Dewlap Extension Research Articles

Meta-Analysis Reveals Behavioral Plasticity, Not Agonistic Behavior, Facilitates Invasion of Brown Anoles (Anolis sagrei) and Replacement of Green Anoles (Anolis carolinensis)

In a meta-analysis, we examined the behavioral portfolio of invasive brown anoles (Anolis sagrei) and native green anoles (Anolis carolinensis) in urban and non-urban environments. We hypothesized that invasive anoles would display more agonistic and bold signals (head bobbing, dewlap extensions, and pushups) than their native-range counterparts and their native competitors. We found that in urban settings, anoles of both species signaled more with dewlap extensions than with head bobs. Brown anoles displayed significantly more in non-urban habitats and their native range compared to urban habitats and invasive ranges. The outcome of our analysis suggests that brown anoles have plastic behavioral portfolios, whereas green anoles have relatively balanced preferences for head bobbing, irrespective of the habitat in which the populations were collected. We attribute the success of the brown anole invasion to the flexible strategy in the face of higher mate competition, higher predation risks, and less resource competition in both urban and invasive ranges. Lastly, we observed publication biases. More studies were conducted with urban and invasive brown anoles and specifically in manipulative mesocosm experimental settings—transplanting populations from native field settings. We show this altered the display rates across all studied signals.

Intersexual chemo-sensation in a "visually-oriented" lizard, Anolis sagrei.

While the conspicuous visual displays of anoles have been studied in great depth, the possibility that these lizards may also interact through chemical signalling has received hardly any consideration. In this study, we observed the behaviour of male brown anoles (Anolis sagrei) when introduced into an environment previously inhabited by female conspecifics, and compared it to when they were introduced into an untreated environment. The males in our tests exhibited significantly more elaborate display behaviour (i.e., greater number of dewlap extensions and head-nods) and a significantly greater number of tongue extrusions while in the cage formerly occupied by females than when placed in the untreated, control cage. The absolute numbers of tongue extrusions, however, were relatively low in comparison to average tongue-flick rates of ‘true’ chemically-oriented lizards. Our results strongly suggest that the males were capable of detecting chemical cues left behind by the females. These observations provide the first evidence of intersexual chemo-sensation in an anole lizard.

Messages conveyed by assorted facets of the dewlap, in both sexes of Anolis sagrei

Dewlaps of Anolis lizards are complex multicomponent signaling devices that have been intensively studied. Yet, the functions and multiple messages conveyed by the dewlap remain largely unknown. Here, we assess some aspects of sexual identity, individual quality, and social status that may be signaled by the dewlap in both sexes of Anolis sagrei. In addition, we investigate whether diverse facets of dewlap signaling provide additive information (redundant message hypothesis) or highlight different characteristics of the sender (multiple-message hypothesis). To do so, components of dewlap design (area, color, and pattern ratio) and use (dewlap extension frequency during intersexual context) were quantified and investigated for relationships with sexual identity (sex), individual quality (performance and health state measurements), and social status (mirror-motivated aggression). First, we found that body size together with relative dewlap area and color act as redundant messages in the advertisement of sexual identity. Second, we found that dewlap coloration in the center and edge region signals aspects of individual quality, specifically health state, but only in males. The dewlap center and edge acts primarily as redundant signals, at least for body condition and immune response. However, different color components irrespective of dewlap region convey nonredundant information about aspects of health state in males, supporting the multiple-message hypothesis. Surprisingly, dewlap use in A. sagrei males conveyed no information about the tested quality measurements nor about mirror-motivated aggression. Neither dewlap design nor use in females was related to any of these parameters. In contrast to males, correlations between components of dewlap design and use during intersexual interactions were found for females, suggesting important signaling functions of the female dewlap in a courtship context.

