical cues in Scleroglossa and in one of its subtaxa in which nearly all species are active foragers or plant eaters derived from them (Cooper and Vitt, 2002). The evolutionary relationship between plant consumption and plant chemical discrimination is unknown in Iguania, as is the relationship between ambush foraging and plant chemical discriminations in ambush foragers. Although ambush foragers lack prey chemical discrimination, the first study of food chemical discrimination in an iguanian herbivore, Dipsosaurus dorsalis, a member of a lineage derived from ambushers, revealed a well-developed capacity to recognize both animal and plant foods using lingually sampled chemical cues (Cooper and Alberts, 1990). This and subsequent findings suggested that adoption of a plant diet might have two major selective effects on food chemical discrimination. First, because the lizards consume plants, selection should favor an ability to identify them for several possible reasons. Ambush foragers typically respond visually to moving prey, but omnivores and herbivores may frequently need to identify immobile plant parts as food. Plant parts such as leaves and fruits vary greatly in their digestibility and nutritional value with maturity, and some of these differences may not be detectable using visual cues, suggesting that lizards eating them would benefit from an ability to chemically assess nutritional quality (Cooper and Alberts, 1990). Avoidance of plant defensive toxins is another potentially important impetus for evolution of plant chemical discrimination by lizards. An ability to detect plant toxins has been demonstrated in two species of scleroglossan omnivores (Cooper et al., 2002; Schall, 1990).
The other major hypothetical effect of incorporating plants into the diet is evolution of prey chemical discrimination. This ability would be useful for omnivores and even herbivores, which continue to consume some animal prey (reviewed by Cooper and Vitt, 2002). Because ambush foragers remain immobile while waiting for prey to approach them, tongue-flicking substrates might provide them some information about the recent presence of prey when they first adopt an ambush station, but they cannot gain additional information useful for locating prey by repeated tongue-flicking at the same site (Cooper, 1995, 1997). The movement of tongue-flicking conflicts with their primary defense of crypsis through immobility (Vitt and Price, 1982) and might reveal the presence of the lizard to prey or predators. Because lizards that eat plants must move through the habitat to locate them and because many of them are large (Cooper and Vitt, 2002; Pough, 1973), immobility is not an option, and prey chemicals may be encountered during movements through the habitat and while foraging on plants.
I predicted that omnivorous and herbivorous lizards, both iguanians and those derived from ambush foragers in general, are capable of both prey and plant chemical discrimination and that there has been correlated evolution between plant diet and these discriminations. In cases of reversion from plant consumption to insectivory and ambush foraging, I predicted loss of prey and plant chemical discrimination. The findings of a comparative study using phylogenetic methods are reported here.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Evolution of plant consumption and plant chemical discrimination
To assess the evolution of omnivory and herbivory, I reviewed the literature on diets of iguanian lizards. A few iguanian species undergo ontogenetic increases in plant consumption (e.g., Durtsche, 2000
; Cooper and Vitt, 2002). I used dietary data for adults. Diets were mapped on the phylogeny of Iguania (Estes et al., 1988; Frost and Etheridge, 1989; Macey et al., 1997; Moody, 1980; Schulte et al., 1998). Because some aspects of the phylogeny of Iguania are uncertain, I used four alternatives that span the range of phylogenies that have some empirical support and are likely to affect the analyses. One of these, phylogeny 1, is shown in Figure 1, which shows species for which food chemical discrimination has been studied. Phylogeny 1 shows relationships among Acanthodactylus, Chamaeleo, Leiolepis, and Pogona supported by morphological data (Moody, 1980; Macey et al., 1997) and among other iguanians as supported by molecular data, with the exception that Tropidurus and Phymaturus are shown as more closely related to each other than to Crotaphytus, a relationship supported by morphological and combined data (Schulte et al., 1998). Phylogeny 2 differs from phylogeny 1 only in that Leiolepis belliana is the sister of Chamaeleo pardalis, which is supported by Schulte et al. (1998). With the exception that Phymaturus is the sister of Iguanidae (the three rightmost species in Figure 1, supported by molecular data of Schulte et al., 1998), phylogeny 3 is identical to phylogeny 1, and phylogeny 4 is identical to phylogeny 2. For additional tests of the broader relationship between plant diet and chemical discriminations in ambush foraging lineages, I added data for two gekkonid species, inserting them as the sister taxon of Iguania.
