Dewlap Color Research Articles

Testing for heterogeneous rates of discrete character evolution on phylogenies

Abstract Many hypotheses in the field of phylogenetic comparative biology involve specific changes in the rate or process of trait evolution. This is particularly true of approaches designed to connect macroevolutionary pattern to microevolutionary process. We present a method to test whether the rate of evolution of a discrete character has changed in one or more clades, lineages, or time periods. This method differs from other related approaches (such as the “covarion” model) in that the “regimes” in which the rate or process is postulated to have changed are specified a priori by the user, rather than inferred from the data. Similarly, it differs from methods designed to model a correlation between two binary traits in that the regimes mapped onto the tree are fixed. We apply our method to investigate the rate of dewlap colour and/or caudal vertebra number evolution in Caribbean and mainland clades of the diverse lizard genus Anolis. We find little evidence to support any difference in the evolutionary process between mainland and island evolution for either character. We also examine the statistical properties of the method more generally and show that it has acceptable type I error, parameter estimation, and power. Finally, we discuss some general issues of frequentist hypothesis testing and model adequacy, as well as the relationship of our method to existing models of heterogeneity in the rate of discrete character evolution on phylogenies.

The genetic architecture of dewlap pattern in Hispaniola anoles (Anolis distichus).

Color and pattern are often critical to survival and fitness, but we know little about their genetic architecture and heritability in groups like reptiles. We investigated the genetic architecture for the pattern of the dewlap-an extensible throat fan important for communication-in anole lizards. We studied the Hispaniolan bark anole (Anolis distichus)-a species that exhibits impressive intraspecific dewlap polymorphism across its range-by conducting multigenerational experimental crosses with 2 populations, one with a solid pale yellow dewlap and another with an orange dewlap surrounded by a yellow margin. Upon rejecting the hypothesis that the extent of the orange pattern is a quantitative trait resulting from many loci of minor effect, we used a maximum likelihood model-fitting framework to show that it is better explained as a simple Mendelian trait, with the solid yellow morph being dominant over the blush orange. The relatively simple genetic architecture underlying this important trait helps explain the complex distribution of dewlap color variation across the range of A. distichus and suggests that changes in dewlap color and pattern may evolve rapidly in response to natural selection.

A picture is worth a thousand dollars: a photographic approach to studying colour in anoles

Abstract Colours relay information to conspecifics and predators unique to an environment and are shaped by natural selection favouring colours that enable higher fitness. For decades, ecologists have grappled with various methods of quantifying colour. Spectrophotometers offer precise and accurate data, but their high price limits accessibility. Here we test the validity of an accessible method of quantifying colour. We analysed photographs from four species of Anolis lizards from urban and forest habitats. We compared dewlap colour in order to determine if photographic analysis can detect inter- and intraspecific differences with the same power as a spectrophotometer. We hypothesized that photographs would capture colour data comparable to a spectrophotometer within the visible light range, and that habitat divergence would be associated with intraspecific differences in dewlap. We demonstrate, as hypothesized, that photographic colour data are consistent with spectrophotometer data and capable of differentiating dewlap variation within the visible light spectrum. Differences in colour between urban and forest populations were significant for some but not all species, and the part of the colour spectrum that shifted was not consistent across species. Our results support photographic analysis as an alternative for quantifying colour to study both inter- and intraspecific variation in visible colour.

Two new species of semiaquatic Anolis (Squamata: Dactyloidae) from Costa Rica.

We describe two new species of Draconura-clade semiaquatic anoles from the central Pacific versant of Costa Rica. The two new species are similar to Anolis aquaticus in external appearance and ecology but differ from this species in male dewlap coloration and scalation. Anolis robinsoni sp. nov. and A. riparius sp. nov. differ from each other mainly in male dewlap color. All three species are distinct according to diagnostic morphological traits and a phylogenetic analysis of mitochondrial DNA sequences (669 bases of COI gene). We discuss the distribution and ecology of Anolis aquaticus and the new species.

Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis

The Hamilton-Zuk hypothesis indicates that parasites may have a negative effect on the appearance of sexual traits within an infected individual. Anolis sagrei, or brown anoles, are small invasive lizards common throughout Florida and many other areas where they have been introduced. The colorful dewlaps under the chins of males are used as a signal during territorial contests with other males and as an ornament to attract females. Anoles may be infected by the malaria parasite Plasmodium floridense. In this study, we investigated the relationship of malarial infection with dewlap color and spectral brightness of A. sagrei. We achieved this by capturing male brown anoles, taking blood samples to examine for malarial infection, and recording the color of their dewlaps. We found that the dewlaps of infected Anolis sagrei had duller coloration than the dewlaps of uninfected lizards. These results provide support for the Hamilton-Zuk hypothesis. Our results suggest that infection by P. floridense could potentially influence fitness of the lizards by reducing the expression of their color signals. Additional research on fitness effects of the malaria parasite on anoles is important for fully understanding this phenomenon.

Evolutionary loss of complexity in animal signals: cause and consequence.

We identified hypotheses for the cause and consequences of the loss of complexity in animal signals and tested these using a genus of visually communicating lizards, the Southeast Asian Draco lizards. Males of some species have lost the headbob component from their display, which is otherwise central to the communication of this genus. These males instead display a large, colorful dewlap to defend territories and attract mates. This dewlap initially evolved to augment the headbob component of the display, but has become the exclusive system of communication. We tested whether the loss of headbobs was caused by relaxed selection, habitat-dependent constraints, or size-specific energetic constraints on display movement. We then examined whether the consequences of this loss have been mitigated by increased signaling effort or complexity in the color of the dewlap. It appears the increased cost of display movement resulting from the evolution of large body size might have contributed to the loss of headbobs and has been somewhat compensated for by the evolution of greater complexity in dewlap color. However, this evolutionary shift is unlikely to have maintained the complexity previously present in the communication system, resulting in an apparent detrimental loss of information potential.

Can Sensory Drive Explain the Evolution of Visual Signal Diversity in Terrestrial Species? A Test with Anolis Lizards.

AbstractAnimal signal colors evolve to efficiently stimulate conspecific visual systems. The sensory drive hypothesis proposes that species differences in habitat light conditions favor the evolution of color diversity. The strongest support comes from aquatic systems, while terrestrial systems offer fewer convincing examples. Anolis lizards occupy diverse habitats and signal with a colorful dewlap. Dewlap visibility depends on perceived chromatic contrast with the background. Visual system modeling has shown that red dewlaps are most visible in most habitat types. However, a majority of species possess white or yellow dewlaps. In a recent behavioral study, we showed that low light conditions can sometimes make yellow and white colors more visible by altering chromatic contrast perception with the background. Using 17 Caribbean Anolis species, we showed that cut-on wavelength, a measure of dewlap color in a white to red continuum, correlates with habitat light intensity. Pairwise comparisons revealed that red dewlaps are most visible in bright habitats, whereas yellow and white are more visible in darker habitats. We conclude that sensory drive has contributed to the evolution of dewlap color differences through the interactive effects of total habitat light intensity and chromatic contrast perception and may provide a mechanism for speciation among anoles.

Dewlap colour variation in Anolis sagrei is maintained among habitats within islands of the West Indies.

