The diets of Hispaniolan colubrid snakes

Summary Approximately 1590 Hispaniolan colubrid snakes representing six genera and eight species were examined for prey remains (Alsophis cantherigerus, Antillophis parvifrons, Darlingtonia haetiana, Hypsirhynchus ferox, Ialtris dorsalis, Uromacer catesbyi, U. frenatus, and U. oxyrhynchus). The snakes were collected at many localities over a span of 80 years.Of 426 prey items, 77.9% were lizards (of which 69.6% were anoles), 19% frogs, 2.6% birds and mammals, and 0.5% other snakes. Darlingtonia was the only snake that did not exploit lizards; it fed exclusively on Eleutherodactylus frogs, including egg clutches. Disregarding Darlingtonia, there is no size class of Hispaniolan colubrids between 20–90 cm SVL that does not prey primarily on Anolis. Certain prey genera are added to, or deleted from, diets depending on snake size, but the data suggest that snake SVL alone does little to dictate what prey genera (or groups) are eaten. Shannon-Wiener values (H') indicate that Darlingtonia has the narrowest trophic niche, while Alsophis and Ialtris have the widest. Values of H' are not correlated with snake SVL, but highly significant (P<0.001) correlations exist between H' and mid-body circumference, head width, and snout width, and these characters may be indicators of trophic generalists and specialists. Anolis lizards are the most ubiquitous and conspicuous vertebrates on Hispaniola, and it is not surprising that they are widely exploited as a food source. Although as some snake species grow larger, anoles play a decreasingly important role in their diets, there is no evidence to suggest that they are ever abandoned as a food source by any Hispaniolan colubrid of any size.Secretive lizards of low vagility are eaten almost exclusively by wide ranging foragers (Alsophis, Antillophis); very active prey (Ameiva) is taken by sit-and-wait strategists (Hysirhynchus, U. frenatus). Those snakes which exploit the most prey groups are active foragers. Uromacer catesbyi exhibits both foraging modes, and predictably, eats diurnally active (anoles) and diurnally quiescent (hylid frogs) prey with almost equal frequency.Within Maglio's cantherigerus species assemblage, in which an Alsophis cantherigerus-like snake was ancestral to the other species, and in which longsnouted Uromacer are the most morphologically derived, there is an obvious trend toward trophic specialization on Hispaniola. The West Indies have provided an ideal natural laboratory for the investigation of many aspects of vertebrate ecology, and an arena in which to test theories of island biogeography. The most extensively studied West Indian vertebrates have been the lizards of the iguanid genus Anolis. Conversely, the ecology of West Indian snakes has been largely ignored. This is surprising in light of the fact that much has been written about Anolis predation, but little has been written about predators of Anolis; snakes may be important, frequent consumers of anoles.Hispaniola is physiographically and ecologically the most diverse of the Greater Antilles and, concomitantly, it has the most diverse snake fauna, including six colubrid genera containing 11 described species. It has rich frog and lizard faunas, but only two endemic mammals. Study of the diets of Hispaniola's colubrid snakes was undertaken to gain initial insights into the ecology of the snakes and to determine 1) what the snakes eat; 2) what relationships exist between snake diet and snake size as well as head and body proportions; 3) what relationships exist between snake foraging mode and prey type and size; 4) if anoles, as the most ubiquitous and conspicuous vertebrates on Hispaniola, comprise an important source of food; 5) if significant geographical differences in diet exist, expecially on satellite islands; 6) if north island and south island (sensu Williams 1961) Anolis ecomorphs are preyed upon by the same snake species in similar proportions; 7) if snakes are selective or opportunistic predators.This paper, the first in a series that will address all of the above topics, will briefly describe methods, snake species and prey genera. Prey genera are analyzed in terms of what snake taxa prey upon them, what size classes of snakes prey upon them, and prey genera diversity versus snake size and proportions.     

