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.     

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.     

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.     

Differences in visual signal design and detectability between allopatric populations of anolis lizards

We tested the prediction of the sensory drive hypothesis using four allopatric populations of the lizard Anolis cristatellus from two distinct environments (i.e., mesic and xeric conditions). For each population, we measured habitat light characteristics and quantified signal design by measuring the spectral and total reflectance and transmittance of the dewlap. We used these data to calculate dewlap detectability using an empirically based model of signal detection probability. We found that populations from mesic and xeric conditions occupy two distinct habitats with respect to light intensity and spectral quality and that dewlap design has diverged between populations in a way that increases signal detectability in each habitat. The major difference in dewlap design was in total reflectance and transmittance, making dewlaps from xeric habitats darker and dewlaps from mesic habitats brighter. Furthermore, dewlap detection decreased significantly when a dewlap from a xeric habitat is detected under the spectral conditions of a mesic habitat. The converse is true for a dewlap from a mesic habitat. We propose that sensory drive has promoted divergence in dewlap design in distinct habitat light conditions, and we discuss the possibility that selection might promote early stages of reproductive isolation as a by-product of selection on dewlap design to distinct habitat light conditions.     

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.     

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards

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 40 years 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.     

Does breeding season variation affect evolution of a sexual signaling trait in a tropical lizard clade?

Sexually selected traits can be expected to increase in importance when the period of sexual behavior is constrained, such as in seasonally restricted breeders. Anolis lizard male dewlaps are classic examples of multifaceted signaling traits, with demonstrated intraspecific reproductive function reflected in courtship behavior. Fitch and Hillis found a correlation between dewlap size and seasonality in mainland Anolis using traditional statistical methods and suggested that seasonally restricted breeding seasons enhanced the differentiation of this signaling trait. Here, we present two tests of the Fitch–Hillis Hypothesis using new phylogenetic and morphological data sets for 44 species of Mexican Anolis. A significant relationship between dewlap size and seasonality is evident in phylogenetically uncorrected analyses but erodes once phylogeny is accounted for. This loss of strong statistical support for a relationship between a key aspect of dewlap morphology and seasonality also occurs within a species complex (A. sericeus group) that inhabits seasonal and aseasonal environments. Our results fail to support seasonality as a strong driver of evolution of Anolis dewlap size. We discuss the implications of our results and the difficulty of disentangling the strength of single mechanisms on trait evolution when multiple selection pressures are likely at play.     

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.     

Species Recognition, Dewlap Function and Faunal Size

Although having a number of functions in reproductive, territorialand aggressive behavior, Anolis dewlaps are only one means ofintraspecific signaling and they are always present in smallanole faunas (e.g., those of one or two species islands) buthere, in contrast to the situation in large faunas, their colorand pattern appear usually very similar and appear to be unimportantfor species (or population) recognition. The latter functionis then performed by such characteristics as adult size andbody color and pattern. Where, however, numerous species abutor overlap, dewlap color and pattern tend to be diverse anddiagnostic (particularly between overlapping forms). Even here,however, adult size, body shape and body color often redundantlyreinforce the species and population recognition function ofeven marked dewlap difference. In certain cases in complex faunas,size and/or body pattern substitute for the species recognitionfunction of reduced or absent dewlaps.     

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.     

Evolution of the ungulate dewlap: thermoregulation rather than sexual selection or predator deterrence?

Background

Dewlaps are iconic features of several ungulate species and, although a role in signalling has been postulated, their function remains largely unexplored. We recently failed to find any age-independent link between dewlap size and social status in the common eland (Tragelaphus oryx), pointing to the possibility that sexual selection may not be the primary cause of dewlap evolution in ungulates. Here I use a two-pronged approach to test hypotheses on the function of ungulate dewlaps: an interspecific comparative analysis of bovids and deer, and an intraspecific study of eland antelopes in the wild.

Results

Across species, the presence of dewlaps in males was not found to be associated with sexual size dimorphism, a commonly used measure of the intensity of sexual selection. The presence of dewlaps was, however, linked to very large male body size (>400 kg), which agrees with a thermoregulatory function as lower surface/volume-ratio counteracts heat dissipation in large-bodied species. In eland antelopes, large dewlap size was associated with higher, rather than lower, incidence of claw-marks (independently of age), a result which speaks against the dewlap as a predator deterrent and rather indicates a predation cost of the structure.

Conclusion

The findings suggest that, although an additional function in communication should not be ruled out, the dewlap of ungulates may contrast with that of lizards and birds in thermoregulation being a primary function.