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Sixteen iguanian species, 3 gekkonoid species, and the tuatara Sphenodon punctatus (Table 1) were studied as representatives of the major iguanian clades and as an outgroup, respectively. Iguania and Gekkonoidea include more than 1000 species each, but small samples are adequate for testing the relationship between diet and food chemical discrimination because (1) the majority of species are insectivores, and all 26 (22 iguanians, 4 gekkonids) species of insectivores studied in these groups lack prey chemical discrimination (Cooper, 1994b
, 1999; Cooper and Vitt, 2002); (2) only 9 independent origins of omnivory and herbivory are known within Iguania (although more may have occurred) and one or two independent origins in Gekkonoidea (Cooper and Vitt, in press); and (3) yhe sample includes representatives of at four or five independent origins in Iguania and one in Gekkonoidea (Figures 1, 2).
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Each species was identified as insectivorous or omnivorous/herbivorous from the literature and as using or not using plant chemical discrimination. The experimental methods and inferences about chemosensory discriminations were consistent among studies because I conducted or participated in all of them. The experiments tested whether the lizards are capable of lingually mediated plant food chemical discrimination, presumably mediated by vomerolfaction, which detects primarily large, nonvolatile molecules sampled by tongue-flicking (Cooper and Burghardt, 1990
; Halpern, 1992). Blocking vomerolfaction eliminates lingually mediated discrimination between food chemicals and control stimuli even if olfaction remains intact, whereas elimination of olfaction does not prevent discrimination (Cooper and Alberts, 1991; Graves and Halpern, 1990; Halpern and Frumin, 1979). Omnivorous, herbivorous, and insectivorous species were selected for study of plant chemical discrimination to facilitate comparisons between diet and chemosensory responses in relation to iguanian phylogeny. The 10 insectivorous species were selected to represent the major clades of iguanian and gekkonid insectivores and the outgroup.
The evolution of plant diet and plant chemical discrimination were reconstructed on all four phylogenies using the TRACE routine of MacClade 3.01 (Maddison and Maddison, 1992). TRACE assigns the ancestral character states by assuming parsimony. Because herbivory and plant chemical discrimination have evolved so infrequently, multiple gains and losses within branches are very unlikely to have been obscured, with the possible exception of Agamidae. Characters traced were considered unordered, and character states were resolved initially using all most parsimonious states rather than only accelerated or delayed transformations. Where the evolution of traits was equivocal, I considered both possible alternatives by assuming delayed and accelerated transformations separately. Because dietary and behavioral characters were not used to determine the phylogeny of Iguania, they are presumably independent of characters that were used. Maximum likelihood methods also can be used to reconstruct character evolution (Pagel, 1994, 1999). They have the advantage of providing an indication of the degree of support for reconstructions at each node but were not used in this study because large numbers of calculations are required for each phylogeny. Given the uncertainties of each phylogeny, the precise reconstructions are less important than establishment that correlated evolution has occurred regardless of which phylogeny is used.
Correlated evolution
I tested three hypotheses: (1) adoption of a plant diet is accompanied by acquisition of plant chemical discrimination in Iguania and in (2) ambush foragers in general; and (3) evolution of omnivory and herbivory by species derived from ambush foragers leads to transitions to both prey and plant chemical discrimination. The first tests were traditional tests for association between characters that did not take into account the phylogenetic relationships among species. This sort of analysis is not valid because the data points are not independent due to sharing of diets and/or chemosensory behaviors retained from common ancestors by some species (Brooks and McLennan, 1991; Harvey and Pagel, 1991). The tests were conducted to determine whether use of phylogenetic and nonphylogenetic methods leads to similar inferences.
I used concentrated changes tests (Maddison, 1990; Maddison and Maddison, 1992) and Pagel's (1994) tests to take phylogenetic relationships into account. The concentrated changes test examines the hypothesis that one binary variable causes changes in the other (Maddison, 1990; Maddison and Maddison, 1992). The major hypothesis tested here is that addition of substantial plant component to the diet (independent variable) favors natural selection for ability to identify food plants using lingually samples chemical cues (dependent variable). All tests were conducted using exact counts of all possible trees rather than simulations.