Control of arthropod abundance by Anolis lizards on St. Eustatius (Neth. Antilles)

The two Anolis lizard species of St. Eustatius (Neth. Antilles) have large effects on the abundance of arthropods. Over a six-month period, we excluded Anolis lizards from three experimental areas and maintained three other areas with natural densities of lizards. Exclusion of anoles resulted in a two to three-fold increase in the abundance of arthropods on the forest floor (mainly Dipterans), and a twenty to thirty-fold increase in the abundance of three large web-building spiders. These abundant web-building spiders, in turn, caused approximately a 25% decrease in the abundance of insects between the forest floor and canopy. Exclusion of anoles had no observed effect on the degree of herbivory as assayed by the amount of leaf damage on two plant species.     

Tree-based delimitation of morphologically ambiguous taxa: a study of the lizard malaria parasites on the Caribbean island of Hispaniola

Malaria parasites in the genus Plasmodium have been classified primarily on the basis of differences in morphology. These single-celled organisms often lack distinguishing morphological features, and this can encumber both species delimitation and identification. Six saurian malaria parasites have been described from the Caribbean island of Hispaniola. All six infect lizards in the genus Anolis, but only two of these parasites can be distinguished using morphology. The remaining four species overlap in morphology and geography, and cannot be consistently identified using traditional methods. We compared a morphological approach with a molecular phylogenetic approach for assessing the taxonomy of these parasites. We surveyed for blood parasites from 677 Anolis lizards, representing 26 Anolis spp. from a total of 52 sites across Hispaniola. Fifty-five of these lizards were infected with Plasmodium spp., representing several new host records, but only 24 of these infections could be matched to previously described species using traditional morphological criteria. We then estimated the phylogeny of these parasites using both mitochondrial (cytb and coxI) and nuclear (EF2) genes, and included carefully selected GenBank sequences to confirm identities for certain species. Our molecular results unambiguously corroborated our morphology-based species identifications for only the two species previously judged to be morphologically distinctive. The remaining infections fell into two well-supported and reciprocally monophyletic clades, which contained the morphological variation previously reported for all four of the morphologically ambiguous species. One of these clades was identified as Plasmodium floridense and the other as Plasmodium fairchildi hispaniolae. We elevate the latter to Plasmodium hispaniolae comb. nov. because it is polyphyletic with the mainland species Plasmodium fairchildifairchildi and we contribute additional morphological and molecular characters for future species delimitation. Our phylogenetic hypotheses indicate that two currently recognised taxa, Plasmodium minasense anolisi and Plasmodium tropiduri caribbense, are not valid on Hispaniola. These results illustrate that molecular data can improve taxonomic hypotheses in Plasmodium when reliable morphological characters are lacking.     

Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade*

Urbanization is intensifying worldwide, and while some species tolerate and even exploit urban environments, many others are excluded entirely from this new habitat. Understanding the factors that underlie tolerance of urbanization is thus of rapidly growing importance. Here, we examine urban tolerance across a diverse group of lizards: Caribbean members of the neotropical genus Anolis. Our analyses reveal that urban tolerance has strong phylogenetic signal, suggesting that closely related species tend to respond similarly to urban environments. We propose that this characteristic of urban tolerance in anoles may be used to forecast the possible responses of species to increasing urbanization. In addition, we identified several key ecological and morphological traits that tend to be associated with tolerance in Anolis. Specifically, species experiencing hot and dry conditions in their natural environment and those that maintain higher body temperatures tend to have greater tolerance of urban habitats. We also found that tolerance of urbanization is positively associated with toepad lamella number and negatively associated with ventral scale density and relative hindlimb length. The identification of factors that predispose a species to be more or less urban tolerant can provide a starting point for conservation and sustainable development in our increasingly urbanized world.     

