Dewlap Color Research Articles

Using genomic data to revisit an early example of reproductive character displacement inHaitianAnolislizards

The pattern of reproductive character displacement (RCD)-in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation-is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A.caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.

The Role of Heritable and Dietary Factors in the Sexual Signal of a Hispaniolan Anolis Lizard, Anolis distichus

The diversity of sexual signals is astounding, and divergence in these traits is believed to be associated with the early stages of speciation. An increasing number of studies also suggest a role for natural selection in driving signal divergence for effective transmission in heterogeneous environments. Both speciation and adaptive divergence, however, are contingent on the sexual signal being heritable, yet this often remains assumed and untested. It is particularly critical that the heritability of carotenoid-based sexual signals is investigated because such traits may instead be phenotypically plastic indicators of an individual's quality that exhibit no or little heritable variation. We present the first study to investigate the relative contribution of genetic and environmental factors to the striking diversity of dewlap color and pattern in Anolis lizards. Using a breeding experiment with Anolis distichus populations exhibiting different dewlap phenotypes, we raise F1 offspring in a common garden experiment to assess whether dewlap color is inherited. We follow this with carotenoid supplementation to investigate the influence of dietary pigments to dewlap color variation. We find significant differences in several aspects of dewlap color and pattern to persist to the F1 generation (fathers: N = 19; F1 males: N = 50; P < 0.01) with no change in dewlap phenotype with carotenoid supplementation (N = 52; P > 0.05). These results strongly support that genetic differences underlie dewlap color variation, thereby satisfying a key requirement of natural selection. Our findings provide an important stepping-stone to understanding the evolution of an incredibly diverse signal important for sexual selection and species recognition.

CORRELATION BETWEENANOLISLIZARD DEWLAP PHENOTYPE AND ENVIRONMENTAL VARIATION INDICATES ADAPTIVE DIVERGENCE OF A SIGNAL IMPORTANT TO SEXUAL SELECTION AND SPECIES RECOGNITION

Although the importance of signals involved in species recognition and sexual selection to speciation is widely recognized, the processes that underlie signal divergence are still a matter of debate. Several possible processes have been hypothesized, including genetic drift, arbitrary sexual selection, and adaptation to local signaling environments. We use comparative analyses to investigate whether the remarkable geographic variation of dewlap phenotype in a Hispaniolan trunk Anolis lizard (A. distichus) is a result of adaptive signal divergence to heterogeneous environments. We recover a repeated pattern of divergence in A. distichus dewlap color, pattern, and size with environmental variation across Hispaniola. These results are aligned with ecological models of signal divergence and provide strong evidence for dewlap adaptation to local signaling environments. We also find that A. distichus dewlaps vary with the environment in a different manner to other previously studied anoles, thus expanding upon previous predictions on the direction dewlaps will diverge in perceptual color space in response to the environment.

Evidence for the recognition of two species of Anolis formerly referred to as A. tropidogaster (Squamata: Dactyloidae)

Based on differences in hemipenial morphology, male dewlap coloration, pholidosis, and 16S mtDNA, we recognize twospecies of anoles related to what was formerly referred to as Anolis tropidogaster: Anolis tropidogaster Hallowell 1856and A. gaigei Ruthven 1916. The hemipenis in A. tropidogaster is large, bulbous, and bilobed whereas it is small, thin,and unilobed in A. gaigei; the male dewlap is almost uniform purplish red, sometimes with a paler orange central area inA. tropidogaster versus orange yellow with a darker orange central area in A. gaigei; and—aside from more subtle differ-ences in several pholidotic characteristics—in male A. gaigei there is a pair of greatly enlarged postcloacal scales whichis absent in A. tropidogaster. In the western part of its geographic range, A. gaigei has been confused with another anolespecies, A. polylepis Peters 1873, from which it can be readily distinguished by its strongly keeled ventral scales (smooth in A. polylepis).