Display behaviour and dewlap colour as predictors of contest success in brown anoles

Many animals display visual signals in male contests for access to females and territories. These visual signals can be multimodal and stimulate different aspects of a signal receiver’s visual system. Over two summers, we tested whether aspects of behaviour and dewlap colour might function as signals that predict contest success when males compete for access to either mates or territories in male brown anole lizards. We found that behaviour (PC1, a correlated composite of head-bob, push-up, and dewlap extension frequency) and an aspect of dewlap colour (PC3, the relative amounts of ultraviolet, yellow, orange, and red of the dewlap margin) were retained in the minimum adequate model predicting contest success across years and social contexts. Winners showed significant differences in behaviour (winners displayed more) and dewlap margin PC3 (winners had lower PC3 scores) compared to contest losers. These findings suggest that display behaviour and dewlap colour might serve as signals indicating a male’s ability to win contests for access to females and territories. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 646–655. ADDITIONAL KEYWORDS: lizard.

Deterring predators, daunting opponents or drawing partners? Signaling rates across diverse contexts in the lizard Anolis sagrei

Although the visual display behavior in Anolis lizards has received ample attention, the function of dewlap extensions (DE), push-ups (PU), and head-nods (HN) in general, and in Anolis sagrei in particular, remains highly equivocal. Therefore, our primary goal was to quantify the display rates of these visual signal types (DE, PU, and HN) in a variety of contexts, using A. sagrei as study species. To our knowledge, this is the first study to test individuals of both sexes in a repeated-measures design across multiple contexts, including predator, non-predator and social interactions (mirror, male–male, male–female, female–male). We found that males have an overall higher signaling rate than females across all contexts. In addition, we found that lizards of both sexes exhibited higher display rates in the presence of conspecifics than when confronted with a predator or non-predator, suggesting that DE, PU, and HN function in intraspecific communication, not in predator deterrence. Whereas females did not significantly raise display rates in a consexual and heterosexual context with respect to subject-alone context, males did. The PU signal type only appears to play a major role for A. sagrei males during aggressive encounters. During heterosexual interactions, increased frequencies of all signal types suggest that DE, PU, and HN are essential for male courtship. Finally, we suggest that intersexual selection is probably a driving force for frequency-related dewlap use in both sexes. In contrast, pronounced intersexual differences were detected for PU and HN rates within a social context.

Immunocytochemical localization of cysteine‐rich beta‐proteins in the extensible epidermis of the dewlap in the lizard Anolis carolinensis

AbstractThe dewlap in the lizard Anolis carolinensis is made of scales separated by large interscale regions capable of broad stretching during fan extension. This indicates that the skin contains proteins that allow extension of interscale regions. The immunocytochemical analysis of the epidermis indicates that HgG5, a glycine‐rich hydrophobic beta‐protein poor in cysteine is localized only in the stiff beta‐layer of the outer scale surface, but is completely absent in mesos and alpha‐layers and in hinge regions. HgGC10, a cysteine‐medium‐rich beta‐protein is present in beta‐layers but especially in alpha‐layers of interscale epidermis that presents folds and lacks a beta‐layer. HgGC3 is weakly localized in the alpha‐layer, but is mainly found in hinge regions. HgGC8 and HgG13 are low to absent in the alpha‐ and beta‐layer. The immunolocalization of cysteine‐rich beta‐proteins such as HgGC10/3 in alpha‐layers and interscale epidermis suggests that these small proteins are involved in the formation of a corneous material compatible with dewlap extension. The basement membrane underneath scales is joined to bundles of collagen fibrils in the dermis through anchoring fibrils that likely determine flattening of the epidermis during the extension of the throat fan.

