Journal of Herpetobgy, Vol. 35, No. 1, pp. 1-12, 2001 Copyright 2001 Society for the Study of Amphibians and

Evolutionary Relationships of the bimaculatus Group from the Northern

CHRISTOPHER J. SCHNEIDER/-^ JONATHAN B. LOSOS/ AND KEVIN DE QUEIROZ^

'Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA ^Department of Biology, Boston University, Boston, Massachusetts 02215, USA ^Department of Biology, Washington University, St. Louis, Missouri 63130, USA ''Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA

ABSTRACT.• in Ihe group from the northern Lesser Antilles have played an important role in theoretical and empirical developments in ecology, behavior, and evolution over the last four decades. Despite intense interest, the lack of a formal phylogenetic analysis for the bimaculatus group has limited comparative and historical evolutionary analyses. Here we present a phylogenetic analysis of species relationships within the bimaculatus group based on separate and combined analyses of mitochon- drial DNA and previously published allozyme data. These analyses indicate that (1) the wattsi group of small anoles is a basal, well-supported monophyletic group; (2) the large anoles A. bimaculatus and A. leachi are not sister species•rather, there is a well-supported sister relationship between A. bimaculatus and A. gingivinus; (3) the A. marntoratus complex from the Guadeloupean archipelago is deeply differentiated and paraphyletic, with A. sabanus, A. lividus, and possibly A. oculatus nested within it; (4) the phylogenetic position of A. leachi is not well resolved, but a combined analysis of mtDNA and allozyme data favor placing A. leachi as the sister to the {A. marmoratus, A. lividus, A. sabanus, A. oculatus) group; and (5) the phylogenetic position of A. nubilus remains uncertain pending additional data. The proposed phylogeny elucidates the evolutionary history and biogeography of the bimaculatus group and allows a reassessment of the character displacement and taxon cycle/loop hypotheses.

The radiation of Anolis lizards is dian anoles (Underwood, 1959; Etheridge, 1960). one of the best known cases of adaptive radia- A number of phylogenetic hypotheses, often tion (reviewed in Williams, 1983; Losos, 1994; conflicting with each other, have been proposed Jackman et al., 1997; Jackman et al., 1999). More for the two groups (e.g., Lazell, 1972; Yang et al., than 100 of the approximate 140 species of Ca- 1974; Gorman and Kim, 1976; Roughgarden et ribbean anoles occur on the islands of the Great- al., 1987). Given the advent of DNA sequencing er Antilles, where most research has been con- and advances in analytical techniques, the time ducted. Nonetheless, the 20 species from the seems ripe for a new look at the phylogeny of Lesser Antilles have received significant atten- these groups, particularly given the great tion, including studies of locomotor behavior breadth of information that could be interpreted (Moermond, 1986), habitat use (Roughgarden et in an evolutionary context once a robust hy- al., 1981, 1983; Losos and de Queiroz, 1997; pothesis of relationships is obtained. Recently, Staats et al., 1997), size evolution (Roughgarden such a hypothesis has been derived for the ro- and Pacala, 1989; Losos, 1990), interspecific in- quet group in the southern Lesser Antilles (D. A. teractions (Pacala and Roughgarden, 1982; Creer, K. de Queiroz, T R. Jackman, J. B. Losos, Roughgarden et al., 1984, 1987; Rummel and and A. Larson, unpubl. data). Here, we present Roughgarden, 1985; Schall, 1992), social behav- a phylogeny for the bimaculatus group of the ior (e.g.. Stamps, 1991; Stamps and Krishnan, northern Lesser Antilles based on analysis of 1994a, b, 1995, 1997, 1998); phenotypic and ge- mtDNA sequence data in combination with pre- netic differentiation (Malhotra and Thorpe, viously published allozyme data (Gorman and 1991a, b, 1993, 1994, 1997a, b; Schneider, 1996), Kim, 1976). and (Malhotra and Thorpe, 1991a, 1994). MATERIALS AND METHODS Traditionally, anoles of the Lesser Antilles We sequenced a portion of the mitochondrial have been classified in two distantly related cytochrome b (cyt b) gene from at least two in- groups, the roquet group in the southern Lesser dividuals from each of 20 populations repre- Antilles (north to ), allied to certain senting all species from the bimaculatus group South American taxa, and the bimaculatus group (sensu Etheridge, 1960; Gorman and Kim, 1976), in the northern Lesser Antilles (from plus one individual from a Puerto Rican out- northward, see Fig. 1), related to other West In- group A. cristatellus. The only taxon missing C. J. SCHNEIDER ET AL.

had been frozen or fixed in absolute ethanol, using standard phenol-chloroform or NaCl extractions (Maniatis et al., 1982; Miller et al., 1988). We amplified nearly the entire cyt b gene via the Polymerase Chain Reaction with primers MVZ49-M13RSP (CGAAGCTTGATAT- A. tífnaajñivt GAAAAACCATCGTTGATAA[A/ G]AACAATGACAAT[C/T]ATACGAA), a light- A. fnafmaralus £TP. il^ strand primer with the 3' end at position 16267 of the Xenopus mitochondrial genome (Roe et al.,

A. nr. Intttia ai 1985), and MVZ14-M13SP (CGCCAGGGTTTT- CCCAGTCACGACGGTCTTCATCT[C / T] [C /T/A]GG[T/C]TTACAAGAC), a heavy strand primer whose 3' end is in the Threonine tRNA at position 17422 of the Xenopus genome. We then generated single-stranded DNA via asym- metric amplification (Gyllensten and Erlich, 1988) using these same primers at 1:50 concen- tration. Asymmetric amplifications with these FIG. 1. Distribution of species on islands of the primers provided single-stranded template of a northern Lesser Antilles and their relative body size (after Schoener, 1970): I = intermediate; S = small; 1110-base-pair (bp) fragment of the cyt b gene and L = large. for direct sequencing. Primers MVZ14-M13SP MVZ49, and cyt b2 (Kocher et al., 1989) were used for sequencing with the Sequenase® '^S se- from our analysis was Anolis nubilus for which quencing protocol. To assess the utility of the cyt tissues were unavailable. Locality and voucher b gene for this study, we initially sequenced specimen information are contained in Table 1. both light and heavy strands of the 363-bp frag- DNA was prepared from liver tissue, which ment corresponding to codons 11-131 of the

TABLE 1. Specimens examined.