Animal signals evolve in an ecological context. Locally adapting animal sexual signals can be especially important for initiating or reinforcing reproductive isolation during the early stages of speciation. Previous studies have demonstrated that dewlap colour in Anolis lizards can be highly variable between populations in relation to both biotic and abiotic adaptive drivers at relatively large geographical scales. Here, we investigated differentiation of dewlap colouration among habitat types at a small spatial scale, within multiple islands of the West Indies, to test the hypothesis that similar local adaptive processes occur over smaller spatial scales. We explored variation in dewlap colouration in the most widespread species of anole, Anolis sagrei, across three characteristic habitats spanning the Bahamas and the Cayman Islands, namely beach scrub, primary coppice forest and mangrove forest. Using reflectance spectrometry paired with supervised machine learning, we found significant differences in spectral properties of the dewlap between habitats within small islands, sometimes over very short distances. Passive divergence in dewlap phenotype associated with isolation‐by‐distance did not seem to explain our results. On the other hand, these habitat‐specific dewlap differences varied in magnitude and direction across islands, and thus, our primary test for adaptation—parallel responses across islands—was not supported. We suggest that neutral processes or selection could be involved in several ways, including sexual selection. Our results shed new light on the scale at which signal colour polymorphism can be maintained in the presence of gene flow, and the relative role of local adaptation and other processes in driving these patterns of dewlap colour variation across islands.

Genetic analysis in Saccharum spontaneum accessions of Maharashtra collection

In this study, 41 Saccharum spontaneum accessions collected from Maharashtra, India was characterized for 13 quantitative traits and 25 qualitative traits. The accessions were then planted in the field using a randomised block design with three replications. The quantitative traits were analysed using descriptive statistics, correlation, principal component analysis and cluster analysis. Phenotypic parameters viz., plant height ranged from 74.30 to 239.60 cm, stalk diameter ranged from 2.20 to 4.80 cm and HR brix varies from 5.30 to 15.20%. Also found strong association between stalk diameter and HR brix content. In PCA analysis, the first four components exhibited more than one eigenvalue. All accessions were clustered into four groups using agglomerative cluster analysis. The  Shannon  weaver index was used to analyze the qualitative traits. The highest diversity among the traits was found for bud germpore (0.96), leaf dewlap colour (0.94), bud shape (0.93), and stalk colour- exposed to sun (090).

A new giant anole (Squamata: Iguanidae: Dactyloinae) from southwestern Ecuador.

We describe a new species of Anolis lizard from the Pacific slopes of the Andes of southwestern Ecuador at elevations between 3721,000 m. The new species belongs to the Dactyloa clade and may be distinguished from other Anolis by size, external anatomy, mitochondrial DNA divergence, and dewlap color. Based on phylogenetic analyses of mitochondrial and nuclear DNA sequence data, we found that the new species is sister to A. fraseri in a clade composed primarily of large Dactyloid species. The new species is known from a protected area in southern Ecuador, Buenaventura Reserve, which suggests that at least some its populations are well protected.

Evolutionary drivers of sexual signal variation in Amazon Slender Anoles.

Phenotypic variation among populations, as seen in the signaling traits of many species, provides an opportunity to test whether similar factors generate repeated phenotypic patterns in different parts of a species' range. We investigated whether genetic divergence, abiotic gradients, and sympatry with closely related species explain variation in the dewlap colors of Amazon Slender Anoles, Anolis fuscoauratus. To this aim, we characterized dewlap diversity in the field with respect to population genetic structure and evolutionary relationships, assessed whether dewlap phenotypes are associated with climate or landscape variables, and tested for nonrandom associations in the distributions of A. fuscoauratus phenotypes and sympatric Anolis species. We found that dewlap colors vary among but not within sites in A. fuscoauratus. Regional genetic clusters included multiple phenotypes, while populations with similar dewlaps were often distantly related. Phenotypes did not segregate in environmental space, providing no support for optimized signal transmission at a local scale. Instead, we found a negative association between certain phenotypes and sympatric Anolis species with similar dewlap color attributes, suggesting that interactions with closely related species promoted dewlap divergence among A. fuscoauratus populations. Amazon Slender Anoles emerge as a promising system to address questions about parallel trait evolution and the contribution of signaling traits to speciation.