The biomechanical basis of evolutionary change in a territorial display

SummaryFew studies have examined how the anatomy of an animal signal contributes to, or limits, the evolution of signal differentiation among closely related species.InAnolislizards, adult males extend a large, conspicuous dewlap as part of a territorial advertisement display. Males of species from the island of Jamaica rely on the rapid extension of the dewlap to facilitate display detection by territorial neighbours and conspecific females. Males of other species on the island of Puerto Rico extend the dewlap at considerably slower speeds and instead rely on other strategies to maintain an effective display. What initially prompted this divergence in display between the islands is unknown, but evidence suggests that it may have something to do with the way the dewlap is extended during display.Our goal was to determine whether an innovation in the dewlap lever in Jamaican lineages, but absent in Puerto Rican lineages, accounted for the evolution of the high‐speed dewlap on Jamaica. We began by modelling the performance of theAnolisdewlap as a first‐order lever system. We then simulated changes to this system relating to its morphology, articulation and input force in biologically realistic ways to predict how such changes impact dewlap speed. Finally, we compared these predictions with data on the morphology of the dewlap lever system from museum specimens and actual dewlap speed recorded for lizards in the field.This investigation revealed that changes to the dewlap lever have affected the performance of the dewlap display in at least two ways. Within islands, structural changes to the hyoid morphology seem to have led to differences in dewlap speed among species. Between islands, however, differences in dewlap speed were most likely the result of a major increase in muscle contraction velocity that powers the dewlap extension in Jamaican species, but has not originated in species on Puerto Rico.Our study shows how the biomechanics of a social signal can have important implications for understanding why closely related species might differ in signal behaviour, despite apparent similarities in the selection pressures that act on the signal.

Convergent evolution in the territorial communication of a classic adaptive radiation: Caribbean Anolis lizards

To demonstrate adaptive convergent evolution, it must be shown that shared phenotypes have evolved independently in different lineages and that a credible selection pressure underlies adaptive evolution. There are a number of robust examples of adaptive convergence in morphology for which both these criteria have been met, but examples from animal behaviour have rarely been tested as rigorously. Adaptive convergence should be common in behaviour, especially behaviour used for communication, because the environment often shapes the evolution of signal design. In this study we report on the origins of a shared design of a territorial display among Anolis species of lizards from two island radiations in the Caribbean. These lizards perform an elaborate display that consists of a complex series of headbobs and dewlap extensions. The way in which these movements are incorporated into displays is generally species specific, but species on the islands of Jamaica and Puerto Rico also share fundamental aspects in display design, resulting in two general display types. We confirm these display types are convergent (the consequence of independent evolution on each island) and provide evidence that the convergence was driven by selection for enhanced signal efficiency. Our study shows how adaptation to common environmental variables can drive the evolution of adaptive, convergent signals in distantly related species.

Historical contingency and behavioural divergence in territorial Anolis lizards

The extent that evolution - including adaptation - is historically contingent (dependent on past events) has often been hotly debated, but is still poorly understood. In particular, there are little data on the degree that behaviour, an aspect of the phenotype that is strongly linked to contemporary environments (social or physical), retains the imprint of evolutionary history. In this study, I examined whether differences in the design of the territorial displays among species of Caribbean Anolis lizards reflect island-specific selection regimes, or historically contingent predispositions associated with different clade histories. Adult males advertise territory ownership using a series of headbobs and dewlap extensions, bouts of which vary in duration among species. When display durations were mapped onto the Anolis phylogeny, prominent differences between species belonging to the Western and Eastern Caribbean radiations were apparent. Statistical analyses confirmed that species differences in the duration of headbob displays, and to some extent the duration of dewlap extensions, were historically contingent. The unique evolutionary histories of each clade have seemingly had a profound effect on the subsequent direction of display evolution among descendent taxa. These results combined with those from previous studies on these lizards show that past history can have an important impact on the type of behaviour exhibited by species today, to the point that adaptive evolution can proceed quite differently in lineages originating from different evolutionary starting points.

Assessing display variability in wild brown anoles Anolis sagrei using a mechanical lizard model

Abstract Signals used for species identity ought to be highly stereotyped so as to facilitate immediate recognition by con-specifics. It is surprising therefore to find variability in putative species signature displays. The brown anole Anolis sagrei has a high degree of variability in its signature bobbing display. In this study we collected descriptive data on variability in the temporal structure of wild brown anole bobbing patterns, finding that no two displays analyzed had the same temporal structure, and we also tested whether wild brown anoles prefer the signature display over an alternate display pattern by using mechanical robot playbacks in the field. As a response metric we assessed whether or not the lizards showed social responses (pushup, dewlap extension, or head-nod) in response to the robotic presentations. We found that the lizards responded slightly more to the signature than to the alternate pattern, providing support for the idea that despite the variability seen in displays, the signature pattern is meaningful to them. We tested two other independent variables: speed of the display and elevation of the robot during its display, neither of which was significant. Dewlap extensions were given predominantly by adult males and were more likely to be given in the breeding season than the nonbreeding season. Pushups and head-nods were given equally by males and a combined class of females and juveniles, and were not seasonal. Head-nods increased after the robot turned off, suggesting that they may be used in a conversational turn-taking style during communication.