A. m. setosus Plage de Clugny, north end Basse Terre, (N = 2) A. m. marmoratus St. Sauveur, southeastern Basse Terre, Guadeloupe (N = 2) A. m. speciosus Pointe-a-Pitre, Grande Terre, Guadeloupe (N = 2) A. m. alliaceus N Col des Mamelles, 600 m elevation, Basse Terre, Guadeloupe (N = 2) A. m. alliaceus N Trace Victor Hugues, 500 m, Basse Terre, Guadeloupe (N = 2) A. m. girafus Baillif, southwestern Basse Terre, Guadeloupe (N = 2) A. m. girafus Bouillante, western Basse Terre, Guadeloupe (N = 2) A. m. desiradei 1 km N of Beausejour, He de la Desirade, Guadeloupe (N = 2) A. m. chrysops Terre de Bas, Iles de la Petite Terre, Guadeloupe (N = 2) A. m. inornatus Le Moule, Grande Terre, Guadeloupe (N = 2) A. m. alliaceus S Bains Jaunes, 1000 m, southern slope of Soufrière, Basse Terre, Guadeloupe (N = 2) A. (m.) ferreus 1 km N St. Louis, Marie Galante, Guadeloupe (N = 2) A. m. terraealtae Plage de Pompierre, east end of Terre de Haut, Les Iles des Saintes, Guadeloupe A. m. terraealtae Plage de Figuierre, west end of Terre de Haut, Les Iles des Saintes, Guadeloupe A. 0. oculatus Vicinity of Canefield, Dominica A. 0. winstoni Vicinity of Marigot, Dominica A. bimaculatus St. Eustatius A. bimaculatus Vicinity Boyd's, Trinity Parish, St. Kitts (N = 2) A. ivattsi St. Mary's Parish, A. ivattsi St. George's Parish, Antigua A. schzmrtzi Trinity Parish, St. Kitts (N = 2) A. lividus St. Anthony Parish, (N = 2) A. leachi St. Mary's Parish, Antigua A. leachi St. George's Parish, Antigua A. gingivinus Baie aux Prunes, St. Martin A. gingivinus Baie Rouge, St. Martin A. pogus Pic Paradis, St. Martin (N = 2) A. sabanas Windwardsidea, (N = 2) A. acutus St. Croix, U.S. Virgin Islands (N = 2) A. c. cristatellus Hwy 304 just south of Hwy 116 to Parguera, Puerto Rico ANOLIS PHYLOGENY

Xenopus genome (Roe et al., 1985) using primers among taxa (see Berlocher and Swofford, 1997). MVZ49 and cyt b2. We then sequenced the Under the MANOB criterion, internal node as- heavy strand of a 333-bp fragment, correspond- signments are limited to those states observed ing to codons 271-380 in the Xenopus genome, in the terminal taxa. from at least one individual from each locality In addition, we combined the allozyme and using primer MVZ14-M13SP. This latter region mtDNA data in a parsimony analysis. Because encompasses the variable portion of the gene C T changes as one step and all other chang- and Palumbi, 1993; Meyer, 1994; Irwin et al., es as two steps. Second positions were unor- 1991). Sequences were aligned by eye using the dered and given a weight of two so that all amino acid sequences of translated DNA se- changes were counted as two steps. We applied quences. a step matrix to third positions, which counted For phylogenetic analyses of mitochondrial transversions as two steps and transitions as DNA (mtDNA) data, we used both parsimony one. Finally, we applied the Manhattan distance and maximum likelihood methods as imple- step matrices to the allozyme characters and as- mented in PAUP* 4.0d64 (Swofford, 1998). We signed a weight of two to each of those char- treated each nucleotide position as a multistate acters. This resulted in allozyme changes (the character with up to four states and, for parsi- origin of a new alíele) being counted as two mony analyses, employed various weighting steps, equivalent to nonsynonymous substitu- schemes for transitions and transversions, and tions and third position transversions in the synonymous and nonsynonymous base substi- mtDNA. In the combined analysis, all taxa were tutions (detailed below). For maximum-likeli- retained even though allozyme data were lack- hood (ML) analyses we used a general time re- ing for several of the taxa within the Anolis mar- versible model with gamma-distributed rate moratus complex, and mtDNA data were lacking variation. Both the alpha shape parameter of the for A. nubilus. gamma distribution and number of invariant sites were estimated using maximum likeli- RESULTS hood. Nucleotide frequencies were set to the ob- We obtained 696-bp of cyt b sequence from 48 served frequency of each nucleotide in the entire individuals of Anolis from the Northern Lesser dataset. Trees were rooted with Anolis cristatel- Antilles (sequences available in Genbank, Ac- lus, a member of the closely related cristatellus cession numbers AF212110-AF212129). Se- species group (Etheridge, 1960; Williams, 1976), quence differences within localities were gen- as the sole outgroup in each analysis. erally low, with zero to three silent transitions To examine phylogenetic signal in different between sequences in A. ferreus (N = 2), A. m. types of character state change at different hi- desiradei (N = 2), A. m. inornatus (N = 2), A. erarchical levels of relationship, we used the pogus (N = 2), A. sabanus (N = 2), A. bimaculatus skewness of the tree length distribution (Hillis, (N = 3), A. leachi (N = 2), A. gingivinus (N = 2), 1991; Hillis and Huelsenbeck, 1992) generated A. lividus (N = 2), A. m. chrysops (N = 2), A. m. from 10,000 random trees or from all trees when terrealtae (N = 2), and A. acutus (N = 2). Se- the number of taxa included was < 10. To esti- quences within A. oculatus {N = 2) differed by mate the degree of support for phylogenetic nine silent transitions, whereas sequences with- groupings, we calculated decay indices for each in A. wattsi (N = 2) and A. schwartzi (N = 2) (Bremer, 1988; Donoghue et al, 1992) and differed at 21 and 17 sites respectively. Sequenc- performed phylogenetic analyses on 1000 boot- es from populations of A. marmoratus on the strap replicates of the dataset (Felsenstein, 1985). main islands of the Guadeloupean archipelago We analyzed the allozyme data of Gorman display strong geographic structure (Schneider, and Kim (1976) both separately and in combi- 1993, 1996) and differed at up to 65 sites (9.3% nation with the mtDNA data. We constructed observed sequence divergence; Table 2). Fitch-Margoliash (FM) and neighbor-joining To reduce the size of the dataset for phylo- (NJ) trees from the distance matrix presented by genetic analyses, we combined similar sequenc- Gorman and Kim (1976), using PHYLIP 3.5 (Fel- es from the same locality (differing at 2% of senstein, 1995), and we also analyzed the data sites or less) into single OTUs, scoring variable in a parsimony framework using the MANOB sites as polymorphic in the combined dataset. optimization criterion (Swofford and Berlocher, With unordered characters and 100 replicates of 1987; Berlocher and Swofford, 1997). For the random taxon addition, a heuristic search using MANOB analysis, we used step matrices rep- parsimony criteria resulted in a single tree of resenting the locus-specific Manhattan distances 1052 steps (Fig. 2A). The tree is rooted with An- C. J. SCHNEIDER ET AL.