Genetic differentiation among populations of a Hispaniolan trunk anole that exhibit geographical variation in dewlap colour

Long neglected by classic island biogeographical theory, speciation within and among islands is increasingly recognized as a major contributor to insular diversity. Although the factors responsible for island speciation remain poorly understood, this process appears critically dependent on geographical variation and speciation in allopatry or parapatry. Here, we investigate geographical variation and speciation in a complex of Hispaniolan trunk anoles (Anolis distichus), where populations with strikingly distinct dewlap colours and patterns correspond with deeply divergent mtDNA structure. Using a multilocus, population-level analysis, we investigate whether these phenotypically and mitochondrially distinct populations exhibit the type of nuclear differentiation expected among species or incipient species. Along a transect that extends across a recently recessed marine barrier, our results are consistent with the persistence of an abrupt phenotypic and mitochondrial transition following secondary contact, in spite of little or no evidence for a reduction in nuclear gene flow. Along a second transect extending across a steep environmental gradient, our phenotypic and microsatellite data suggest a sharp genetic break with little or no admixture, whereas mtDNA recovers a signature of extensive unidirectional introgression. Together, these results are consistent with previous studies of Lesser Antillean anoles, suggesting that allopatric divergence alone is insufficient for speciation, whereas reduced gene flow and partial reproductive isolation may accumulate in the presence of ecological gradients.

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 of Genetic Differentiation Between Anoles With Different Dewlap Color Patterns

Color variation across and within populations can play an important role in speciation and our understanding of the maintenance of genetic variation. Trait polymorphisms may be important in reproductive isolation and speciation. Conversely, if 2 morphs exist within a species, then the classical question of how the polymorphism is maintained in the face of drift and selection becomes relevant. In Anolis lizards, variations in dewlap size and color are often used as diagnostic markers of species and considered important traits in population divergence and speciation. The aim of this study was to describe dewlap color pattern variation in Anolis apletophallus and estimate gene flow between populations that have different dewlap color patterns. We confirmed that 2 dewlap morphs exist, a "solid" morph that has an orange dewlap and a "basal" morph that has a white dewlap with an orange basal spot. Throughout most of A. apletophallus' range, the morphs have nonoverlapping distributions, except for one area where both morphs occur in equal frequencies. Analysis of reflectance spectra demonstrated that the color of the dewlap margin differed between morphs but that dewlap color and pattern did not differ across populations within morphs. Using 8 microsatellite markers, we found little genetic differentiation between populations or individuals with different dewlap morphs. In contrast, the small amount of genetic structure that does exist is due to current day geographic barriers. Therefore, dewlap color variation in A. apletophallus appears to be a polymorphism rather than an indicator of 2 fully or partially reproductively isolated populations.

Carotenoid Access, Nutritional Stress, and the Dewlap Color of Male Brown Anoles

Carotenoids are integumentary colorants that must be ingested by vertebrates to be used as colorants. In many studies of fish and birds, carotenoid color serves as an indicator of foraging success, nutritional state, or parasite load. The dewlap of male Brown Anoles (Norops sagrei) contains the carotenoid pigments lutein and zeaxanthin. We performed a two-factor experiment to determine the effects of nutritional stress and xanthophyll supplementation on male dewlap color in N. sagrei. We tested the hypotheses that dewlap color is dependent on access to carotenoids and good nutrition. Contrary to our predictions we found no significant differences among groups of anoles that were either supplemented or not supplemented with carotenoids. Similarly, post-experimental dewlap spectral variation did not differ significantly among groups that were provided a standard or reduced diet. These findings demonstrate that dewlap color of adult male Brown Anoles does not change in response to food access or carotenoid supplementation.

Habitat light and dewlap color diversity in four species of Puerto Rican anoline lizards

Closely related species often have signals that differ dramatically in design. The evolution of such differences may be important in the process of speciation. Selection for signal detectability under different habitat conditions has been proposed as a mechanism leading to the evolution of signal diversity. We examined dewlap color in four closely related species of Anolis lizards that occupy habitats with different light conditions. Initially, we tested the hypothesis that lizards choose specific light conditions within each habitat in which to signal. We rejected this hypothesis for all four species. We next calculated the detectability of the dewlap color of all four species at display locations in each habitat. If selection for detectability under the different light conditions explained the divergence in signal design, the occupant of a given habitat was predicted to have the highest signal detectability in that habitat. However, the rank order of detectability of the four dewlap colors was nearly the same in all four habitats. We concluded that divergent selection for signal detectability does not, by itself, explain the evolution of dewlap color diversity. We hypothesize that the evolution of dewlap color diversity results from simultaneous selection for multiple functions of dewlap color.