     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae)

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full‐sibling, split‐family rearing design to estimate genetic correlations (r_G) between fecundity and signal traits, and compared those relationships against population‐level mate preferences for the signal traits. Animal model estimates for r_G between female fecundity and male signal traits overlapped zero—rejecting the hypothesis—but could reflect sample size limitations. The magnitude of r_G correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population‐level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high‐performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.     

Ornament size and colour as alternative strategies for effective communication in gliding lizards

Sexual ornamentation needs to be conspicuous to be effective in attracting potential mates and defending territories and indeed, a multitude of ways exists to achieve this. Two principal mechanisms for increasing conspicuousness are to increase the ornament's colour or brightness contrast against the background and to increase the size of the ornament. We assessed the relationship between the colour and size of the dewlap, a large extendible throat‐fan, across a range of species of gliding lizards (Agamidae; genus Draco) from Malaysia and the Philippines. We found a negative relationship across species between colour contrast against the background and dewlap size in males, but not in females, suggesting that males of different species use increasing colour contrast and dewlap size as alternative strategies for effective communication. Male dewlap size also increases with increasing sexual size dimorphism, and dewlap colour and brightness contrast increase with increasing sexual dichromatism in colour and brightness, respectively, suggesting that sexual selection may act on both dewlap size and colour. We further found evidence that relative predation intensity, as measured from predator attacks on models placed in the field, may play a role in the choice of strategy (high chromatic contrast or large dewlap area) a species employs. More broadly, these results highlight that each component in a signal (such as colour or size) may be influenced by different selection pressures and that by assessing components individually, we can gain a greater understanding of the evolution of signal diversity.     

Conserved visual sensitivities across divergent lizard lineages that differ in an ultraviolet sexual signal

The sensory drive hypothesis predicts the correlated evolution of signaling traits and sensory perception in differing environments. For visual signals, adaptive divergence in both color signals and visual sensitivities between populations may contribute to reproductive isolation and promote speciation, but this has rarely been tested or shown in terrestrial species. We tested whether opsin protein expression differs between divergent lineages of the tawny dragon (Ctenophorus decresii) that differ in the presence/absence of an ultraviolet sexual signal. We measured the expression of four retinal cone opsin genes (SWS1, SWS2, RH2, and LWS) using droplet digital PCR. We show that gene expression between lineages does not differ significantly, including the UV wavelength sensitive SWS1. We discuss these results in the context of mounting evidence that visual sensitivities are highly conserved in terrestrial systems. Multiple competing requirements may constrain divergence of visual sensitivities in response to sexual signals. Instead, signal contrast could be increased via alternative mechanisms, such as background selection. Our results contribute to a growing understanding of the roles of visual ecology, phylogeny, and behavior on visual system evolution in reptiles.     

COLOR PATTERN EVOLUTION,ASSORTATIVE MATING,AND GENETIC DIFFERENTIATION IN BRIGHTLY COLORED BUTTERFLYFISHES (CHAETODONTIDAE)

In butterflyfishes (Chaetodontidae), color pattern evolves rapidly and is often the only morphological trait separating closely related species. Vivid coloration is frequently assumed to provide critical signals for mate recognition and mate choice, but few direct experimental tests are available. Here we analyze the relationship between color pattern change, mate choice, and genetic differentiation in a group of three very closely related allopatric butterflyfishes. We found that in only one member of this group, Chaetodon multicinctus, is color pattern evolution associated with mate preference and genetic divergence. For its two sister species, C. punctatofasciatus and C. pelewensis, color pattern change has not resulted in assortative mating (based on laboratory pairing experiments and field observations) or in significant mtDNA or allozyme differentiation. In a contact zone on reefs in the Solomon Islands and Papua New Guinea, hybridization between the two forms has nearly homogenized color pattern differences. Outside these areas, however, color pattern remains distinct. Genetic variation is homogeneous over a much larger geographic scale. Sequence variation in the tRNA-proline end of the mitochondrial control region and allozyme variation was distributed widely within C. punctatofasciatus and C. pelewensis, which suggests few constraints to mitochondrial or nuclear gene flow across the color pattern boundary. These contrasting patterns strongly suggest that selection is maintaining color pattern differences in allopatry in the face of potentially homogenizing levels of gene flow. The mating pattern data show that this selection is not operating on mate recognition in the strictest sense, but probably on some other aspect of the social system of these territorial fish. In this case, divergence in mating preference can follow color pattern evolution, but is not contemporaneous with it.     