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Unordered Parsimony Weiqhted Change Maximum Likelihood Parsimony loor A. m, inomatus A, m. maotiQratus^ MÍI»L A, m. chrysops A. m. inomatus J *^l• A. m. marmoratus' A. m. chrysops I• A. m. desiradei A. m. desiradei M Guadeloupean- A. m. girafus Dominican A. m. girafus su A.sabanus Ciade A. sabanus A. m. alliaceus North A. m. alliaceus I• A. m, alliaceus South A, m. ferreus - A, lividus A. lividus A. m. ferreus A. m. alliaceus S - A. oculaius A. oculatus - A. m. terraeattae C A. m. terraealtae- • A. leachi A, gingivinus • A. gingivinus BG" Clade A. bimaculalus • A. bimaculatijs ]• A. leachi A. schwartzi 351 A. Schwartz i "wattsi' group of iopi•;A. vuattsi small anoles 59 A. wattsi A. pogus A.pogus A. acutus A. acutus • A. cristate! I us A. cristatelius

Combined mtDNA Body Size and Atlozyme Data A. m, marmoratus* oculatus oculatus A. m, inomatus ferreus ie:tcni NJ A. m. chrysops lividus i•A. m. desiradei maimotatus sabânus ggA. m. girafus RUÛJkuS bímacutaius-i Jl-A. sab a nus bjmaculalus ' LA. m. alliaceus N gingtvinua •A. m. alliaceus S sctvMaiW ^ pogua •A. tivtdus A. m, ferreus •A. m. terraealtae L^ OCUlBtliS A. oculatus oculatus -A, leachi fvlANOB t&achi ferrauE A. n ubi lus Ifvkjus -A, gingivinus ^ marrnDratus b4 -sstjanus -A. bimaculatus L nubilus j blmaculalus -A, schwartzi s J 1 • bimaculatus -A. wattsi S - gingnfinus -A. pogus S - wattsi kíB, • schwartzi -A. acutus I -pogus A. cristatelius

FIG. 2. (A) Minimum length tree with all characters unordered (1052 steps; CI = 0.506). Bootstrap values from 1000 bootstrap replicates are shown above the nodes (values of less than 50% are not shown). Values below nodes are decay indices. Shaded boxes identify important discussed in the text. (B) Weighted- change parsimony and maximum-likelihood trees generated from mtDNA data. (C) Fitch-22 Margoliash (FM), neighbor-joining (NJ), and MANOB trees constructed from allozyme data presented by Gorman and Kim (1976). (D) Single most-parsimonious tree resulting from analysis of the combined mtDNA and allozyme data. Values above the branches are bootstrap values from 1000 bootstrap replicates. Values less than 50% are not shown. Body size for each species is shown in the right hand column: I = intermediate; L = Large; and S = small. * The OTU marmoratus here represents the phylogenetic position of sequences from three described subspecies {A. m. marmoratus, A. m. speciosus, and A. m. setosus), which together form an exclu- sive group within which sequences differ by less than 2%. 6 C. J. SCHNEroER ET AL.

TABLE 3. Phylogenetic signal in different partitions of the dataset as shown by g,-statistics of tree length distribution for 10,000 random trees (or all possible trees if less than 10 taxa were included). Analyses are presented such that the first subset of taxa represents the deepest divergences in the tree, with subsequent analyses adding taxa that represent successively shallower levels of divergence. Synonymous transitions (C^->T changes in first positions of leucine codons and all third-position transitions) represent the fastest evolving character state changes and show significant phylogenetic signal only for the most recent divergences while slowly evolving classes of changes show significant phylogenetic signal for even the deepest relationships. ** = P < 0.01; * = 0.01 < P fi 0.05; ns = P > 0.05.

Transversions and Synonymous nonsynonymous All diaracters Informative Taxa included transitions transitions (unordered) characters A. m. marmoratus, A. oculatus, A. kachi, A. bimaculatus, A. pogus -0.049 ns -0.962* -0.299 ns 92 Above + A. gingivinus -0.217 ns -1.166** -0.545* 129 Above + A. m. terrealtae -0.384 ns -0.782** -0.541*» 150 Above + A. schivartzi -0.208 ns -1.046** -0.794** 169 Above + A. wattsi -0.446»» -0.899** -0.700** 178 Above + A. (m.) ferreus -0.348** -1.069** -0.730** 186 Above + any other of the Guadeloupean clade ** ** ** s205

olis cristatellus as the sole outgroup and is pre- acters (sites) at different positions within codons sented with a basal trichotomy because the re- of mitochondrial protein-coding genes change lationship of A. acutus to the bimaculatus and at radically different rates; synonymous substi- cristatellus species groups is uncertain (see Gor- tutions occur at a much higher rate than non- nnan and Atkins, 1969; Lazell, 1972; Williams, synonymous substitutions, and there is a strong 1976; Roughgarden et al., 1987). transition bias (Irwin et al., 1991; Martin and The minimum length tree contains a well- Palumbi, 1993). As a heuristic, we used the supported monophyletic group of sequences skewness of tree-length distribution (Hillis, from the ivattsi group of small-bodied anoles (A. 1991; Hillis and Huelsenbeck, 1992) to examine schwartzi, A. wattsi, and A. pogus), but sequences phylogenetic signal in synonymous and nonsy- from the large-bodied anoles that occur on two- nonymous substitutions at various nodes in the species islands (A. bimaculatus and A. kachi) are tree representing different levels of divergence not sister taxa. In the minimum length tree, A. (Table 3). Synonymous transitions (including gingivinus (an intermediate-sized anole) and A. both third-position transitions and first-position bimaculatus are sister spedes (henceforth the BG C <-^ T changes in leucine codons) represent the clade), and A. kachi is the sister group to the most frequent type of character state change in Guadeloupean-Dominican clade (which con- the dataset, and the phylogenetic signal in those tains sequences from A. marmoratus ssp, A. liz>- characters is mainly among terminal taxa at the idus, A. sabanus, and A. oculatus). However, the tips of the tree. In contrast, nonsynonymous position of A. kachi relative to the BG clade is transitions and all transversions contain phylo- unresolved in the 50% majority rule consensus genetic signal for even the deepest relationships. of the bootstrapped data (see Fig. 2A). Sequenc- To see whether accounting for these differ- es from the Guadeloupean Archipelago are not ences in phylogenetic signal at different depths monophyletic and the clade stemming from in the tree would help resolve the deep relation- their most recent common ancestor also con- ships within the bimaculatus group, we searched tains sequences from A. lividus (from Montser- for the most-parsimonious tree using step-ma- rat) and A. sabanus (from the island of Saba, ap- trices that reduced by a factor of two the cost proximately 200 km northwest of Guadeloupe), (in number of steps) of transitions at third po- and also possibly A. oculatus from Dominica, al- sitions and C <-> T transitions in first positions though this latter relationship is not strongly (nearly all of which were synonymous changes supported (Fig. 2A). in leucine codons). Second position changes of Use of unordered character states is perhaps all kinds, third-position transversions, and non- the simplest assumption, but for nucleotide se- C <-^ T changes at first positions carried twice quence data, it may not always be most appro- the cost of third-position transitions and first- priate. Methods of phylogenetic reconstruction position C <-> T changes. A heuristic search with using parsimony perform best when the rate of random taxon addition (100 replicates) resulted character state change is low (Felsenstein, 1978, in two equally parsimonious trees of 1398 steps, 1981; Huelsenbeck and Hillis, 1993), but char- the strict consensus of which is shown in Figure ANOLIS PHYLOGENY