The concentrated changes test requires fewer changes to have adequate statistical power than some other tests for discrete variables (Ridley, 1983; Sillén-Tullberg, 1993) and is well suited for testing the hypothesis that change in diet causes change in chemosensory responsiveness. It was criticized for being subject to bias due to selection of taxa not representative of the entire group (Sillén-Tullberg, 1993). However, Lorch and Eadie (1999) found that changing the proportion of branches lacking both traits does not affect the probability of type I errors, and that for trees having less than 20% of branches lacking both traits, the probability of type II errors increases, making the test too conservative. The concentrated changes test is also conservative when only gains occur for a trait, but not losses, which is the case for several of the tests conducted here. Concentrated changes tests may suffer from reduced power if both characters change on the same branch (Pagel, 1994), which is the case for all but one change here. The data (Table 1) include several omnivores, herbivores, and insectivores in the same or closely related lineages. Levels of phylogenetic resolution were as similar as possible among branches of the iguanian tree to avoid possible problems for concentrated changes tests due to biased sampling of branches (Sillén-Tullberg, 1993).
Pagel's (1994) tests for correlated evolution between discrete characters have the advantages of taking into account both the branching structure and branch lengths of a phylogeny and of using maximum likelihood methods to analyze trait evolution. This allows tests for directional trait evolution and tests for causation in some cases of correlated evolution. However, these latter two tests cannot be used make inferences for the lizard data because both traits change simultaneously on all but one branch. The main disadvantage of Pagel's tests is that branch lengths must be known. In the case of iguanian lizards, divergence times among some families are poorly known. However, estimates taken from published paleontological and other phylogenetic sources, primarily from Estes (1983) and Garland (1994, and associated unpublished appendix), undoubtedly represent an improvement over the assumption of equal branch lengths that is implicit in concentrated changes tests. These tests were conducted for all four phylogenies with and without the two species of geckos, using 1000 simulations each to test for correlated evolution between plant diet and plant chemical discrimination. Similar tests were not conducted for correlated evolution between plant chemical discrimination and prey chemical discrimination because the calculations were far too slow to be useful or did not operate properly, even using branch length scaling.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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For the nonphylogenetic analysis assuming that the data for each iguanian species are independent of historical influences, there are seven species that are herbivores or omnivores that are capable of prey and plant chemical discrimination, eight species that are insectivores lacking prey and plant chemical discrimination, and one omnivore lacking prey and plant chemical discrimination. Herbivory was significantly associated with both prey and plant chemical discrimination (Fisher
). The evolution of both plant consumption and prey and plant chemical discrimination was equivocal in agamine chamaeleonids in all likely iguanian phylogenies. Figures 1 and 2 show phylogeny 1 with character states resolved by delayed and accelerated transformation, respectively. The evolutionary history of plant diet in Iguania as reconstructed by parsimony varies somewhat with the phylogeny used (Table 2). In all four phylogenies the only species for which reconstructions of the two traits differed was the phrynosomatid Sceloporus poinsettii, which is a herbivore that lacks plant chemical discrimination.
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In the phylogenetic analyses using concentrated changes tests, significant correlated evolution between herbivory and both prey and plant chemical discrimination was detected in Iguania on all four phylogenies (Table 2). Due to the lack of resolution of character states in Agaminae in all phylogenies, I conducted separate tests for each phylogeny assuming delayed or accelerated transformation of changes (Table 2). Despite the small numbers of origins and losses of both traits, results were significant because nearly all origins and losses of prey and plant chemical discrimination occurred on identical branches of the trees for these traits and plant diet in all phylogenies with the sole exception that herbivory evolved in S. poinsettii with no corresponding acquisition of prey or plant chemical discrimination. Only in the case of delayed transformation with phylogeny 3 was the correlation not clearly significant, but in that case it was very nearly so.
Pagel's test for all four iguanian phylogenies corroborated the findings of the concentrated changes tests (Table 2). Significant correlated evolution occurred between plant diet and both plant and prey chemical discrimination (
). Based on 10 calculations each, the likelihood ratios for the phylogenies were: phylogeny 1, 
(
); phylogeny 2, 
; phylogeny 3, 
; and phylogeny 4, 
. The actual p values are presumably much lower because none of the likelihood ratios of the 1000 simulations closely approached the test value for any of the phylogenies (greatest simulated ratios were 9.37, 12.75,10.48, and 12.19 for the phylogenies 1–4, respectively).
Prey chemical discrimination in Iguania was significantly correlated with plant chemical discrimination in concentrated changes tests for all four phylogenies under delayed and accelerated transformation (Table 2). Although only four or five changes in each trait occurred in the four phylogenies, changes in the two traits corresponded perfectly, with acquisition of both plant and prey chemical discrimination or their joint loss occurring in the same species in all cases.