How dewlap color reflects its carotenoid and pterin content in male and female brown anoles (Norops sagrei)

Sexually selected colors in animals can be created by multiple pigments (e.g., carotenoids, melanins, pterins), but how these pigment classes interact to generate intraspecific color variation has rarely been tested, especially in reptiles. We examined full-spectrum color variation as well as pterin (i.e., drosopterin) and carotenoid (i.e., xanthophyll) pigment concentrations in the yellow and red sexually dichromatic dewlaps of male and female Brown Anoles (Norops sagrei) to understand their color-generating mechanisms and information content. Reflectance curves showed significant sexual differences in dewlap color that could only partially be explained by pigment composition. For example, drosopterin concentration correlated significantly with red chroma in the male's dewlap center. In females, drosopterin concentration correlated significantly with yellow and red chroma along the dewlap edge. In addition, xanthophyll concentration showed a significant inverse correlation with hue in the center of female dewlaps only. There were several other correlations between pigment concentrations and spectral variables, which hinted at ways that pigments produce color in male and female dewlaps, but these were non-significant after statistically correcting for multiple comparisons. These results demonstrate that sexes differ in how pigment classes influence dewlap spectral variation, but also that there may be other aspects of the integument not measured here that also influence dewlap color.

Eleven highly polymorphic microsatellite markers for the lizard Anolis distichus

We isolated and characterized 11 polymorphic microsatellite loci for Anolis distichus, a West Indian lizard endemic to Hispaniola and the Bahamas. The number of alleles per locus ranged from 10 to 34, with levels of observed heterozygosity ranging from 0.10 to 1.00. Four loci significantly deviated from Hardy–Weinberg equilibrium for most of the populations sampled, and seven pairs of loci demonstrated linkage disequilibrium for 1–2 populations. These markers provide a valuable set of tools for fine-scale population genetics studies of A. distichus, a species that exhibits striking geographic variation in dewlap coloration and pattern.

New Species of Anolis Formerly Referred to as Anolis altae from Monteverde, Costa Rica (Squamata: Polychrotidae)

Abstract I describe a new species of Anolis formerly referred to as Anolis (or Norops) altae from Monteverde, Costa Rica. The new species differs from Anolis altae by having a small unilobate hemipenis (large and bilobate in A. altae), in male dewlap coloration (male dewlap more or less uniformly reddish-orange in A. altae versus basal portion yellow ocher to orange yellow, distal portion reddish-orange in the new species), and in the mean values of several scalation and morphometric characteristics (e.g., ratio tail length/SVL 1.8–2.2, mean 2.1 in A. altae vs. 1.7–1.9, mean 1.8 in the new species). At this point no characteristics, besides geographic location, are known to separate females of the new species from A. altae.

Another New Species of Green Anolis (Squamata: Iguania) from the Eastern Andes of Peru

We describe a new species of Anolis from cloud forest habitat in Department of San Martin, Peru. The new species shares distinctive aspects of color and scalation with Anolis huilae from Colombia and Anolis boettgeri and Anolis cuscoensis from Peru but differs from these species in dewlap color, limb length, and scalation. Phylogenetic analysis places the species among the basal group of “alpha” Anolis (latifrons group sensu lato, “Dactyloa”).

FOUR NEW SPECIES OF ANOLES (GENUS ANOLIS) FROM THE SERRANÍA DE TABASARÁ, WEST-CENTRAL PANAMA (SQUAMATA: POLYCHROTIDAE)

We describe four new species of anoles (genus Anolis) from the Serranía de Tabasará, west-central Panama. Two of the new species are most similar in external morphology to a cluster of Central American species that are short-legged (fourth toe of adpressed hindlimb reaches only to tympanum), have a single elongated prenasal scale, smooth ventral scales, and slender habitus, often delicate. They differ from the other species in this cluster by hemipenial morphology and scalation characteristics. One of the new species appears to be most similar to A. pachypus and A. tropidolepis from which it differs by male dewlap coloration and its very small dorsal head scales. The fourth new species appears to be most similar to A. laeviventris from which it differs by its multicarinate head scales, lack of heterogeneous flank scalation, and an overall green coloration.