EVOLUTIONARY PATTERNS OF THE THERMAL SENSITIVITY OF SPRINT SPEED IN ANOLIS LIZARDS

I present evidence that the thermal sensitivity of sprint speed of Anolis lizards has evolved to match the activity body temperatures (T_b) experienced by local populations in nature. Anolis lizards from a range of altitudes in Costa Rica have limited thermoregulatory abilities and consequently have field T_b that differ substantially in median and interquartile distance (a measure of variability). Experimentally determined maximal sprint temperatures (T_b at which lizards run fastest) were positively correlated with median field T_b, and performance breadths (ranges of T_b over which lizards run well) were correlated with the variability (interquartile distance) of field T_b in the species I examined. Such correlations would be expected if the thermal sensitivity of sprint speed and field T_b had evolved together to improve the sprint performance of lizards in nature. Integration of laboratory and field studies indicates that several species of Anolis regularly experience impaired sprint speeds in the field, despite apparent evolutionary modification of their thermal physiologies. However, this impairment would have been more severe if the thermal sensitivities of sprint speed had not evolved. Data from other groups of lizards indicate that the thermal sensitivity of sprint speed has not evolved to match T_b of local populations (Hertz et al., 1983; Crowley, 1985). These lizards experience less variable T_b and less impairment of sprint speeds in the field than do the anoles. Thus, selection for modification of the thermal sensitivity of sprint speed might have been stronger for anoles than for other groups of lizards.     

Mainland colonization by island lizards

Aim We investigate biogeographic relationships within the lizard genus Anolis Daudin, 1802 to test the hypothesis that the mainland (Central and South American) Norops‐clade species descended from a West Indian Anolis ancestor. Previous hypotheses have suggested that close island relatives of mainland Norops species (the Cuban Anolis sagrei and Jamaican A. grahami series) represent over‐water dispersal from a mainland ancestor. These previous hypotheses predict that the A. sagrei and A. grahami series should be phylogenetically nested within a Norops clade whose ancestral geography traces to the mainland. If Norops is West Indian in origin, then West Indian species should span the deepest phylogenetic divergences within the Norops clade. Location Central and South America and West Indian islands. Methods The phylogenetic relationships of Anolis lizards are reconstructed from aligned DNA sequences using both parsimony and Bayesian approaches. Hypotheses are tested in two ways: (1) by reconstructing the ancestral geographic location for the Norops clade using Pagel & Lutzoni's (2002) Bayesian approach, and (2) by testing alternative topological arrangements via Wilcoxon Signed‐Ranks tests ( Templeton, 1983 ) and Shimodaira–Hasegawa tests ( Shimodaira & Hasegawa, 1999 ). Results Our evidence supports an origin of mainland Norops anoles from a West Indian ancestor. A West Indian ancestor to the Norops clade is statistically supported, and alternatives to the biogeographic pattern [Cuban (Jamaican, Mainland)] are statistically rejected by Shimodaira–Hasegawa tests, although not by Wilcoxon Signed‐Ranks tests. Main conclusions Our data support the hypothesis of a West Indian origin for mainland Norops. This result contradicts previous hypotheses and suggests that island forms may be an important source for mainland biodiversity.     

A family of short retroposons (Squam1) from squamate reptiles (Reptilia: Squamata): Structure,evolution, and correlation with phylogeny

Sequences of the SINE family specific to squamate reptiles have been isolated from the genomes of lacertid lizards and sequenced. These retroposons, which we called Squam1, are 360–390 bp long and contain a region similar to the tRNA gene sequence at the 5’ end. This family has also been detected in representatives of other reptile families (varanids, iguanids (Anolis), gekkonids, and snakes), being absent from the genomes of crocodiles as well as amphibians, birds, and mammals. The primary structures of Squam1 copies have been comprehensively analyzed and compared with GenBank sequences. The genomes of most taxa contain two to three SINE subfamilies with specific diagnostic features in their primary structures. Individual similarity between the copies within each taxon is about 85%, with intrageneric similarity being only slightly higher. A comparison of consensus sequences between different lizard families has shown that Squam1 may be a convenient phylogenetic marker for this group of reptiles, having a number of both apomorphic and more or less pronounced synapomorphic features. By this criterion, snakes slightly differ from lizards but obviously belong to the same clade. However, they show no special affinity to varanids as the putative closest relatives of snakes, compared to other lizards.     