The Effects of Limited Visual Acuity and Context on the Appearance of Anolis Lizard Dewlaps

Male Anolis lizards display their colorful dewlaps in a variety of contexts, ranging from long-distance territorial displays to close-range agonistic and courtship displays. Anoles have eyes of high optical quality and a retina that contains tightly spaced, small-diameter photoreceptors. Highest visual acuity is associated with the center of the retina (=12.5 cycles o -1), whereas acuity is much lower in the periphery. Anoles possess a small eye that creates a small retinal image, which limits their maximum visual spatial acuity to approximately 1/10 that of humans. In animal visual systems spatial resolution falls rapidly with distance from the stimulus. In some species, dewlap color patterns are fairly complex and may transmit various kinds of information. To gain insight into the visual information that conspecifics can potentially extract from dewlap color patterns, we modified high-resolution digital photographs reflecting the limits imposed by the acuity of the Anolis eye. For central retinal vision, from a distance of 0.5 m or less, the finest levels of dewlap pattern spatial detail were visible. At greater distances, and/or for peripheral vision, much less detail could be resolved. When viewed from 1 m away with peripheral vision, only the average color of the large patches could be detected, and all pattern detail was lost. The potential information content of the dewlap patterns changes dramatically with the context in which it is viewed. We show that a clear knowledge of an animal's sensory limitations can lead to greatly improved hypotheses about signal function.

Intrasexual variability of a conspicuous social signal influences attack rate of lizard models in an experimental test

Colorful sexual traits are shaped by the opposing pressures of natural and sexual selection. Although increased conspicuousness improves mating success, an individual bearing brighter sexual traits may pay direct costs in terms of detectability to predators. While it is well established that the mere presence of non-aposematic, conspicuous sexual traits influences predation risk, little empirical work has examined how within-sex variability in sexual trait coloration affects attack rates; of these studies, results are equivocal. We experimentally tested the hypothesis that, within a single sex, brighter sexually selected traits impose a greater survival risk. We created clay models resembling male water anoles (Anolis aquaticus) and manipulated the coloration (bright red vs. brown-orange) of their colorful sexual ornament, the dewlap. Models were placed and monitored within A. aquaticus habitat. Our results suggest that a more conspicuous dewlap coloration is a cause of increased attack: redder models were attacked more than twice as often as less red models. Although previous studies have found correlational relationships between conspicuous coloration and predation, or have demonstrated long-term evolutionary changes in sexual dichromatism caused by a change in predator regime, our results show direct, within-lifetime costs of conspicuous sexual coloration among individuals of the same sex. These findings correspond well with a contemporary understanding of the drivers of female choice for costly male traits. These results also suggest the need for additional study on the effects of predation on the evolution of intrasexual variation in colorful sexual traits.