Contributions of pterin and carotenoid pigments to dewlap coloration in two anole species

Animals can acquire bright coloration using a variety of pigmentary and microstructural mechanisms. Reptiles and amphibians are known to use two types of pigments—pterins and carotenoids—to generate their spectrum of colorful red, orange, and yellow hues. Because both pigment classes can confer all of these hues, the relative importance of pterins versus carotenoids in creating these different colors is not always apparent. We studied the carotenoid and pterin content of red and yellow dewlap regions in two neotropical anole species—the brown anole ( Norops sagrei) and the ground anole ( N. humilis). Pterins (likely drosopterins) and carotenoids (likely xanthophylls) were present in all tissues from all individuals. Pterins were more enriched in the lateral (red) region, and carotenoids more enriched in the midline (yellow) region in N. humilis, but pterins and carotenoids were found in similar concentrations among lateral and midline regions in N. sagrei. These patterns indicate that both carotenoid and pterin pigments are responsible for producing color in the dichromatic dewlaps of these two species, and that in these two species the two pigments interact differently to produce the observed colors.

Role of the adrenal gland in early post-hatching differentiation of alternative male phenotypes in the tree lezard ( Urosaurus ornatus)

During development, sex steroids are important in establishing differences between males and females. However, sex steroids also are involved in the development and maintenance of individual differences in morphology and behavior within each sex. As adults, male tree lizards ( Urosaurus ornatus) exhibit alternative reproductive tactics correlated with dewlap (throat fan) coloration. Males with orange-blue dewlaps are aggressive and territorial, whereas males with orange dewlaps are less aggressive and employ a satellite strategy. Dewlap coloration develops within the first 90 days after hatching and remains fixed throughout life. Recent work demonstrates that individual males differ in progesterone and testosterone secretion during development, suggesting that these hormones regulate the development of alternative male phenotypes. The current work uses in vitro incubation of adrenal and gonadal tissues to identify the source of progesterone and testosterone during the period of male differentiation and to follow ontogenetic changes in hormone release. The results indicate that, in all developmental stages sampled, adrenal incubations primarily contain progesterone and corticosterone whereas gonadal incubations contain primarily testosterone. These data indicate that the hatchling adrenal is the primary source of progesterone during early post-hatching development. Since progesterone has been demonstrated to play a role in the establishment of individual differences in morphology and behavior in male tree lizards, our results suggest that the hatchling adrenal gland plays an important role in post-hatching development of alternative male phenotypes.

Color Variation, Habitat Light, and Background Contrast in Anolis carolinensis along a Geographical Transect in Florida1

Abstract A hallmark trait of the lizard genus Anolis is the presence of remarkable interspecific variation in dewlap color patterns. Yet, considerable intraspecific variation also occurs in many Anolis species. In Florida different populations of the Green Anole (Anolis carolinensis) exhibit red, pink, magenta, and even greenish-gray dewlaps. To date, comparisons of color variation in this species have used subjective techniques based on human color perception. Instead, we used an objective method—reflectance spectrometry—to quantify A. carolinensis dewlap and body color variation along a transect from northeastern to southwestern Florida. Reflectance readings of local vegetation allowed us to calculate contrast of the lizards with their visual backgrounds. By incorporating local ambient light and A. carolinensis spectral sensitivity into additional calculations, we were able to estimate lizard-background contrast from the perspective of the lizards. Results revealed dewlap and dorsum spectra to differ si...