TABLE 4. Results (P-values) from Templeton (1983) one-tailed signed-ranks tests of alternative topologies. P-values indicate the probability that alternative trees are not significantly worse explanations of the data than the most-parsimonious tree. Three separate tests were conducted for each comparison: (1) using the mtDNA dataset with character-state changes unordered and of equal weight and comparing alternative trees against the tree shown in Fig. 2A; (2) using the mtDNA dataset with character states partially ordered and weighted ("weighted-change" as described in the text) and comparing alternative trees against the weighted-change parsimony tree shown in Fig. 2B; and (3) using the allozyme dataset and the MANOB assumptions and com- paring the alternative trees against the MANOB tree in Fig. 2C. The tests using the allozyme dataset included only those taxa for which allozyme data were complete (see Fig. 2C). Alternative topologies were produced by constraining the relationships of interest and searching for the most-parsimonious tree containing those rela- tionships (heuristic search with 100 replicates of random taxon addition when employing the mtDNA dataset with all taxa, or branch and bound searches using the allozyme dataset with 15 taxa).

Dataset and assumptions mtDNA mtDNA weighted Allozymes Test trees unordered diange MANOB mtDNA unordered >0.80 >0.60 mtDNA weighted-change or ML >0.50 >0.80 >0.50 Allozyme MANOB and distance trees (Fig. 2C) <0.01 <0.01 >0.80 Most-parsimonious tree with A. kachi nested within the Guadelou- pean-Dominican clade (not as the sister group to the GD clade) 0.01 <0.05 • Most-parsimonious tree with A. kachi as the sister group to the Guadeloupean-Dominican clade • >0.40 >0.50 Most-parsimonious tree with A. kachi and A. bimaculatus as sister taxa <0.01 <0.01 <0.01 Most-parsimonious tree with (leachi,(bimaculatus,gingivinus)) >0.20 >0.10 >0.30