Review: Lizard Evolution Virtual Lab

Heads up and right this way to discovery! Evolutionary and general biology students, teachers and lizard-lovers of all ages, HHMI-Biointeractive has put together a clever, articulate, and richly informative virtual lab to teach central concepts of evolution to high school and college students as well as AP/IB classes. Students use actual field-biology research techniques, data collection, and statistical methods in the investigation, along with documentation and classification of lizard traits and speciation in this captivating suite of activities.The website, HHMI Lizard Evolution Virtual Lab, is divided into four modules: Ecomorphs, Phylogeny, Experimental Data, and Dewlap Colors. In the Ecomorphs module, students examine pictures of eight lizards in their natural habitats (tree, twig, grass, and bush), four from Puerto Rico and four from Hispaniola (Haiti and the Dominican Republic, for the uninitiated), and group them according to appearance.Students then can gather phenotypic information about specific traits in order to make sense of their lizard classification. A video explains how scientists x-ray the lizards and scan their toe pads. After viewing a tutorial, students use a nifty measuring app to get body and hind-limb lengths and toe-pad sizes of the lizards to notice differences and similarities. They can view their compiled data set and use statistics to analyze and compare it with classmates' data. With the new trait data, students revise their initial groupings and think about the effects of natural selection in similar habitats in the two different geographic areas.In another module, students enter mitochondrial DNA sequences for the eight species into a website and build and annotate a phylogenetic tree to determine their evolutionary relationships. The tree convincingly shows that lizards with different traits living in different habitats on Puerto Rico are more closely related than they are to lizards on Hispaniola with similar traits. In other words, similar habitats on different islands select for the evolution of identical traits, demonstrating convergent evolution.Why do different lizard species on the same island not mate and reproduce? How does speciation occur? Colorful accessories, for reptiles as well as humans, add the spice to your basic green, gray, or brown! The color of the skin flap (dewlap) under the male lizard's chin is important for attracting females and for ensuring that neighboring species only mate with their own, thus maintaining a species' reproductive isolation. How different are two species' dewlap shades? Students can compare dewlaps to a sliding color bar scale to obtain precise, quantitative data for two Puerto Rican anole species; they can then calculate the means, standard deviations, and standard error of the mean and get the significance of their dewlap difference data using confidence intervals (a statistics tutorial is provided). Besides the color difference between the species, the females must also be able to see the dewlaps against the background coloration.These visually dazzling and informative virtual activities can either be done during class (time suggestions for each of the four modules are provided) or assigned for homework. Quiz questions are also included. Data can be printed out or saved, and any activity can be revisited. The website also suggests cross-curriculum and NGSS connections. The “Educators” tab includes a list of key concepts and detailed suggestions for using the lab in instruction. A five-page student handout about the activity is also provided for download.This virtual experience is a great way to teach about evolutionary concepts, including phylogenies, evolutionary histories, and common ancestry.

FEMALE SIGNAL VARIATION IN THE ANOLIS LEMURINUS GROUP

Within the lizard genus Anolis, color variation in the dewlap, an important signaling trait, can indicate local adaptation or divergence between populations. Most research on anole dewlaps has taken aim at males rather than females. Despite several publications of unrelated lizard genera with links between female signal color polymorphisms and fecundity, variation in female anole dewlaps has received less inquiry. We compiled dewlap photographs of females from several populations of the Anolis lemurinus group, characterized color variants through visual assignment, and tested for associations of dewlap color to body size and dewlap area. We describe the first case of polymorphic dewlap color in females and relatively monomorphic dewlap color in males within a group of anoles. Our survey found that female dewlap color variation in the group is more similar between geographically proximate northern populations of A. lemurinus and A. bicaorum than between populations ascribed to A. lemurinus from different regions. Additionally, we provide evidence that female body size in this group may correlate with dewlap coloration. Our findings support the need for further taxonomic research within the A. lemurinus group, as well as research into the potential mechanisms driving and maintaining color polymorphism in female signaling traits.

Diurnal colour change in a sexually dimorphic trait in the Andean lizard Anolis heterodermus (Squamata: Dactyloidae)

ABSTRACTSexual dimorphism in body size, shape and colour is widespread in lizards as well as in other taxa. In the context of sexual selection, these sex differences are commonly manifested as exaggerated male traits, which are selected by females to assess the quality of males. However, differences in sex by environment interactions can also lead to sexual dimorphism. The genus of Anolis lizards is particularly well known for sharp sexual dimorphism in dewlap colour and size; however, this is not the case in all anole species. Using digital image analyses, I assessed the existence of sexual differences in the diurnal change in colour and size of a conspicuous patch on the tail of the lizard Anolis heterodermus Duméril 1851. Results showed that the tail patch of both males and females changed in colour, but not size, from red to blue throughout the day in a similar fashion. This process took almost half a day to complete and occurred in the absence of conspecifics, suggesting that the change itself may not have an active role in social communication. However, the colour patches of males were consistently larger. The cause of the substantial variation in colour and size of the tail patch of A. heterodermus is still unknown and deserves more research. This study highlights the importance of continuous wildlife observations to identify life history traits that may be important in animal behaviour but are challenging to observe in nature.