Concentrated changes tests of the more general relationship between plant consumption and ambush foraging including geckos were significant for all four phylogenies under both delayed and accelerated transformation of characters. The significance levels in all cases were slightly lower than for the corresponding tests within Iguania (Table 2): phylogeny 1 (delayed transformation, 
; accelerated transformation, 
); phylogeny 2 (delayed, 
; accelerated, 
); phylogeny 3 (delayed, 
; accelerated, 
); and phylogeny 4 (delayed, 
; accelerated, 
). Pagel's tests also revealed significant correlated evolution between plant diet and plant chemical discrimination among ambush foragers (
for each phylogeny). Based on 10 calculations each, the likelihood ratios for the phylogenies were: phylogeny 1, 19.48 ± 0.02 (mean ± SE); phylogeny 2, 18.48 ± 0.42; phylogeny 3, 18.86 ± 0.03; and phylogeny 4, 18.69 ± 0.39. The actual p values are presumably much lower because none of the likelihood ratios of the 1000 simulations closely approached the test value for any of the phylogenies (greatest simulated ratios were 10.29, 10.09, 12.75, and 12.57 for the phylogenies 1–4, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Plant diet and plant chemical discrimination have undergone correlated evolution in Iguania, as indicated by seven of the eight tests in Table 2 and marginally by the eighth test. To attain significance despite the scarcity of independent origins of omnivory in Iguania, the relationship had to be and was very strong. Whether the changes were all gains of the traits, as in the tests using trees with delayed transformation, or a mixture of gains and losses, as in the tests with accelerated transformation, plant diet or plant chemical discrimination changed together on the same branches in all but one instance.
The exception was S. poinsettii, which evolved omnivory without acquiring plant or prey chemical discrimination. Because this species appears to consume plants in substantial quantities in some years, but not in others (Barbault et al., 1985), plant consumption may not be consistent or predictable enough to have produced strong selection favoring plant chemical discriminations (Cooper et al., 2001a). Alternatively, there might be unknown constraints on evolution of food chemical discrimination in Phrynosomatidae.
Whatever the reason for the lack of food chemical discrimination in S. poinsettii, plant diet and plant chemical discrimination are strongly associated in Iguania. The same is true for plant diet and prey chemical discrimination because prey chemical discrimination occurs only in omnivorous and herbivorous species, and in all of them. Thus, there has been correlated evolution between plant consumption and prey chemical discrimination at the same significance levels found for the relationship between plant diet and plant chemical discrimination.
Plant chemical discrimination and prey chemical discrimination have also undergone correlated evolution, as shown by the significant association between them in all eight phylogenetic tests in Table 2. The perfect agreement between these traits in which all species either have both traits or lack both supports the hypothesis that prey chemical discrimination would evolve in omnivorous and herbivorous lizards because they are freed from constraints of ambush foraging and could benefit from using chemical cues to identify prey. Because both prey and plant chemical discrimination are mediated by vomerolfaction (Cooper and Alberts, 1991; Cooper and Burghardt, 1990; Halpern and Frumin, 1979), selection for plant chemical discrimination might lead to improvements in vomerolfactory capacity that also facilitate prey chemical discrimination. Evolution of both traits might be hastened by selection for improved vomerolfactory sensitivity for each trait. In either case, it is likely that sensitivity to types of chemicals found in both plant and animal foods would facilitate evolution of ability to identify both types of food (Cooper, in press). However, the two traits are not inextricably linked because insectivorous active foragers in Scleroglossa do not exhibit plant chemical discrimination (Cooper, in press).
The association between plant diet and plant chemical discrimination in lineages of ambush foragers is even stronger than in Iguania due to the correspondence between these traits in the scleroglossan geckos in Table 1 added to the iguanian data. The occurrence of prey and plant chemical discrimination in the omnivorous geckos of Rhacodactylus (Cooper, 2000b) shows that evolution of these traits in omnivores derived from ambush foragers is not restricted to Iguania. Similarly, although no statistical tests were conducted, the association between the two types of food chemical discrimination clearly is even stronger for trees including the geckos than for Iguania alone due to the presence of both traits in Rhacodactylus and their absence in G. gecko (Cooper, 2000c; Cooper and Habegger, 2000). These findings suggest that the reasons for correlated evolution may not be related to iguanian traits per se but to ambush foraging, as hypothesized.