Habitat light, colour variation, and ultraviolet reflectance in the Grand Cayman anole, Anolis conspersus

Data from a diversity of sources are consistent with the hypothesis that the Grand Cayman anole,Anolis conspersus , is descended directly from Anolis grahami of Jamaica. Although the two species have remained morphologically similar, coloration in A. conspersus has changed considerably from that of its ancestor. The most dramatic difference is seen in dewlap colour, where A. conspersus has evolved a blue and highly UV-reflective dewlap from the ancestral orange-and-yellow colour state. In addition, variation in normal (non-metachrosis) dorsum coloration in A. grahami populations is limited to shades of green (olive, emerald, teal), whereas in A. conspersus dorsum coloration varies from green to blue and to brown. This increased colour variation occurs despite Grand Cayman being a small, relatively featureless island only 35 km in length. Results of this study suggest that ambient light differences associated with precipitation-related vegetation structure may have played an important role in the evolution of A. conspersus body colour variation. Evidence is presented to show how geological, ecological, and physiological factors could have interacted to select for a short wavelength-reflective dewlap from a long wavelength-reflective precursor following the colonization of Grand Cayman from Jamaica by A. grahami between 2 and 3 Mya.

Habitat light, colour variation, and ultraviolet reflectance in the Grand Cayman anole, Anolis conspersus

Data from a diversity of sources are consistent with the hypothesis that the Grand Cayman anole, Anolis conspersus, is descended directly from Anolis grahami of Jamaica. Although the two species have remained morphologically similar, coloration in A. conspersus has changed considerably from that of its ancestor. The most dramatic difference is seen in dewlap colour, where A. conspersus has evolved a blue and highly UV-reflective dewlap from the ancestral orange-and-yellow colour state. In addition, variation in normal (non-metachrosis) dorsum coloration in A. grahami populations is limited to shades of green (olive, emerald, teal), whereas in A. conspersus dorsum coloration varies from green to blue and to brown. This increased colour variation occurs despite Grand Cayman being a small, relatively featureless island only 35 km in length. Results of this study suggest that ambient light differences associated with precipitation-related vegetation structure may have played an important role in the evolution of A. conspersus body colour variation. Evidence is presented to show how geological, ecological, and physiological factors could have interacted to select for a short wavelength-reflective dewlap from a long wavelength-reflective precursor following the colonization of Grand Cayman from Jamaica by A. grahami between 2 and 3 Mya.

Plasma Steroid-Binding Globulin Mediation of Differences in Stress Reactivity in Alternative Male Phenotypes in Tree Lizards, Urosaurus ornatus

Plasma steroid-binding globulins, for example, corticosteroid-binding globulin and sex hormone-binding globulin (SHBG), have been identified in a number of vertebrates. One possible function of these proteins is to regulate the amount of steroid delivery to target tissues, as only free steroids are believed to diffuse from the circulation to target cells. Male tree lizards, Urosaurus ornatus, exhibit alternative male reproductive tactics correlated with dewlap (throat-fan) coloration. Males with orange-blue dewlaps are aggressive and territorial, whereas males with orange dewlaps are less aggressive and employ a satellite strategy. The two types of males have similar basal levels of total plasma corticosterone and testosterone. However, testosterone levels of nonterritorial males are more sensitive than those of territorial males to negative regulation by stress-induced increases in corticosterone. We tested the hypothesis that this difference in corticosterone feedback on testosterone could be mediated, in part, by differences in binding globulin levels between the two types of males. We have identified two steroid-binding globulins in male tree lizards. The first binds androgens and estradiol with high affinity (10−9 M) and is similar to previously described sex hormone-binding globulins. The second binds both androgens and C21 steroids, such as progesterone and corticosterone, with higher specificity than estradiol and is best described as an androgen-glucocorticoid-binding globulin (AGBG). In both types of males, the capacity of AGBG is much higher than SHBG. In addition, AGBG capacity is significantly greater in territorial than nonterritorial males, whereas the capacity of SHBG does not differ between the two types of males. Calculations of free steroid levels based on the affinity and capacity measures suggest that although most testosterone circulates bound to binding globulins, binding capacity is high enough that binding globulins are also able to bind to other steroids such as corticosterone. Thus, differences in binding capacity between the two types of males could result in higher levels of free corticosterone in nonterritorial males than in territorial males, especially during stress-induced increases in corticosterone, and may explain why testosterone levels of nonterritorial males are more sensitive to negative feedback by corticosterone.