Communication Signal Rates Predict Interaction Outcome in the Brown Anole Lizard, Anolis sagrei

Communication signals often function in multiple contexts such as territory defense, mate attraction, and predator deterrence. If signals indicate the quality of the signaler, then high rates of signal use may be associated with successful outcomes across multiple contexts. Here, I examined the relationship between signal use and interaction outcome during territorial defense and courtship bouts in field populations of the Brown Anole lizard, Anolis sagrei, in the middle of their breeding season. High bobbing rates, which are associated with high endurance in males of other lizard species, predicted both successful territorial defense and courtship bouts that resulted in copulation, while high rates of nodding, a signal typically associated with subordinate behavior during agonistic encounters, predicted unsuccessful outcomes in both contexts. Males performed dewlap extensions to females at a higher rate than to other males, independently of interaction outcome. In interactions with females, dewlap extens...

Behavioural display systems across nine Anolis lizard species: sexual dimorphisms in structure and function

Relationships between structure and function are a primary focus in biology, yet they are most often considered within individual species. Sexually dimorphic communication behaviours and the morphology of associated structures can vary widely, even among closely related species, and these traits provide an ideal opportunity to investigate the evolution of structure-function patterns. Using nine Anolis lizard species, we addressed a series of questions regarding sex differences in and the evolution of relationships between extension of the throat fan (dewlap) and morphology of the muscles and cartilage controlling it. The main results indicated that within species, males displayed the dewlap more often than females and consistently exhibited larger associated structures. These data are consistent with work in other vertebrates in which corresponding sex differences in reproductive morphology and behaviour have been documented. Across species, however, we found no evidence that the rate of dewlap extension evolved in association with dewlap morphology. Thus, we provide an example of traits that, when considered in a phylogenetic framework, exhibited limited associations between behaviour and morphology, perhaps as the result of constraints imposed by the ecological contexts in which different species occur.

Changes in the Intensity of Male Courtship Behavior Following Physical Exposure of Males to Previously Unfamiliar Females in Brown Anoles (Anolis Sagrei)

Male Brown Anoles (Anolis sagrei) have been found in laboratory studies to court unfamiliar females more intensely than familiar females and in choice tests to preferentially court and mate with unfamiliar females. The objective of the present study was to determine how the intensity of male courtship behavior changes following physical exposure of males to previously unfamiliar females. The courtship behavior of males was recorded in 30-min courtship tests with familiar females (pretest), with unfamiliar females (first test), and with previously unfamiliar females after males had been physically exposed to them for two days (retest). When males were first visually exposed to unfamiliar females in the first test, they courted them significantly more intensely than they had courted familiar females in the pretest. Specifically, males gave more bobbing displays with dewlap extensions and spent more time adjacent to the stimulus female in courtship tests with unfamiliar females than in tests with familiar females. However, when males were housed with previously unfamiliar females for two days and then visually exposed to them in the retest, they did not court them significantly differently than they had courted familiar females. These results suggest that the heightened courtship response of males to unfamiliar females disappears relatively quickly after males have had physical exposure to females.

Not All Signals are Equal: Male Brown Anole Lizards (Anolis sagrei) Selectively Decrease Pushup Frequency Following a Simulated Predatory Attack

AbstractThe use of conspicuous communication signals often increases a signaler's risk of predation. Many species communicate with a repertoire of signals that may differ in their conspicuousness to predators. Few studies have examined the ability of prey to selectively decrease the use of individual signals in their displays under heightened predation risk. Here, I examined the behavior of male brown anole lizards (Anolis sagrei) in response to a simulated predatory attack from a model kestrel. This species communicates with three major visual signal types, the head‐bob, pushup, and dewlap extension, which vary in their motion and spectral characteristics. I predicted that lizards would decrease frequencies of the dewlap extension and pushup following the attack, but not the head‐bob. Males modulated their use of individual signals by decreasing pushup rates, but not head‐bob rates. Decreases in dewlap frequency were marginally significant. One explanation for these results is that lizards decrease frequencies of signal types based partly on their conspicuousness. The energetic cost of each signal type may be an equally important factor that determines the signaler's response to predators, particularly if a predatory attack is perceived as imminent.

Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles ( Anolis carolinensis)

Male green anole lizards court females using a red throat fan (dewlap) and copulate by intromitting one of two penises (hemipenes). These structures begin sexually monomorphic, but by adulthood males have larger dewlaps, only males have hemipenes, and many of the neuromuscular components of both systems show male-biased dimorphisms. We hypothesized that testosterone (T), which increases in juvenile males but not females about a month after hatching, facilitates masculinization. To test this idea, on post-hatching day 30, gonadally intact females received either a blank or T implant, and males were either castrated or sham-castrated. At day 90, juveniles were euthanized and the length of the cartilage and cross-sectional areas of the muscle fibers and motoneurons required for dewlap extension were examined. We also measured the cross-sectional areas of the hemipenes and associated muscle fibers and motoneurons, and counted the motoneurons. T-treated females had longer cartilages and larger dewlap muscle fibers compared to those with blank implants. No effects on motoneurons were detected, and no females possessed hemipenes or associated musculature. In males, castration produced shorter dewlap cartilages and smaller hemipenes; other measures were not affected by treatment. These data indicate that components of the dewlap system differentiate relatively late in development, that T likely mediates the process, and that although components of the copulatory system are plastic in juvenile males, sexual differentiation of peripheral features is complete before day 30. The data also suggest that target structures (dewlap cartilage and hemipenes), compared to their neuromuscular effectors, are particularly sensitive to developmental T exposure.

Laboratory and Field Test of the Functional Significance of the Male's Dewlap in the Lizard Anolis sagrei

Abstract The extension and retraction of the throat fan or dewlap is one of the most conspicuous aspects of the display behavior of male Anolis lizards. We explored aspects of the functional significance of displaying the male's dewlap by surgically preventing male brown anoles (Anolis sagrei) from extending their dewlaps and comparing their behavior with controls that could extend their dewlaps. In 30-min laboratory contests, we compared the display behavior of untreated males paired with either experimental males or with sham-treated control males. In a subsequent field study, we tested what effect displaying the dewlap has on male residence time (days males remained at a site), visibility (number of sightings of males), maximum distance moved (from site of release), home range size, and body size during 18 censuses over a 47-day period. Untreated males paired with the two types of stimulus males in the laboratory study did not differ significantly in latency to display, number of dewlap extensions, num...

Seasonal and Sexual Dimorphisms in the Green Anole Forebrain

During the breeding season, male green anole lizards extend a throat fan (dewlap) in courtship. This behavior is facilitated by testosterone (T). Females extend a much smaller dewlap less often, even with the same dose of T. During the nonbreeding season when T is low, dewlap extension is reduced. To determine if parallels exist between structure and function, we investigated neuron soma size and density in the preoptic area (POA) and ventromedial nucleus of the amygdala (AMY), which are involved in the display behavior, in breeding and nonbreeding males and females. Cells from breeding animals were larger than cells from nonbreeding animals, but they were not sexually dimorphic. No significant effects existed in neuron density. This experiment indicates that portions of the anole forebrain important for sexual behavior are plastic and might be influenced by seasonal changes in steroid hormones. To investigate whether T can reverse the seasonal difference in soma size in both sexes, gonadectomized nonbreeding anoles were implanted with an empty or T propionate-filled capsule; animals were also tested for male-typical courtship behavior. Males and females treated with T had higher rates of dewlap extension, but across treatment groups these rates were greater in males. Neuron soma size in the POA and AMY was larger in males than females, but no effects of treatment were detected. Taken together, the results indicate that T can stimulate behavior in the nonbreeding season and suggest that a dissociation exists between the regulation of the courtship display and soma size of relevant brain regions.