2B. As in the most-parsimonious tree with un- man and Kim's genetic distance matrix are sim- ordered characters, the large anoles {A. bimacu- ilar to the mtDNA phylogeny in that they con- latus and A. leachi) are not sister taxa, and the tain a group of small, terrestrial anoles (the watt- small wattsi group anoles (A. schimrtzi, A. irnttsi, si group), show A. gingivinus as the sister taxon and A. pogus) form a well-supported clade that to A. bimaculatus, and show a close relationship is the sister group to all other taxa. These trees between Guadeloupean anoles {A. marmoratus) differ from the most-parsimonious trees in the and A. lividus. The MANOB tree is similar in placement of A. leachi but otherwise are similar most respects except that it shows the wattsi Further reducing the cost of fast evolving char- group as paraphyletic. The allozyme trees all acter state changes does not significantly alter contain the following nested groups: {{(ferreus, the relationships shown in Figure 2B. oculatus, leachi), {lividus, marmoratus)), sabanus). Maximum-likelihood (ML) analysis of the se- Although the monophyly of the largest of these quence data under a general time-reversible groups is consistent with the trees produced model with gamma-distributed rate variation from the mtDNA data, the mitochondrial and among sites resulted in a tree that is similar in allozyme trees disagree substantially on rela- most respects to the weighted-change parsi- tionships within this putative clade. The precise mony consensus tree (Fig. 2B). We tested the topology suggested by the allozyme trees is in- three alternative topologies (Fig. 2A, B) in a par- congruent with the mtDNA sequence data simony framework using Templeton's (1983) (signed-ranks test; P < 0.01; Table 4). However, two-tailed signed-ranks test with character trees with A. leachi as the sister to the Guade- changes unordered and of equal weight, or par- loupean-Dominican taxa do not differ signifi- tially ordered and weighted as in the weighted- cantly from the most-parsimonious mtDNA change parsimony analysis. None of the trees trees (P > 0.10; Table 4). The allozyme data are differs significantly from any other (P a 0.50 in consistent with the trees suggested by the all cases; Table 4). mtDNA data in that none of the mtDNA trees Distance and parsimony analyses of Gorman is significantly worse than the MANOB tree in and Kim's allozyme data (Gorman and Kim, signed-ranks tests using the allozyme data (Ta- 1976) resulted in trees (Fig. 2C) that were sim- ble 4). Interestingly, the inconsistency between ilar to each other and to the mtDNA trees (Fig. the allozyme and mtDNA trees may be the re- 2A, B). Neighbor-joining (NJ) and Fitch-Margo- sult of different rooting of the (Guadeloupean- liash (FM) trees (Fig. 2C) produced from Gor- Dominican, A. leachi) group. If, in the allozyme C. J. SCHNEIDER ET AL. trees, the (Guadeloupean-Dominican, A. leachi) relationships among the Guadeloupean and Do- group was rooted on the branch leading to A. minican anoles. leachi, the allozyme trees would be nearly iden- tical to the unordered mtDNA topology (Fig. Previous Phylogenetic Hypotheses 2A). Phylogenetic relationships among taxa within Combining the allozyme and mtDNA data (as the bimaculatus group have been considered pre- described in the Materials and Methods section) viously in three studies. Based on external anat- resulted in a single tree (Fig. 2D), which is sim- omy, Lazell (1972:100) presented a hypothetical ilar in most respects to the mtDNA trees. The diagrammatic scheme of the evolution of this 50% majority rule bootstrap consensus tree of group. Gorman and Kim (1976) presented a the combined data is nearly identical to the UPGMA phenogram of Nei's (1972) genetic dis- mtDNA bootstrap consensus tree (compare Fig. tance estimated from protein electrophoretic 2A, D). The allozyme data do not significantly variation. Finally, Roughgarden et al. (1987) sug- improve the resolution of relationships above gested a phylogeny based on a variety of dis- that of the mtDNA data alone except that there parate data, drawn primarily from the previous is additional bootstrap support for the sister re- two studies. lationship of A. bimaculatus and A. gingivinus. Lazell (1972) did not present his scenario in The combined data favor placing A. leachi as the the form of a phylogenetic tree but provided sister group to the Guadeloupean-Dominican sufficient detail that phylogenetic relationships clade (which is also consistent with the presence can be determined. Importantly, Lazell identi- of a clade containing A. leachi, A. oculatus, A. fied a closely related group of small anoles, the marmoratus, A. liuidus, and ^4. sabanus in the sep- wattsi group, which he considered a single spe- arate allozyme and tmordered mtDNA trees), cies with four subspecies, and he recognized the but the precise placement of A. leachi is not close relationship among A. marmoratus, A. livi- strongly supported in any analysis. We regard dus, and A. oculatus. We also note that he con- the tree shown in Figure 2D as the best estimate sidered A. leachi and A. bimaculatus to be con- of phylogeny from the available data. specific and A. nubilus to be closely related to A. bimaculatus. DISCUSSION The phylogenetic hypothesis proposed by Our phylogenetic analysis reveals two sur- Roughgarden et al. (1987) was not based on any prises. First, A. sabanus, from the island of Saba, formal analysis; hence, we will not consider it is nested within A. marmoratus from Guade- explicitly, but, because it was based in large part loupe. In terms of gross morphology, A. sabanus on Gorman and Kim's (1976) study, most of our is very similar to A. marmoratus (Losos and de comments below pertain to it as well. We do Queiroz, 1997; but see Lazell, 1972, who sees note, however, that Roughgarden considered the affinities between A. sabanus and the ivattsi zmttsi group of small anoles as monophyletic, group), although its spotted pattern does not considered A. marmoratus, A. liuidus, and A. ocu- closely resemble that of any of the diverse pop- latus as a monophyletic group, and left the re- ulations of A. marmoratus. These results suggest lationships of A. bimaculatus, A. leachi, A. gingi- a recent colonization event followed by rapid vinus unresolved. Neither Roughgarden (1987) evolutionary change in body coloration, or al- nor Lazell (1972) suggested a close relationship ternatively, long-distance dispersal from Gua- between A. sabanus and A. marmoratus. deloupe to Saba and hybridization with a pre- Gorman and Kim (1976) presented a UPGMA existing population resulting in mtDNA intro- tree based on Nei's genetic distance (Nei, 1972). gression. By contrast, the close relationship of Their UPGMA tree differs substantially from A. lividus and A. marmoratus has long been sus- our FM and NJ trees which were constructed pected (e.g., Lazell, 1972) and was corroborated using the same distance matrix. The discrep- by Gorman and Kim (1976). In addition, our re- ancy likely results from the restrictive assump- sults suggest that populations on the islands of tion of equal rates of evolution among taxa im- Les Saintes, situated between Dominica and posed by UPGMA (reviewed by de Queiroz and Guadeloupe (Fig. 1), may be more closely relat- Good, 1997). Interestingly, trees constructed ed to A. oculatus from Dominica than they are from the allozyme data (NJ, FM, and MANOB to A. marmoratus, even though previous studies trees) are inconsistent with the mtDNA data (Lazell, 1964, 1972) have treated the Les Saintes (Table 4), but the converse is not true•trees populations as a subspecies of A. marmoratus. constiucted from the mtDNA dataset are not in- from Dominica is characterized consistent with the allozyme data (Table 4). This by a unique karyotype (Gorman and Atkins, result may stem from the allozyme dataset lack- 1969), and examination of the karyotype from ing the power to reject alternative topologies Les Saintes, in addition to further mtDNA sam- (i.e., the pattern of informative character covari- pling within A. oculatus, may help resolve the ation in the allozyme dataset may be so weak ANOLIS PHYLOGENY as to allow many alternative topologies), where- between A. bimaculatus and A. leachi (P < 0.01 as the strong patterns of character covariation in for both datasets; Table 4). the mtDNA dataset allow the rejection of many Because A. bimaculatus and ^4. leachi are not alternative topologies. Additional data from nu- sister taxa, evolutionary changes in size must clear markers are needed to examine the con- have occurred more frequently than Losos cordance between evolutionary histories of nu- (1990) concluded. Depending on how the rela- clear and mitochondrial genomes. tionship of A. leachi is finally resolved, large In summary the available mtDNA and allo- body size may have evolved separately (twice) zyme data suggest that the Guadeloupean-Do- in A. leachi and A. bimaculatus or once in their minican clade of taxa (including A. lividus and common ancestor We note that large body size A. sabanus) form a monophyletic group exclusive may have evolved as many as three times in the of the other bimaculatus group taxa. The position bimaculatus group as a whole, if we consider the of A. nubilus, for which DNA sequences are not solitary large anole ^4. m. ferreus (see Lazell, available, differs in the allozyme trees (Fig. 2C) 1972; Roughgarden and Fuentes, 1977), and that and remains uncertain pending additional data. the more frequently body size is inferred to The position of A. leachi is unresolved but its have changed, the less reliable are our recon- placement as the sister group to the Guadelou- structions of ancestral states likely to be (e.g., pean-Dominican group (as in Fig. 2D) is consis- Schlüter et al, 1997; Cunningham et al, 1998). tent with both mtDNA and allozyme data. More If A. leachi is the sister group to the BG clade, important, the large anoles A. bimaculatus and then large body size may have evolved only A. leachi are not sister taxa, whereas the small once in the common ancestor of A. bimaculatus anoles A. wattsi, A. schwartzi, and A. pogus form and A. leachi, with a reversion to intermediate a well-supported monophyletic group. size in A. gingivinus. The most-parsimonious tree with A. leachi, A. bimaculatus, and A. gingi- Body Size Evolution vinus as a monophyletic group is not incompat- The distribution of body sizes among species ible with the available data (Table 4). If, in fact, in the Lesser Antilles is decidedly nonrandom large size only evolved once in the common an- (Schoener, 1970; Losos, 1990): species occurring cestor of A. bimaculatus and A. leachi, then a hy- alone on an island tend to be intermediate in pothesis of character displacement, with the size, whereas on two-species islands, a large wattsi complex evolving small size concurrently, and a small species are usually found (Fig. 1). would still be tenable, although the reversion of The two exceptions to this are the solitary large A. gingivinus to intermediate size while in sym- anole (A. marmoratus ferreus) from Marie Gal- patry with loattsi complex species would require ante, and the coexistence of a small (A. pogus) explanation. However, if large size evolved in- and an intermediate-sized anole (A. gingivinus) dependently in A. bimaculatus and A. leachi, then on St. Martin (Fig. 1). Schoener (1970) and Wil- a character displacement hypothesis becomes liams (1972; see also Lazell, 1972:99) suggested less tenable. The reason is that a character dis- that the pattern of body-size distribution could placement hypothesis implies simultaneous result from character displacement, in which change in size in two species•one getting larg- two similar and presumably intermediate-sized er and the other getting smaller•and thus im- species came into sympatry and then diverged plies that the number of increases in size should in body size to minimize competition. Losos be the same as the number of decreases. Of (1990) tested this hypothesis in a phylogenetic course, ad hoc scenarios could always be de- context and concluded that large and small size vised to account for this discrepancy. had each evolved once in the bimaculatus-leachi As an alternative evolutionary explanation for and zmttsi clades, respectively, and that this pat- size distributions in the northern Lesser Antil- tern was consistent with a character displace- les, Roughgarden and Pacala (1989) suggested ment explanation (for further discussion of the a taxon cycle hypothesis, which was later mod- statistical analysis underlying these conclusions, ified to a taxon loop hypothesis (Roughgarden, see Miles and Dunham, 1996; Butler and Losos, 1992, 1995). This hypothesis assumes that inter- 1997). However, this analysis was conducted us- mediate size is optimal for anoles on the Lesser ing Üie phylogeny of Roughgarden et al. (1987) Antilles and that larger species are behaviorally with the trichotomy involving A. bimaculatus, A. dominant over smaller ones. Hence, if an island leachi, and A. gingivinus resolved in favor of an with an intermediate-sized species is invaded A. bimaculatus-A. leachi sister taxon relationship by a larger species, the larger species will begin following Lazell's (1972). However, to evolve toward intermediate size while the ini- the existing molecular data do not support a sis- tially intermediate-sized species evolves to ter relationship of A. bimaculatus and A. leachi: smaller size to lessen competitive effects (for a both the allozyme and mtDNA data unambig- discussion of the data relevant to this and the uously reject any tree with a sister relationship character displacement hypothesis, see Rough- 10 C. J. SCHNEIDER ET AL.