SIGNAL DESIGN AND PERCEPTION IN HYPOCNEMIS ANTBIRDS: EVIDENCE FOR CONVERGENT EVOLUTION VIA SOCIAL SELECTION

Natural selection is known to produce convergent phenotypes through mimicry or ecological adaptation. It has also been proposed that social selection—i.e., selection exerted by social competition—may drive convergent evolution in signals mediating interspecific communication, yet this idea remains controversial. Here, we use color spectrophotometry, acoustic analyses, and playback experiments to assess the hypothesis of adaptive signal convergence in two competing nonsister taxa, Hypocnemis peruviana and H. subflava (Aves: Thamnophilidae). We show that the structure of territorial songs in males overlaps in sympatry, with some evidence of convergent character displacement. Conversely, nonterritorial vocal and visual signals in males are strikingly diagnostic, in line with 6.8% divergence in mtDNA sequences. The same pattern of variation applies to females. Finally, we show that songs in both sexes elicit strong territorial responses within and between species, whereas songs of a third, allopatric and more closely related species (H. striata) are structurally divergent and elicit weaker responses. Taken together, our results provide compelling evidence that social selection can act across species boundaries to drive convergent or parallel evolution in taxa competing for space and resources.     

Are morphology–performance relationships invariant across different seasons? A test with the green anole lizard (Anolis carolinensis)

A key assumption in ecomorphological studies is that morphology–function relationships are invariant due to underlying biomechanical principles. We tested the hypothesis that morphology–performance relationships are invariant across different seasons by examining how a key performance trait, bite force, and two aspects of morphology (head shape and dewlap size) changed seasonally in the field and in the laboratory in the green anole lizard Anolis carolinensis . We found that not only did bite force change seasonally (up to 80% within the same individual), but relationships between morphology and bite force are highly plastic. Of the three traits examined (bite force, head shape, and dewlap area), only head shape did not change seasonally. We noted opposing trends for how bite force and dewlap area changed seasonally; whereas dewlap areas were large in the spring, and small in the winter, bite forces were low in the spring and high in the winter. This pattern occurred because of a tradeoff at the individual level: individuals in the spring with large dewlaps and high bite forces diminish their dewlaps (but not bite force), whereas individuals with small dewlaps and low bite forces in the spring increase their bite forces (but not dewlap size). We also show that this trend was apparent both in the field (comparing different individuals) and the laboratory (comparing the same set of individuals under standardized conditions). Finally, seasonal changes were not consistent among individuals for either bite force or dewlap area, as individuals changed seasonally in proportion to their initial state. These findings cast doubt on the widely held view of invariant morphology–performance relationships, and offer a cautionary note for eco-morphological studies.     

SEXUAL SELECTION CAN INCREASE THE EFFECT OF RANDOM GENETIC DRIFT—A QUANTITATIVE GENETIC MODEL OF POLYMORPHISM IN OOPHAGA PUMILIO,THE STRAWBERRY POISON‐DART FROG

The variation in color pattern between populations of the poison‐dart frog Oophaga pumilio across the Bocas del Toro archipelago in Panama is suggested to be due to sexual selection, as two other nonsexually selecting Dendrobatid species found in the same habitat and range do not exhibit this variation. We theoretically test this assertion using a quantitative genetic sexual selection model incorporating aposematic coloration and random drift. We find that sexual selection could cause the observed variation via a novel process we call “coupled drift.” Within our model, for certain parameter values, sexual selection forces frog color to closely follow the evolution of female preference. Any between‐population variation in preference due to genetic drift is passed on to color. If female preference in O. pumilio is strongly affected by drift, whereas color in the nonsexually selecting Dendrobatid species is not, coupled drift will cause increased between‐population phenotypic variation. However, with different parameter values, coupled drift will result in between‐population variation in color being suppressed compared to its neutral value, or in little or no effect. We suggest that coupled drift is a novel theoretical process that could have a role linking sexual selection with speciation both in O. pumilio, and perhaps more generally.     

Quantitative traits and mode of speciation in Martinique anoles

We investigate extensive quantitative trait variation (dewlap hue, colour pattern, dorsum hue, body proportions and scalation) in the Martinique anole across eight transects representing nascent parapatric ecological speciation, nascent allopatric speciation and allopatric divergence without sufficient genetic structure to suggest speciation. Quantitative trait divergence can be extremely large between adjacent sets of populations, but with one exception that this is associated with difference in habitat rather than past allopatry. Nascent ecological speciation shows the greatest level of quantitative trait divergence across all character sets including those implicated in natural, as well as sexual selection. The sole example of nascent allopatric speciation is associated with fairly strong quantitative trait divergence among most character sets, but not the set most implicated in natural (rather than sexual) selection. The role of sexual selection in ecological speciation is discussed, both in terms of female choice with assortative mating and male–male competition with condition‐dependant sexual signals.