Eggshell Types and Their Evolutionary Correlation with Life-History Strategies in Squamates

The eggshell is an important physiological structure for the embryo. It enables gas exchange, physical protection and is a calcium reserve. Most squamates (lizards, snakes, worm lizards) lay parchment-shelled eggs, whereas only some gekkotan species, a subgroup of lizards, have strongly calcified eggshells. In viviparous (live-bearing) squamates the eggshell is reduced or completely missing (hereafter “shell-less”). Recent studies showed that life-history strategies of gekkotan species differ between species with parchment- and rigid-shelled eggshells. Here we test if the three different eggshell types found in the squamates are also associated with different life-history strategies. We first investigated the influence of the phylogeny on the trait “eggshell type” and on six life-history traits of 32 squamate species. Phylogenetic principal component analysis (pPCA) was then conducted to identify an association between life-history strategies and eggshell types. Finally, we also considered adult weight in the pPCA to examine its potential effect on this association. Eggshell types in squamates show a strong phylogenetic signal at a low taxonomical level. Four out of the six life-history traits showed also a phylogenetic signal (birth size, clutch size, clutches per year and age at female maturity), while two had none (incubation time, maximum longevity). The pPCA suggested an association of life-history strategies and eggshell types, which disappeared when adult weight was included in the analysis. We conclude that the variability seen in eggshell types of squamates is weakly influenced by phylogeny. Eggshell types correlate with different life-history strategies, and mainly reflect differences in adult weights of species.     

ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.     

ADAPTATION AND CONSTRAINT IN THE EVOLUTION OF SPECIALIZATION OF BAHAMIAN ANOLIS LIZARDS

Interspecific interactions affect habitat use and subsequent morphological adaptation in Anolis lizards. We examined populations of two species of Anolis lizards that evolved in the species-rich communities of Cuba and are now widespread in the Bahamas. Because the species occupy islands in the Bahamas that vary in the number of lizard species present and other characteristics, we predicted that directional selection should have led to morphological differentiation. In particular, we expected that populations on one-species islands should have evolved toward a generalist morphology because of the lack of competitors. Divergence in both species has been adaptive; populations that use wider perches have longer legs. Nonetheless, these differences are relatively minor, and none of the populations appears to have differentiated from its ancestral “ecomorph” type toward a more generalized morphology. This stasis mirrors a trend observed in the radiation of Caribbean anoles, which exhibits repeated instances of evolutionary specialization, but few or no cases of reversion to a more generalized condition. The explanation for this directionality of evolution is not obvious but probably involves the tendency of specialized species to continue using and further adapting the niches for which they are specialized even as conditions change.     

Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared

Sympatric species that initially overlap in resource use are expected to partition the environment in ways that will minimize interspecific competition. This shift in resource use can in turn prompt evolutionary changes in morphology. A classic example of habitat partitioning and morphological differentiation are the Caribbean Anolis lizards. Less well studied, but nevertheless striking analogues to the Anolis are the Southeast Asian Draco lizards. Draco and Anolis have evolved independently of each other for at least 80 million years. Their comparison subsequently offers a special opportunity to examine mechanisms of phenotypic differentiation between two ecologically diverse, but phylogenetically distinct groups. We tested whether Draco shared ecological axes of differentiation with Anolis (e.g., habitat use), whether this differentiation reflected interspecific competition, and to what extent adaptive change in morphology has occurred along these ecological axes. Using existing data on Anolis, we compared the habitat use and morphology of Draco in a field study of allopatric and sympatric species on the Malay Peninsula, Borneo and in the Philippines. Sympatric Draco lizards partitioned the environment along common resource axes to the Anolis lizards, especially in perch use. Furthermore, the morphology of Draco was correlated with perch use in the same way as it was in Anolis: species that used wider perches exhibited longer limb lengths. These results provide an important illustration of how interspecific competition can occur along common ecological axes in different animal groups, and how natural selection along these axes can generate the same type of adaptive change in morphology.     