garden and Pacala, 1989; Roughgarden, 1992, of Agriculture, Fisheries, Lands and Housing, 1995; Losos, 1992). The taxon q^cle/loop hy- Antigua; G. A. L. Gray, F A. L. Margetson, and pothesis seems to require some additional as- the Ministry of Agriculture, Trade, and the En- sumptions. For one, it requires dispersal of vironment, Montserrat for additional permits, large-sized lizards from a source where inter- and to G. Zug for specimens of A. gingivinus and mediate size is not optimal. For another, it A. Malhotra and R. Thorpe for tissue samples equates behavioral dominance with competitive from A. oculatus. Support was provided by the dominance but then assumes that evolution of Kellogg fund of the Museum of Vertebrate Zo- small size by the smaller species is advanta- ology, Sigma Xi, and the National Science Foun- geous because it lessens competition despite the dation (DEB 9112602 and DEB 9318642). Early fact that it increases the disadvantage of the spe- drafts of this manuscript benefited from com- cies in terms of behavioral dominance. Evident- ments by D. B. Wake, H. W Greene, and J. L. ly the assumption is that the disadvantage in Patton. behavioral dominance is less important in terms of natural selection than the advantage in terms LITERATURE CITED of reduced competition. BERLOCHER, S. H., AND D. L. SWOFFORD. 1997. Seardi- In the particular scenario proposed by ing for phylogenetic trees under the frequency par- Roughgarden and Pacala (1989), Guadeloupe or simony criterion: an approximation using gener- Dominica is the source for large-bodied colo- alized parsimony. Syst. Biol. 46:211-215. nists that would initiate a taxon cycle/loop. If BREMER, K. 1988. The limits of the amino acid se- that were true, A. bimaculatus and A. leachi se- quence data in Angiosperm phylogenetic recon- quences would be embedded within the Guad- struction. Evolution 42:795-803. eloupean-Dominican clade of sequences, and BUTLER, M. A., AND J. B. Losos. 1997. Testing for un- this is not the case. However, if large body size equal amounts of evolution in a continuous char- acter on different branches of a phylogenetic tree in A. leachi and A. bimaculatus only evolved once, using linear and squared-change parsimony; an then the common ancestor of the BG clade example using lesser antillean Anolis lizards. Evo- would have been large and reversion to inter- lution 51:1623-1635. mediate size in A. gingivinus could be consistent CUNNINGHAM, C. W., K. E. OMLAND, AND T. H. OAK- with a modified taxon loop/cycle hypothesis, LEY. 1998. Reconstructing ancestral character although the lack of an allopatric large ancestral states: a critical reappraisal. Trends Ecol. Evol. 13: population would still be problematic. 361-366. DE QuEiROZ, K., AND D. A. GooD. 1997. Phenetic clus- Conclusions tering in biology: a critique. Q. Rev. Biol. 72:3-30. DoNOGHUE, M. ]., R. G. OLMSTEAD, J. E SMITH, AND J. Resolving the relationships of A. leachi is nec- D. PALMER. 1992. Phylogenetic relationships of essary to further understand patterns of body- Dipsicales based on rbcL sequences. Ann. Mo. Bot. size evolution in the anoles of the bimaculatus Gard. 79:249-265. species group. In addition, our unexpected find- ETHERIDGE, R. E. 1960. The relationships of the anoles ings on the position of A. sabanus and the rela- (Reptilia: Sauria: Iguanidae): an interpretation tionships between Guadeloupean and Domini- based on skeletal morphology. Unpubl. Ph.D. diss., can populations deserves further study. The Univ. of Michigan, Ann Arbor. phylogeny presented above resolves some im- FELSENSTEIN, ]. 1978. Cases in which parsimony and compatibility methods will be positively mislead- portant issues in the evolution and biogeogra- ing. Syst. Zool. 27:27-33. phy of the bimaculatus group of anoles and pro- . 1981. Evolutionary trees from DNA sequenc- vides the framework for future phylogenetic es: a maximum likelihood approach. J. Mol. Evol. analyses of nuclear and mitochondrial genes 17:368-376. targeting poorly supported nodes in this tree. . 1985. Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39:783- Acknowledgments.•We thank C. Guyer and T. 791. Jackman for their insightful reviews of the man- . 1995. PHYLIP Vers. 3.5. Available from http; uscript. We thank T. Benoit, G. Simon, the Pre- / / evolution.genetics.washington.edu / phylip.html. fecture de la region Guadeloupe, Direction de GORMAN, G. C, AND L. ATKINS. 1969. The zoogeog- L'Administration Generale et de la Réglemen- raphy of lesser antillean Anolis lizards•an analy- tation, Bureau de L'Urbanisme et du Cadre de sis based upon chromosomes and lactic dehydro- Vie and the Ministère de L'Environment genase. Bull. Mus. Comp. Zool. 138:53-80. (France) for graciously granting permits to col- GORMAN, G. C, AND Y. J. KIM. 1976. Anolis lizards of the Eastern Caribbean: a case study in evolution. lect samples from the Guadeloupean archipela- II. Genetic relationships and genetic variation of go (permit nos. 88-1225 AD/1 /4 and 92-036, re- the bimaculatus group. Syst. Zool. 25:62-77. spectively). Thaiücs also to B. S. Nisbett and the GYLLENSTEN, V., AND H. ERLICH. 1988. Generation of Ministry of Agriculture, St. Kitts; the Permanent single-stranded DNA by the polymerase chain re- Secretary and Chief Veterinary Officer, Ministry action and its applications to direct sequencing of ANOLIS PHYLOGENY 11

