Molecular phylogenetic perspective on evolution of lizards of the Anolis grahami series

We report the results of phylogenetic analyses of 1447 bases of mitochondrial DNA sequence for 21 populations representing seven species of the Anolis grahami series (A. conspersus, A. garmani, A. grahami, A. lineatopus, A. opalinus, A. reconditus, and A. valencienni), six of which occur on Jamaica. These data include 705 characters that are phylogenetically informative according to parsimony. A parsimony analysis of these data combined with previously published allozymic data yields a single most parsimonious tree with strong support for monophyly of the A. grahami series, the sister-group relationship between Anolis lineatopus and A. reconditus and a clade composed of Anolis garmani, A. grahami, and A. opalinus. Based on DNA data alone, A. conspersus is nested within A. grahami. Haplotypes sampled from geographic populations of A. grahami, A. lineatopus, and A. opalinus are highly divergent (approximately 12-15% sequence difference on average for each species) and show similar phylogeographic patterns, suggesting that each of these currently recognized species may be a complex of species. Anolis valencienni also shows high sequence divergence among haplotypes from different geographic populations (approximately 8% sequence difference) and may contain cryptic species. Divergence among haplotypes within A. garmani is substantially lower (approximately 3% sequence difference), and phylogeographic patterns are significantly different from those observed in A. grahami, A. lineatopus and A. opalinus.     

An incipient invasion of brown anole lizards (<Emphasis Type="Italic">Anolis sagrei</Emphasis>) into their own native range in the Cayman Islands: a case of cryptic back-introduction

Human-mediated dispersal has reshaped distribution patterns and biogeographic relationships for many taxa. Long-distance and over-water dispersal were historically rare events for most species, but now human activities can move organisms quickly over long distances to new places. A potential consequence of human-mediated dispersal is the eventual reintroduction of individuals from an invasive population back into their native range; a dimension of biological invasion termed “cryptic back-introduction.” We investigated whether this phenomenon was occurring in the Cayman Islands where brown anole lizards (Anolis sagrei) with red dewlaps (i.e., throat fans), either native to Little Cayman or invasive on Grand Cayman, have been found on Cayman Brac where the native A. sagrei have yellow dewlaps. Our analysis of microsatellite data shows strong population-genetic structure among the three Cayman Islands, but also evidence for non-equilibrium. We found some instances of intermediate multilocus genotypes (possibly 3–9% of individuals), particularly between Grand Cayman and Cayman Brac. Furthermore, analysis of dewlap reflectance data classified six males sampled on Cayman Brac as having red dewlaps similar to lizards from Grand Cayman and Little Cayman. Lastly, one individual from Cayman Brac had an intermediate microsatellite genotype, a red dewlap, and a mtDNA haplotype from Grand Cayman. This mismatch among genetic and phenotypic data strongly suggests that invasive A. sagrei from Grand Cayman are interbreeding with native A. sagrei on Cayman Brac. To our knowledge, this is the first evidence of cryptic back-introduction. Although we demonstrate this phenomenon is occurring in the Cayman Islands, assessing its frequency there and prevalence in other systems may prove difficult due to the need for genetic data in most instances. Cryptic back-introductions may eventually provide some insight into how lineages are changed by the invasion process and may be an underappreciated way in which invasive species impact native biodiversity.     

Dawn and dusk "chorus" in visually communicating Jamaican anole lizards

A key hypothesis explaining the existence of dawn and dusk choruses in acoustically communicating animals centers on the need to advertise continued territorial occupancy after and before a period of nocturnal inactivity. If this hypothesis is correct, it follows that similar dawn and dusk choruses should occur in territorial animals exploiting other signal modalities. Adult male Anolis lizards defend territories by using elaborate head-bobbing displays and extensions of a throat fan or dewlap. Males are inactive at night and return to their territories at dawn, remaining there until dusk. I quantified the production of visual displays as a function of time of day for four species on the island of Jamaica: Anolis lineatopus, Anolis sagrei, Anolis grahami, and Anolis opalinus. All exhibited dawn and/or dusk peaks in display behavior. These patterns have remarkable parallels with the dawn and dusk choruses reported for many acoustically communicating animals.     