Patterns of interspecific variation in the heart rates of embryonic reptiles

New non-invasive technologies allow direct measurement of heart rates (and thus, developmental rates) of embryos. We applied these methods to a diverse array of oviparous reptiles (24 species of lizards, 18 snakes, 11 turtles, 1 crocodilian), to identify general influences on cardiac rates during embryogenesis. Heart rates increased with ambient temperature in all lineages, but (at the same temperature) were faster in lizards and turtles than in snakes and crocodilians. We analysed these data within a phylogenetic framework. Embryonic heart rates were faster in species with smaller adult sizes, smaller egg sizes, and shorter incubation periods. Phylogenetic changes in heart rates were negatively correlated with concurrent changes in adult body mass and residual incubation period among the lizards, snakes (especially within pythons) and crocodilians. The total number of embryonic heart beats between oviposition and hatching was lower in squamates than in turtles or the crocodilian. Within squamates, embryonic iguanians and gekkonids required more heartbeats to complete development than did embryos of the other squamate families that we tested. These differences plausibly reflect phylogenetic divergence in the proportion of embryogenesis completed before versus after laying.     

Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree

Squamate reptiles (snakes, lizards, and amphisbaenians) serve as model systems for evolutionary studies of a variety of morphological and behavioral traits, and phylogeny is crucial to many generalizations derived from such studies. Specifically, the traditional dichotomy between Iguania (anoles, iguanas, chameleons, etc.) and Scleroglossa (skinks, geckos, snakes, etc.) has been correlated with major evolutionary shifts within Squamata. We present a molecular phylogenetic study of 69 squamate species using approximately 4600 (2876 parsimony-informative) base pairs (bp) of DNA sequence data from the nuclear genes RAG-1(approximately 2750 bp) and c-mos(approximately 360 bp) and the mitochondrial ND2 region (approximately 1500 bp), sampling all major clades and most major subclades. Under our hypothesis, species previously placed in Iguania, Anguimorpha, and almost all recognized squamate families form strongly supported monophyletic groups. However, species previously placed in Scleroglossa, Varanoidea, and several other higher taxa do not form monophyletic groups. Iguania, the traditional sister group of Scleroglossa, is actually highly nested within Scleroglossa. This unconventional rooting does not seem to be due to long-branch attraction, base composition biases among taxa, or convergence caused by similar selective forces acting on nonsister taxa. Studies of functional tongue morphology and feeding mode have contrasted the similar states found in Sphenodon(the nearest outgroup to squamates) and Iguania with those of Scleroglossa, but our findings suggest that similar states in Sphenodonand Iguania result from homoplasy. Snakes, amphisbaenians, and dibamid lizards, limbless forms whose phylogenetic positions historically have been impossible to place with confidence, are not grouped together and appear to have evolved this condition independently. Amphisbaenians are the sister group of lacertids, and dibamid lizards diverged early in squamate evolutionary history. Snakes are grouped with iguanians, lacertiforms, and anguimorphs, but are not nested within anguimorphs.     