Effects of Testosterone Treatment and Season on the Frequency of Dewlap Extensions during Male–Male Interactions in the Lizard Anolis sagrei

Lizards of the genus Anolis extend and retract a large and often brightly colored throat fan called a dewlap. The dewlap in most anoles is a sexually dimorphic structure. It is larger in males than females and males use the dewlap more frequently and in more contexts than do females. In the present study we investigated whether plasma testosterone (T) levels and season affect the frequency of dewlap use in male–male interactions in the brown anole, Anolis sagrei. We manipulated plasma T levels by implanting adult, castrated males with pellets that delivered no T, a moderate dose of T, or a high dose of T. In tests with stimulus males, castrated males that were treated with a moderate or with a high dose of T had a significantly higher frequency of dewlap extensions than did castrated males that received no T. However, the frequency of dewlap extensions in castrated males that received the high dose of T did not differ significantly from castrated males that received the moderate dose of T or from noncastrated control males. Males captured during the breeding season and tested in the laboratory had a significantly higher frequency of dewlap extensions than did males captured in the postbreeding season and tested in the same manner. These results suggest that plasma T levels affect how frequently males of A. sagrei extend their dewlaps in male–male interactions and that seasonal changes in male dewlap use may be due to seasonal differences in plasma T levels.

Sexual dimorphism in neuromuscular junction size on a muscle used in courtship by green anole lizards

The green anole lizard exhibits seasonal courtship behavior that is sexually dimorphic. This courtship consists of the extension of a bright red throat fan (dewlap) associated with head-bobbing display behavior. While males extend their dewlaps in aggressive encounters as well as in courtship, females use their considerably smaller dewlaps much less frequently and mainly in agonistic encounters. In parallel, a number of components of the neuromuscular system controlling dewlap extension are greater in males than in females during the breeding season, including dewlap motoneuron soma size and muscle fiber size and number. These features do not seem to change substantially in adulthood, despite a dramatic decline in dewlap use during the nonbreeding season. We explored the morphology of this neuromuscular system in more detail in the present experiment in males and females during both the breeding and nonbreeding seasons. Fiber and whole muscle length (approximately perpendicular to the fibers) were measured. Acetylcholinesterase histochemistry was used to visualize neuromuscular junctions (NMJs), and the surface area and density of NMJs were assessed for each animal. During the breeding season, NMJ size was larger in males than in females, but NMJ density along each fiber was equivalent between the sexes. In addition, whole muscle length and that of individual muscle fibers, was larger in males than in females. However, when corrected for body size, the sex difference in muscle fiber length disappeared. In the nonbreeding season, the sexual dimorphisms were maintained, suggesting that these features do not change substantially due to differences in circulating testosterone or a difference in use across seasons. Overall, these results are consistent with the idea that enhanced NMJ size is a relatively stable feature of the dewlap muscle in adulthood that either facilitates or is a consequence of using a larger muscle to extend a bigger dewlap in males compared to females.

Development of a Sexually Dimorphic Neuromuscular System Involved in Green Anole Courtship Behavior

During courtship and aggression, adult male green anoles (Anolis carolinensis) extend a large red throat fan called a dewlap. Adult females have a very small dewlap; they rarely use it during agonistic encounters and never during courtship. The motoneurons, nerve, muscle fibers, neuromuscular junctions, and cartilage pieces responsible for dewlap extension are all larger in adult males than females, parallel to the behavioral dimorphisms. However, the general developmental pattern of these structures, and when they become sexually dimorphic, was largely unknown. In the present study, we examined the length of the 2nd ceratobranchial cartilages (which unfold the dewlap), muscle fiber size, nerve cross-sectional area, and motoneuron soma size, as well as measures of body size (snout-vent length and body weight) at post-hatching days 1, 30, 60, 75, and 90. All measures other than motoneuron soma size increased over time. However, only cartilage length and muscle fiber size became sexually dimorphic in the first three months after hatching. The cartilage was greater in males than females by d60, and muscle fiber size differentiated by d75. The results indicate that peripheral structures involved in dewlap extension differentiate prior to those in the brain and thus, because males and females in this age range are identical in size, dewlap (cartilage) size could be a relatively specific factor contributing to the sexual differentiation of the rest of the neuromuscular system.