Morphological variation in the tropical anole, Anolis casildae (Squamata: Polychrotidae)

We describe morphological variation (scalation and coloration) observed among eight individuals of the Panamanian lizard species Anolis casildae. This variation was not observed in the holotype and aids in identification of this recently described species (originally described on the basis of a single, male specimen). This species occurs only in the Reserva Forestal Fortuna (Chiriquí Province) and the adjacent Bosque Protector Palo Seco (Bocas del Toro Province) in western Panama. Anolis casildae can be distinguished from all other Panamanian anole species via six features: (1) two enlarged superciliary scales (the first larger than the second); (2) an anterior nasal scale in contact with the rostral scale or separated from the rostral by one scale; (3) 6-8 sublabial scales to the center of the eye; (4) 3-4 scales between the supraobital semicircles; (5) unique coloration (4-6 oblique brown bands interspersed by blue-outlined yellow patches; dewlap is a dirty cream color with broad yellow scale rows irregularly interspersed with smaller emerald green scales) and (6) A. casildae occurs from 1,050 to 1,400 m in the Cordillera Central. We also compare our natural history observations of A. casildae to a similar large anole, A. frenatus, a species which we believe A. casildae to be closely related.     

Dewlap and other variation in the lizards Anolis distichus and A. brevirostris (Reptilia: Iguanidae)

The dewlap of male anoline lizards is an important component of the mate recognition system. Much attention has focussed on the role dewlap colour plays in the interactions between species of Anolis but little has been paid to the effects of intraspecific variability in this feature. Patterns of intrasubspecific variability in this feature are described for several subspecies of Anolis distichus and A. brevirostris . In most cases variability in dewlap colour appears unrelated to the amount of electrophoretic variability and the level of population differentiation, although there is some evidence for large scale geographic subdivision within three of the taxa examined. Female choice and the implications for various species concepts are discussed.     

Escape tactics and effects of perch height and habituation on flight initiation distance in two Jamaican anoles (Squamata: polychrotidae)

Escape by Anolis lizards is influenced by microhabitats and fight initiation distance increases with predation risk. Differences in microhabitat use among ecomorphs affect escape behavior, but only two studies have reported ecomorphological differences in flight initiation distance among Greater Antillean species. I studied effects of predation risk and microhabitats on escape behavior by conducting field experiments using two species of anoles, Anolis lineatopus and A. grahami, on the campus of the University of the West Indies at Mona, Jamaica. Because ecomorphological variation of anoles has evolved independently within each island of the Greater Antilles, but relationships between ecomorphs and escape behaviors are poorly known, I characterized microhabitat use and escape tactics, and determined relationships between flight initiation distance and two risk factors, habituation to human presence and perch height, in Anolis lineatopus, a trunk-ground anole and A. grahami, a trunk-crown anole. Sample sizes for A. lineatopus and A. grahami were 214 and 93, for microhabitat use and escape destinations, 74 and 34 for human presence and 125 and 34 for perch height. The two species occurred in similar microhabitats and exhibited similar escape tactics, but exhibited key differences expected for their ecomorphs. Both species were sighted frequently on the ground and on trees, but A. lineatopus were more frequently on ground and were perched lower than A. grahami. Both species escaped from ground to trees and when on trees hid on far sides and escaped without changing climbing direction with equal frequency. The frequency of fleeing upward was greater for A. grahami than A. lineatopus. Both species exhibited habituation by having shorter flight initiation distances in areas with more frequent exposure to people. In both species flight initiation distance increased as perch height decreased because, lizards had to climb farther to be out of reach when perched lower. The relationship between flight initiation distance and perch height may apply to other anole ecomorphs that flee upward when low perched on trees.     

Phylogeny,paraphyly and ecological adaptation of the colour and pattern in the Anolis roquet complex on Martinique

Martinique is an environmentally heterogeneous island with a complex geological history. It is occupied by a solitary anole, Anolis roquet, showing marked geographical variation in colour and other features. Phylogenetic analysis of a segment (1 kb) of the mitochondrial cytochrome b gene across the Anolis roquet series in the southern Lesser Antilles and at 63 localities of Anolis roquet in Martinique indicate that A. roquet is paraphyletic as A. extremus (Barbados) is nested within the Martinique populations. Moreover, divergent phylogenetic lineages exist within Martinique (max. 10.6% uncorrected pairwise), and these lineages are closely associated with the geological history of this complex island. However, objective quantification of the spectroradiometric analysis of hue by delta analysis, together with analysis of the colour pattern, indicate that they are primarily determined by adaptation to environmental conditions, irrespective of these phylogenetic lineages. There is remarkable convergence in hue and pattern in both extreme xeric (dark chevrons on a dull, generally grey/brown, background), and montane conditions (black reticulation and non-UV white spots on a bright, saturated green background). Moreover, parallel trends occur between Martinique and other Lesser Antillean anoles, which further argues for adaptation (increase in green saturation in montane areas and higher levels of UV on the dewlap of some Atlantic forms). As an exception, there are two specific situations where anoles from different lineages look different. These are (i). in the low-altitude regions of the northwest where the northwestern and central lineages make contact, and (ii). in the far south of the island where the southern and central lineages meet.     