Lizard scales in an adaptive radiation: variation in scale number follows climatic and structural habitat diversity in Anolis lizards

Lizard scales vary in size, shape and texture among and within species. The overall function of scales in squamates is attributed to protection against abrasion, solar radiation and water loss. We quantified scale number of Anolis lizards across a large sample of species (142 species) and examined whether this variation was related either to structural or to climatic habitat diversity. We found that species in dry environments have fewer, larger scales than species in humid environments. This is consistent with the hypothesis that scales reduce evaporative water loss through the skin. In addition, scale number varied among groups of ecomorphs and was correlated with aspects of the structural microhabitat (i.e. perch height and perch diameter). This was unexpected because ecomorph groups are based on morphological features related to locomotion in different structural microhabitats. Body scales are not likely to play an important role in locomotion in Anolis lizards. The observed variation may relate to other features of the ecomorph niche and more work is needed to understand the putative adaptive basis of these patterns. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 570–579.     

What is bred in the bone: Ecomorphological associations of pelvic girdle form in greater Antillean Anolis lizards

Ecological niche partitioning of Anolis lizards of the Greater Antillean islands has been the focus of many comparative studies, and much is known about external morphological convergence that characterizes anole ecomorphs. Their internal anatomy, however, has rarely been explored in an ecomorphological context, and it remains unknown to what degree skeletal morphology tracks the diversity and ecological adaptation of these lizards. Herein, we employ CT scanning techniques to visualise the skeleton of the pelvic girdle in situ, and 3D geometric morphometrics to compare the form of the ilium, ischium, and pubis within and between ecomorphs. We examine 26 species of anoles representing four ecomorphs (trunk‐ground, trunk‐crown, crown‐giant, twig) from three islands (Jamaica, Hispaniola, and Puerto Rico). The subtle variations in pelvic girdle morphology discovered are directly associable with all three parameters that we set out to focus on: phylogenetic relationship, specimen size, and assigned ecomorph category. Morphometric variation that correlates with size and/or phylogenetic signal varies between species and cannot be eliminated from the data set without markedly reducing its overall variability. The discovered patterns of skeletal variation are consistent with the demands of locomotor mechanics pertinent to the structural configuration of the microhabitat of three of the four ecomorphs, with the fourth having no discernible distinctive features. This manifests itself chiefly in the relative anteroposterior extent and anteroventral inclination of the ilium and pubis, which differ between ecomorphs and are postulated to reflect optimization of the direction of muscle vectors of the femoral protractors and retractors. Our investigation of the form of the pelvic girdle of anoles allows us to generalize our findings to entire ecomorph categories within a broad phylogenetic and biogeographic context. Differences in the form and configuration of the postcranial skeleton are directly related to ecological patterns.     

Roles for modularity and constraint in the evolution of cranial diversity among Anolis lizards

Complex organismal structures are organized into modules, suites of traits that develop, function, and vary in a coordinated fashion. By limiting or directing covariation among component traits, modules are expected to represent evolutionary building blocks and to play an important role in morphological diversification. But how stable are patterns of modularity over macroevolutionary timescales? Comparative analyses are needed to address the macroevolutionary effect of modularity, but to date few have been conducted. We describe patterns of skull diversity and modularity in Caribbean Anolis lizards. We first diagnose the primary axes of variation in skull shape and then examine whether diversification of skull shape is concentrated to changes within modules or whether changes arose across the structure as a whole. We find no support for the hypothesis that cranial modules are conserved as species diversify in overall skull shape. Instead we find that anole skull shape and modularity patterns independently converge. In anoles, skull modularity is evolutionarily labile and may reflect the functional demands of unique skull shapes. Our results suggest that constraints have played little role in limiting or directing the diversification of head shape in Anolis lizards.     