the HLA DQa locus. Proc. Nat. Acad. Sei. USA 85: -•. 1997a. Microgeographic variation in scalation 7652-7656. of Anolis oculatus (Dominica, West Indies): a mul- HiLLls, D. M. 1991. Discriminating between phylo- tivariate analysis. Herpetologica 53:49-62. genetic signal and random noise in DNA sequenc- -. 1997b. Size and shape variation in a Lesser es. In M. M. Miyamoto and J. Cracraft (eds.), Phy- Antillean anole, Anolis oculatus (Sauria: Iguanidae) logenetic Analysis of DNA Sequences, pp. 278-294. in relation to habitat. Biol. J. Linn. Soc. 60:53-72. Oxford Univ. Press, New York. MANIATIS, T., E. E FRISCH, AND J. SAMBROOK. 1982. HiLLis, D. M., AND J. HuELSENBECK. 1992. Signal, Molecular Cloning: A Laboratory Manual. Cold noise, and reliability in molecular phylogenetic Spring Harbor, New York. analyses. J. Hered. 83:189-195. MARTIN, A. P., AND S. R. PALUMBI. 1993. Protein evo- HuELSENBECK, J., AND D. M. HiLLis. 1993. Success of lution in different cellular environments: cyto- phylogenetic methods in the four-taxon case. Syst. chrome b in sharks and mammals. Mol. Biol. Evol. Biol. 42:247-264. 10:873-891. IRWIN, D. M., T. D. KOCHER, AND A. C. WILSON. 1991. MEYER, A. 1994. Shortcomings of the cytochrome b Evolution of the cytochrome b gene of mammals. gene as a molecular marker Trends Ecol. Evol. 9: J. Mol. Evol. 32:128-144, 278-281. JACKMAN, T. R., J. B. LOSOS, A. LARSON, AND K. DE MILES, D. B., AND A. E. DUNHAM. 1996. The paradox QuEiROZ. 1997. Phylogenetic studies of conver- of the phylogeny: character displacement of anal- gent adaptive radiations in Caribbean Anolis liz- yses of body size in island Anolis. Evolution 50: ards. In T. Givnish and K. Systma (eds.), Molecular 594-603. Evolution and , pp. 535-557. MILLER, S. A., D. D. DYKES, AND H. E POLESKY. 1988. Cambridge Univ. Press, Cambridge. A simple salting procedure for extracting DNA JACKMAN, T. R., A. LARSON, K. DE QUEIROZ, AND J. B. from human nucleated cells. Nucí. Acids Res. 16: Losos. 1999. Phylogenetic relationships and the 215. tempo of early diversification in Anolis lizards. MOERMOND, T. C. 1986. A mechanistic approach to Syst. Biol. 48:254-285. the structure of communities: Anolis lizards KIMURA, M. 1980. A simple method for estimating and birds. Am. Zool. 26:23-37. evolutionary rate of base substitutions through NEI, M. 1972. Genetic distance between populations. comparative studies of nucleotide sequences. J. Am. Nat. 106:283-292. Mol. Evol. 16:111-120. PACALA, S., AND J. ROUGHGARDEN. 1982. Resource KOCHER, T. D., W. K, THOMAS, A. MEYER, S. V. ED- partitioning and interspecific competition in two WARDS, S. PÂÂBO, F. X. VILLABLANCA, AND A. C. two-species insular Anolis communities. Sci- WILSON. 1989. Dynamics of mitochondrial DNA ence 217:444-446. evolution in : amplification and sequencing ROE, B. A., D.-R MA, R. K. WILSON, AND J. E-H. with conserved primers. Proc. Nati. Acad. Sei. USA WONG. 1985. The complete nucleotide sequence of 86:6196-6200. the Xenopus laevis mitochondrial DNA genome. J. LAZELL, J. D. 1964. The anoles (Sauria: Iguanidae) of Biol. Chem. 260:9759-9774. the Guadeloupéen archipelago. Bull. Mus. Comp. ROUGHGARDEN, J. 1992. Comments on the paper by Zool. 131:359-401. Losos: character displacement versus taxon loop. . 1972. The anoles (Sauria: Iguanidae) of the Copeia 1992:288-295. Lesser Antilles. Bull. Mus. Comp. Zool. 143:1-115. . 1995. Anolis Lizards of the Caribbean. Ecol- LOSOS, J. B. 1990. A phylogenetic analysis of character ogy, Evolution, and Plate Tectonics. Oxford Univ. displacement in Caribbean Anolis lizards. Evolu- Press, New York. tion 44:558-569. ROUGHGARDEN, J. D., AND E. R. FUENTES. 1977. The . 1992. A critical comparison of the taxon-cycle environmental determinants of size in solitary and character-displacement models for size evolu- populations of West Indian Anolis lizards. Oikos tion of Anolis lizards in the Lesser Antilles. Copeia 29:44-51. 1992:279-288. ROUGHGARDEN, J. D., AND S. W. PACALA. 1989. Taxon . 1994. Integrative approaches to evolutionary ecology•Anolis lizards as model systems. Annu. cycle among Anolis lizard populations: review of Rev. Ecol. Syst. 25:467-493. evidence. In D. Otte and J. A. Endler (eds.), Spe- LOSOS, J. B., AND K. DE QUEIROZ. 1997. Evolutionary ciation and Its Consequences, pp. 403^32. Sinauer consequences of ecological release in Caribbean Associates Inc., Sunderland, Massachusetts. Anolis lizards. Biol. J. Linn. Soc. 61:459^83. ROUGHGARDEN, J., W. PORTER, AND D. HECKEL. 1981. MALHOTRA, A., AND R. S. THORPE. 1991a. Experimen- Resource partitioning of space and its relationship tal detection of rapid evolutionary response in nat- to body temperature in Anolis lizard populations. ural lizard populations. Nature 353:347-348. Oecologia 50:256-264. . 1991b. Microgeographic variation in Anolis ROUGHGARDEN, J. D., D. G. HECKEL, AND E. R. FUEN- oculatus, on the island of Dominica, West Indies. J. TES. 1983. Coevolutionary theory and the island Evol. Biol. 4:321-335. biogeography of Anolis. In R. B. Huey et al. (eds.). . 1993. An experimental field study of a eu- Lizard Ecology: Studies on a Model Organism, pp. rytopic anole, Andis oculatus. J. Zool. (Lond.) 229: 371^10. Harvard Univ. Press, Cambridge, Massa- 163-170. chusetts. 1994. Parallels between island lizards sug- ROUGHGARDEN, J. D., S. W. PACALA, AND J. D. RUM- gests selection on mitochondrial DNA and mor- MEL. 1984. Strong present-day competition be- phology. Proc. R. Soc. Lond. B Biol. Sei. 257:37-42. tween the Anolis lizard populations of St. Maarten 12 C. J. SCHNEIDER ET AL.