Biased predation could promote convergence yet maintain diversity within Müllerian mimicry rings of Oreina leaf beetles

Müllerian mimicry is a classic example of adaptation, yet Müller's original theory does not account for the diversity often observed in mimicry rings. Here, we aimed to assess how well classical Müllerian mimicry can account for the colour polymorphism found in chemically defended Oreina leaf beetles by using field data and laboratory assays of predator behaviour. We also evaluated the hypothesis that thermoregulation can explain diversity between Oreina mimicry rings. We found that frequencies of each colour morph were positively correlated among species, a critical prediction of Müllerian mimicry. Predators learned to associate colour with chemical defences. Learned avoidance of the green morph of one species protected green morphs of another species. Avoidance of blue morphs was completely generalized to green morphs, but surprisingly, avoidance of green morphs was less generalized to blue morphs. This asymmetrical generalization should favour green morphs: indeed, green morphs persist in blue communities, whereas blue morphs are entirely excluded from green communities. We did not find a correlation between elevation and coloration, rejecting thermoregulation as an explanation for diversity between mimicry rings. Biased predation could explain within‐community diversity in warning coloration, providing a solution to a long‐standing puzzle. We propose testable hypotheses for why asymmetric generalization occurs, and how predators maintain the predominance of blue morphs in a community, despite asymmetric generalization.     

Saurian malaria in the Caribbean: Plasmodium azurophilum sp. nov., a malarial parasite with schizogony and gametogony in both red and white blood cells

A survey of 466 Caribbean lizards found Plasmodium parasites present in Anolis species only of five islands. Parasites presently considered to be P. floridense occurred on Grand Cayman, North Bimini, Jamaica, Hispaniola (Haiti), and Puerto Rico. A second species, P. azurophilum, is described as new from Anolis cybotes of Haiti, A. krugi of Puerto Rico, and A. lineatopus and A. grahami of Jamaica. It lacks visible pigment in erythrocytic host cells but can produce it occasionally. Both asexual and sexual forms occur in a variety of white blood cells, notably in azurophil granulocytes and polymorphonuclear leucocytes. Experimental infections indicate that the leucocytic phase occurs after the acute erythrocytic infection declines, thus suggesting that the schizogonic and gametogonic cycles in white cells may represent an adaptive defense against immune mechanisms of the host. Mean numbers of nuclei in schizonts and mean gametocyte size are influenced by host species and type of host cell.     

A new species of dactyloid anole (Iguanidae, Polychrotinae, Anolis) from the southeastern slopes of the Andes of Ecuador

We describe a new species of Anolis from the southeastern slopes of the Andes of Ecuador, province of Zamora-Chinchipe, Parque Nacional Podocarpus. It belongs to (1) the aequatorialis species-group by being of moderate to large size with narrow toe lamellae, and (2) the eulaemus sub-group by having a typical Anolis digit, in which the distal lamellae of phalanx II distinctly overlap the proximal scales of phalanx I. The new species is most similar morphologically to Anolis fitchi but differs from it mainly by having a dewlap with longitudinal rows of 2-5 granular, minute scales separated by naked skin (longitudinal rows of one or two keeled, large scales separated by naked skin in Anolis fitchi) and a vertically shorter dewlap (longer dewlap in Anolis fitchi).     

An experimental test of the effect of food and antioxidants on blue‐green eggshell coloration in mountain bluebirds Sialia currucoides

Evolutionary biologists have long debated the functional relevance of the ornamental traits that occur in many animal taxa, and yet, female ornaments have received relatively little attention compared to those produced by males. A greater understanding of these traits, particularly those that are unique to females, may shed light on the potential for sexual selection to shape female phenotypes. Recently, blue‐green eggshell colour, derived from the antioxidant pigment biliverdin, has been proposed as a candidate trait that advertises female quality to males in species of birds with biparental care. However, studies have been equivocal in their support for blue‐green eggshell colour being an informative signal, and correlations between eggshell colour and other female characteristics have been inconsistent. We conducted a supplementation experiment to test if improving the access of female birds to food resources and micronutrients, thereby improving their condition prior to egg laying, would intensify the blue‐green colouration of the eggs they laid. We provided mountain bluebirds Sialia currucoides with food and carotenoids during nest building and egg laying in two breeding seasons, and assessed both within‐ and among‐clutch variation in colour. Supplementation did not affect patterns of within‐clutch variation, but did result in differences in colour among clutches. Specifically, we found that food, but not carotenoids, resulted in higher colour saturation, and decreased the brightness of blue‐green eggshells. Although this trend was observed in both years, the effect was statistically significant only in one year. Our results suggest that food supplementation influences eggshell colour, but that conditions, such as weather and natural food availability, which can vary annually, may also determine how female birds allocate pigment to eggshells.     