CONSERVED SEX CHROMOSOMES ACROSS ADAPTIVELY RADIATED ANOLIS LIZARDS

Vertebrates possess diverse sex‐determining systems, which differ in evolutionary stability among particular groups. It has been suggested that poikilotherms possess more frequent turnovers of sex chromosomes than homoiotherms, whose effective thermoregulation can prevent the emergence of the sex reversals induced by environmental temperature. Squamate reptiles used to be regarded as a group with an extensive variability in sex determination; however, we document how the rather old radiation of lizards from the genus Anolis, known for exceptional ecomorphological variability, was connected with stability in sex chromosomes. We found that 18 tested species, representing most of the phylogenetic diversity of the genus, share the gene content of their X chromosomes. Furthermore, we discovered homologous sex chromosomes in species of two genera (Sceloporus and Petrosaurus) from the family Phrynosomatidae, serving here as an outgroup to Anolis. We can conclude that the origin of sex chromosomes within iguanas largely predates the Anolis radiation and that the sex chromosomes of iguanas remained conserved for a significant part of their evolutionary history. Next to therian mammals and birds, Anolis lizards therefore represent another adaptively radiated amniote clade with conserved sex chromosomes. We argue that the evolutionary stability of sex‐determining systems may reflect an advanced stage of differentiation of sex chromosomes rather than thermoregulation strategy.     

Digging their own macroevolutionary grave: fossoriality as an evolutionary dead end in snakes

The tree of life is highly asymmetrical in its clade wise species richness, and this has often been attributed to variation in diversification rates either across time or lineages. Variations across lineages are usually associated with traits that increase lineage diversification. Certain traits can also hinder diversification by increasing extinction, and such traits are called evolutionary dead ends. Ecological specialization has usually been considered as an evolutionary dead end. However, recent analyses of specializations along single axes have provided mixed support for this model. Here, we test if fossoriality, a trait that forces specialization at multiple axes, acts as an evolutionary dead end in squamates (lizards and snakes) using recently developed phylogenetic comparative methods. We show that fossoriality is an evolutionary dead end in snakes but not in lizards. Fossorial snakes exhibit reduced speciation and increased extinction compared to nonfossorial snakes. Our analysis also indicates that transition rates from fossoriality to nonfossoriality in snakes are significantly lower than transition rates from nonfossoriality to fossoriality. Overall our results suggest that broad‐scale ecological interactions that lead to specialization at multiple axes limit diversification.     

Phylogenetic Analysis of Reptilian Hemoglobins: Trees, Rates, and Divergences

Phylogenetic relationships among reptiles were examined using previously published and newly determined hemoglobin sequences. Trees reconstructed from these sequences using maximum-parsimony, neighbor-joining, and maximum-likelihood algorithms were compared with a phylogenetic tree of Amniota, which was assembled on the basis of published morphological data. All analyses differentiated α chains into α^A and α^D types, which are present in all reptiles except crocodiles, where only α^A chains are expressed. The occurrence of the α^D chain in squamates (lizards and snakes only in this study) appears to be a general characteristic of these species. Lizards and snakes also express two types of β chains (βI and βII), while only one type of β chain is present in birds and crocodiles. Reconstructed hemoglobin trees for both α and β sequences did not yield the monophyletic Archosauria (i.e., crocodilians + birds) and Lepidosauria (i.e., Sphenodon+ squamates) groups defined by the morphology tree. This discrepancy, as well as some other poorly resolved nodes, might be due to substantial heterogeneity in evolutionary rates among single hemoglobin lineages. Estimation of branch lengths based on uncorrected amino acid substitutions and on distances corrected for multiple substitutions (PAM distances) revealed that relative rates for squamate α^A and α^D chains and crocodilian β chains are at least twice as high as those of the rest of the chains considered. In contrast to these rate inequalities between reptilian orders, little variation was found within squamates, which allowed determination of absolute evolutionary rates for this subset of hemoglobins. Rate estimates for hemoglobins of lizards and snakes yielded 1.7 (α^A) and 3.3 (β) million years/PAM when calibrated with published divergence time vs. PAM distance correlates for several speciation events within snakes and for the squamate ↔ sphenodontid split. This suggests that hemoglobin chains of squamate reptiles evolved ∼3.5 (α^A) or ∼1.7 times (β) faster than their mammalian equivalents. These data also were used to obtain a first estimate of some intrasquamate divergence times. Received: 15 September 1997 / Accepted: 4 February 1998