Two new Andean species of Anolis lizard (Iguanidae: Dactyloinae) from southern Ecuador

ABSTRACTWe describe two new species of Anolis lizard that are sympatric on the Amazonian slopes of the Andes of southern Ecuador at elevations between 1440 and 1970 m. The new species may be distinguished from other Anolis by external anatomy, mitochondrial divergence and dewlap colour. We estimate the phylogenetic positions of the new species using Bayesian analysis of DNA sequence data including all species of Dactyloa-clade Anolis for which DNA data are available. Anolis hyacintogularis sp. nov. is sister to Anolis calimae, whereas Anolis lososi sp. nov. is sister to Anolis williamsmittermeierorum, herein reported for Ecuador for the first time. Individuals of both new species were collected within a protected area in southern Ecuador, Podocarpus National Park, which suggests that at least some populations of these species are well protected.www.zoobank.org/urn:lsid:zoobank.org:pub:E55FA804-E3FD-4412-8FEB-5234E29E272D

Signals and Speciation:AnolisDewlap Color as a Reproductive Barrier

Abstract The divergence of signals used in sexual selection and species recognition is thought to play an important role in speciation. As such, the striking diversity of dewlap color in Anolis lizards may have contributed to the diversification of this species-rich group. Whether the dewlap acts as a reproductive isolating barrier however remains unclear. We tested the prediction that the degree of dewlap divergence between the two closely related and highly polymorphic Hispaniolan trunk anoles Anolis distichus and Anolis brevirostris is correlated with genetic divergence and the frequency of hybridization in nature. We use integrative analyses of dewlap color variation and molecular genetics to investigate two pairs of localities where the species co-occur, including one pair of localities where the two species exhibit dissimilar dewlaps and a second pair of localities where they have similar dewlaps. At one site where species share similar dewlap coloration, we found evidence of hybridization and lower...

The taxonomic and phylogenetic status of some poorly known Anolis species from the Andes of Colombia with the description of a nomen nudum taxon

We studied the phylogenetic status, morphological variation, dewlap color variation, and geographic distribution of four poorly known Anolis species nested in the Norops clade, particularly in the A. fuscoauratus group from the Andes of Colombia. In addition, we also describe a nomen nudum species based on morphological and molecular evidence. This nomen nudum taxa differ from other fuscoauratoids species in a combination of dewlap color, meristic traits, and molecular evidence. Our integrative analysis (molecular phylogenetics, morphology, and dewlap color) revealed the non-monophyletic status of these Andean taxa. We also confirmed the occurrence of A. fuscoauratus in the Magdalena valley in Colombia (a trans-Andean region). Our findings show that the evolution of Andean anoles is more complex than previously thought and more research is necessary to understand the diversity in this cryptic group.

A genomic assessment of species boundaries and hybridization in a group of highly polymorphic anoles (distichus species complex).

Delimiting young species is one of the great challenges of systematic biology, particularly when the species in question exhibit little morphological divergence. Anolis distichus, a trunk anole with more than a dozen subspecies that are defined primarily by dewlap color, may actually represent several independent evolutionary lineages. To test this, we utilized amplified fragment length polymorphisms (AFLP) genome scans and genetic clustering analyses in conjunction with a coalescent‐based species delimitation method. We examined a geographically widespread set of samples and two heavily sampled hybrid zones. We find that genetic divergence is associated with a major biogeographic barrier, the Hispaniolan paleo‐island boundary, but not with dewlap color. Additionally, we find support for hypotheses regarding colonization of two Hispaniolan satellite islands and the Bahamas from mainland Hispaniola. Our results show that A. distichus is composed of seven distinct evolutionary lineages still experiencing a limited degree of gene flow. We suggest that A. distichus merits taxonomic revision, but that dewlap color cannot be relied upon as the primary diagnostic character.