Climate‐related environmental variation in a visual signalling device: the male and female dewlap in Anolis sagrei lizards

Animals communicate using a variety of signals that differ dramatically among and within species. The astonishing dewlap diversity in anoles has attracted considerable attention in this respect. Yet, the evolutionary processes behind it remain elusive and have mostly been explored for males only. Here, we considered Anolis sagrei males and females to study signal divergence among populations. First, we assessed the degree of variation in dewlap design (size, pattern and colour) and displays by comparing 17 populations distributed across the Caribbean. Second, we assessed whether the observed dewlap diversity is associated with variation in climate‐related environmental conditions. Results showed that populations differed in all dewlap characteristics, with the exception of display rate in females. We further found that males and females occurring in ‘xeric’ environments had a higher proportion of solid dewlaps with higher UV reflectance. In addition, lizards inhabiting ‘mesic’ environments had primarily marginal dewlaps showing high reflectance in red. For dewlap display, a correlation with environment was only observed in males. Our study provides evidence for a strong relationship between signal design and prevailing environmental conditions, which may result from differential selection on signal efficacy. Moreover, our study highlights the importance of including females when studying dewlaps in an evolutionary context.     

Analysis of color spectra in comparative evolutionary studies: molecular phylogeny and habitat adaptation in the St. Vincent Anole (Anolis trinitatis)

The use of color (as distinct from color pattern) in comparative evolutionary studies is important, and objective, independent characters are needed. A new method was employed to investigate geographic color variation in the small arboreal lizard Anolis trinitatis on the island of St. Vincent. The simple delta analysis (based on the difference between eigenvector coefficients for adjacent regions of the spectrum) is aimed at increasing the objectivity with which a spectrum is cut into independent segments and does not predetermine segment width or number. There are distinct habitat types within this small island and distinct phylogenetic lineages (based on a kilobase of cytochrome b sequence) within this species. A series of matrix correspondence (Mantel) tests indicate that aspects of color are associated with habitat type (e.g., green dorsum in rain forest lizards), molecular phylogeny, or both. Hence, both adaptation by selection and historical processes are implicated as causes of geographic variation in color. The dewlap variation (e.g., strong ultraviolet reflectance in some Atlantic coastal sites) is very pronounced and, contrary to some expectations, may result in reproductive isolation even within small Lesser Antillean islands.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Attractive blue‐green egg coloration and cuckoo−host coevolution

Recent evidence suggests that blue‐green coloration of bird eggshells may be related to female and/or egg phenotypic quality, and that such colour may affect parental effort and therefore the nutritional environment of developing nestlings. Here we suggest that these relationships and the signal function of eggshell coloration would affect the outcome of coevolution between avian brood parasites and their hosts in at least three different non‐exclusive evolutionary pathways. First, by laying blue‐green coloured eggs, cuckoo females may exploit possible sensory biases of their hosts, constraining the evolution of parasitic egg recognition, and thus avoid rejection. Second, because of the relatively high costs of laying blue eggs, cuckoo females may be limited in their ability to mimic costly blue‐green eggs of their hosts because cuckoo females lay many more eggs than their hosts. Furthermore, costs associated with foreign egg recognition errors would be relatively higher for hosts laying blue eggs. Third, cuckoos may use coloration of host eggs for selecting individuals or specific hosts of appropriate phenotypic quality (i.e. parental abilities). We here explored some predictions emerging from the above scenarios and found partial support for two of them by studying egg coloration of European cuckoos (Cuculus canorus) and that of their 25 main hosts, as well as parasitism and rejection rate of hosts. Cuckoo hosts parasitized with more blue, green, and ultraviolet cuckoo eggs, or those laying more blue‐green eggs, were more prone to accept experimental parasitism with artificial cuckoo eggs. In addition, coloration of cuckoo eggs is more variable when parasitizing hosts laying bluer‐greener eggs, even after controlling for the effect of host egg coloration (i.e. degree of egg matching). Globally, our results are consistent with the proposed hypothesis that host egg traits that are related to phenotypic quality of hosts, such as egg coloration, may have important implications for the coevolutionary interaction between hosts and brood parasites. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 154–168.     