Foraging mode has had a pervasive influence on the evolution of lizards. Ambush foragers have tongues that are not specialized for chemical sampling and low abundance of vomerolfactory chemoreceptor cells, whereas active foragers have evolved elongated, forked tongues for improved chemosensory sampling, including trailing (Cooper, 1996b; Schwenk, 1994), and abundant vomerolfactory receptors (Cooper, 1996a). Active foragers are more likely to eat hidden prey (Huey and Pianka, 1981) and to be omnivorous or herbivorous than are ambush foragers (Cooper and Vitt, 2002). Active foragers also have more streamlined bodies and lower clutch mass relative to body mass than ambush foragers (Vitt and Congdon, 1978), are more subject to attack by ambush predators (Huey and Pianka, 1981), rely more on escape than crypsis to avoid predators (Vitt and Price, 1982), and may be less likely to be territorial (Huey and Bennett, 1986). The present findings and related ones in Scleroglossa (Cooper, in press) add responses to food chemicals by omnivores and herbivores to the list of adaptations influenced by foraging mode.
The absence of prey chemical discrimination in ambush foragers has been explained as a consequence of inability to obtain information by repeated sampling at a single location and as possibly a result of constraints from immobility to avoid being detected by predators and prey (Cooper, 1995, 1997). In the introduction of this paper I hypothesized that omnivores and herbivores are freed from such constraints associated with immobility, which permits them to tongue-flick frequently and that they encounter plant food and prey that can be identified or assessed for nutritional value by chemical cues. Aspects of ambush foraging thus can account for the absence of prey chemical discrimination in ambush foragers and the presence of prey and plant chemical discrimination (in part) in omnivores and herbivores derived from ambush foragers. Plant chemical discrimination is fundamentally an adaptation to permit chemosensory assessment of nutritive and possibly toxic properties of plants in plant eaters derived from both ambush and active foragers.
The data support all predictions for iguanians based on consequences of ambush foraging, and the support is even stronger when scleroglossan data are added, but might there be viable alternative hypotheses? In plant eaters derived from ambushers, prey chemical discrimination might evolve in tandem with plant chemical discrimination due to genetic correlation between them and have nothing to do with elimination of constraints on tongue-flicking. This seems unlikely due to the lack of plant chemical discrimination in actively foraging insectivores (Cooper, in press). Because lizards must seek out food plants rather than lying in ambush for them, diet is confounded with foraging mode, and the movement of plant eaters derived from ambush foragers is one of the arguments for the utility of tongue-flicking to locate prey. No viable competing hypotheses have been advanced, and none are apparent. Selection for food chemical discriminations is founded in diet, but responses to prey cues are strongly constrained by ambush foraging.
The conclusions based on concentrated changes tests and Pagel's tests were nearly identical despite the fundamental difference that the former uses parsimony and the latter maximum likelihood. Nevertheless, the p values for Pagel's tests were lower for all phylogenies in tests for iguanians only and iguanians plus geckos. Making use of information on branch lengths, even rough estimates, presumably accounts for the ability of Pagel's tests to detect correlated evolution at lower p values than the concentrated changes tests. Thus, when concentrated changes tests reveal correlated evolution, they may be conservative. In other cases, they may fail to detect real correlated evolution when information about branch lengths supports its occurrence.
Although Pagel's tests are superior due to inclusion of information about branch lengths, they are more difficult to implement, requiring lengthy calculations. The simulations for Pagel's tests in the present study required 9 days, including runs at night. Worse, the calculations did not work for testing the relationship between prey chemical discrimination and plant chemical discrimination. The only difference in the files used to test for correlated evolution between plant diet and plant chemical discrimination and between prey chemical discrimination and plant chemical discrimination was that in the former there was one species that was herbivorous but lacked plant chemical discrimination, whereas in the latter the same species lacked both plant chemical discrimination and prey chemical discrimination. In the tests that could not be completed, there were no species in two of the four possible combinations of two traits.
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ACKNOWLEDGEMENTS |
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I thank my numerous colleagues who have helped me to obtain animals and collect data for the experimental studies needed for this comparative analysis. I am also grateful to G. M. Burghardt, D. Chiszar, R. B. Huey, E. R. Pianka, K. Schwenk, and L. J. Vitt for their ideas about foraging, chemical senses, and diet that interested me in undertaking this work.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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