(Neth. Antilles). In B. Shorrocks (ed.). Evolutionary . 1995. Territory acquisition in lizards. 3. Com- Ecology, pp. 203-220. Blackwell, London. peting for space. Anim. Behav. 49:679-693. ROUGHGARDEN, J. D., S. D. GAINES, AND S. W. PACALA. 1997. Functions of fights in territory estab- 1987. Supply side ecology; the role of physical lishment. Am. Nat. 150:393-405. transport processes. In P. Giller and J. Gee (eds.). . 1998. Territory acquisition in lizards. IV. Ob- Organization of Communities: Past and Present, taining high status and exclusive home ranges. pp. 459-486. Blackwell Scientific, London. Anim. Behav 55:461^72. RuMMEL, J., AND J. RouGHGARDEN. 1985. A theory of SwoFFORD, D, L. 1998. PAUP* Phylogenetic analysis faunal buildup for competition communities. Evo- using parsimony and other criteria. Beta test ver- lution 39:1009-1033. sion 4.0d64. Current version available from Sinauer SCHALL, J. J. 1992. Parasite-mediated competition in Associates, Inc., Sunderland, Massachusetts. Anûlis lizards. Oecologia 92:58-64. SwoFFORD, D. L., AND S. H. BERLOCHER. 1987. Infer- SCHLüTER, D., T. PRICE, A. O. MOOERS, AND D. LUD- ring evolutionary trees from gene-frequency data WIG. 1997. Likelihood of ancestor states in adap- under the principle of maximum parsimony. Syst. tive radiation. Evolution 51:1699-1711. Zool. 36:293-325. SCHNEIDER, C. J. 1993. Diversification in lizards of the TEMPLETON, A. R. 1983. Phylogenetic inference from genus Anolis from Guadeloupe and the northern restriction endonuclease cleavage site maps with Lesser Antilles. Unpubl., Ph.D. diss., Univ. of Cal- particular reference to the evolution of humans ifornia, Berkeley. and the apes. Evolution 37:221-244. . 1996. Distinguishing between primary and UNDERWOOD, G. 1959. The anoles of the eastern Ca- secondary intergradation among morphologically ribbean. Part III. Revisionary notes. Bull. Mus. differentiated populations of Anolis marmoraius. Comp. Zool. 121:191-226. Mol. Ecol. 5:239-249. WILLIAMS, E. E. 1972. The origin of faunas: evolution SCHOENER, T. W. 1970. Size patterns of West Indian of lizard congeners in a complex island fauna•a Anolis lizards. II. Correlations with the sizes of par- trial analysis. Evol. Biol. 6:47-89. ticular sympatric species•displacement and con- . 1976. West Indian anoles: a taxonomic and vergence. Am. Nat. 104:155-174. evolutionary summary, 1. Introduction and a spe- STAATS, C. M., T. BARTOLOTTA, AND J. J. SCHALL. 1997. cies list. Breviora 440:1-21. Body size and perching behavior of , . 1983. Ecomorphs, faunas, island size, and di- the solitary anole of Saba, Netherland Antilles. verse endpoints in island radiations of Anolis. In R. Herpetol. Nat. Hist. 5:157-164. Huey et al. (eds.). Lizard Ecology, Studies of a STAMPS, J. A. 1991. The effect of conspecifics on hab- Model Organism, pp. 326-370. Harvard Univ. itat selection in territorial species. Behav. Ecol. So- Press, Cambridge, Massachusetts. ciobiol. 28:29-36. YANG, S., M. SOULE, AND G. GORMAN. 1974. Anolis STAMPS, J. A., AND V. V. KRISHNAN. 1994a. Territory lizards of the eastern Caribbean: a case study in acquisition in lizards. 1. First encounters. Anim. evolution. I. Genetic relationships, phytogeny, and Behav 47:1375-1385. colonization sequence of the roquet group. Syst. . 1994b. Territory acquisition in lizards. 2. Es- Zool. 23:387-399. tablishing social and spatial relationships. Anim. Behav 47:1387-1400. Accepted: 8 March 2000.