The incredible shrinking dewlap: signal size,skin elasticity,and mechanical design in the green anole lizard (Anolis carolinensis)

The expression of male secondary sexual traits can be dynamic, changing size, shape, color, or structure over the course of different seasons. However, the factors underlying such changes are poorly understood. In male Anolis carolinensis lizards, a morphological secondary sexual signal called the dewlap changes size seasonally within individuals. Here, we test the hypothesis that seasonal changes in male dewlap size are driven by increased use and extension of the dewlap in spring and summer, when males are breeding, relative to the winter and fall. We captured male green anole lizards prior to the onset of breeding and constrained the dewlap in half of them such that it could not be extended. We then measured dewlap area in the spring, summer, and winter, and dewlap skin and belly skin elasticity in summer and winter. Dewlaps in unconstrained males increase in area from spring to summer and then shrink in the winter, whereas the dewlaps of constrained males consistently shrink from spring to winter. Dewlap skin is significantly more elastic than belly skin, and skin overall is more elastic in the summer relative to winter. These results show that seasonal changes in dewlap size are a function of skin elasticity and display frequency, and suggest that the mechanical properties of signaling structures can have important implications for signal evolution and design.     

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.     

What determines dewlap diversity in Anolis lizards? An among‐island comparison

Animal signalling systems are extremely diverse as they are under different, often conflicting, selective pressures. A classic textbook example of a diverse signal is the anoline dewlap. Both at the inter‐ and intraspecific levels, dewlap size, colour, shape and pattern vary extensively. Here, we attempt to elucidate the various factors explaining the diversity in dewlap size and pattern among seven Anolis sagrei populations from different islands in the Bahamas. The seven islands differ in the surface area, number and kind of predators, sexual size dimorphism and Anolis species composition. In addition, we investigate whether selective pressures acting on dewlap design differ between males and females. Whereas dewlap pattern appears to serve a role in species recognition in both sexes, our data suggest that relative dewlap size is under natural and/or sexual selection. We find evidence for the role of the dewlap as a pursuit‐deterrence signal in both males and females as relative dewlap size is larger on islands where A. sagrei occurs sympatrically with predatory Leiocephalus lizards. Additionally, in males relatively large dewlaps seem to be selected for in a sexual context, whereas in females natural selection, for instance by other predators than Leiocephalus lizards, appears to constrain relative dewlap size.     

Are subspecies of Anolis lizards that differ in dewlap color and pattern also genetically distinct? A mitochondrial analysis

Subspecies of Anolis lizards are often defined on the basis of geographic variation in the color and pattern of the dewlap, an extensible throat fan considered central to species recognition and sexual selection. Among the most impressive examples of this phenomenon are two species of trunk anoles found across Hispaniola and the Bahamas: Anolis distichus is divided into 16 subspecies with dewlap colors ranging from deep wine red to pale yellow while Anolis brevirostris is divided into three subspecies with dewlaps ranging from pale yellow to orange. Limited sampling of allozyme data indicates some genetic divergence among subspecies and suggests that they may deserve recognition at the species-level. Our goal here is to use more comprehensive geographic sampling of mtDNA haplotypes to test whether the five subspecies of A. distichus and three subspecies of A. brevirostris that occur in the Dominican Republic correspond with genetically distinct populations that may warrant recognition under the general lineage concept. We obtain an aligned dataset of 1462bp comprised of the genes encoding ND2 and adjacent tRNAs from 76 individuals of A. distichus from 28 localities and 12 individuals of A. brevirostris from five localities. We find that haplotypes sampled from each Dominican subspecies of A. distichus form well-supported and deeply divergent clades (>10% uncorrected sequence divergence). Strong concordance between mtDNA haplotype structure and previously diagnosed phenotypic variation in traits central to interspecific communication (i.e., the dewlap) leads us to hypothesize that each of the presently recognized Dominican subspecies of A. distichus and A. brevirostris deserves elevation to full species status under the general lineage concept.     

No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment

Condition-dependence is a central but contentious tenet of evolutionary theories on the maintenance of ornamental traits, and this is particularly true for structural plumage colour. By providing diets of different nutritional quality to moulting male and female blue tits, we experimentally manipulated general condition within the natural range, avoiding deprivation or stressful treatments. We measured reflectance of the structural-coloured UV/blue crown, a sexually selected trait in males, and the white cheek, a nonpigmented structural colour, directly after moult and again during the following spring mating season. We employed a variety of colour indices, based on spectral shape and avian visual models but, despite significant variation in condition and coloration, found no evidence for condition-dependence of UV/blue or white plumage colour during either season. These and previously published results suggest that structural colour might be sensitive to stress, rather than reduced body condition, during moult.