Throat Coloration Research Articles

Revealing the Biochemical and Genetic Basis of Color Variation in a Polymorphic Lizard.

Determining the mechanistic and genetic basis of animal coloration is essential to understand the costs and constraints on color production, and the evolution and maintenance of phenotypic variation. However, genes underlying structural color and widespread pigment classes apart from melanin remain largely uncharacterized, in part due to restricted taxonomic focus. We combined liquid chromatography-mass spectrometry and RNA-seq gene expression analyses to characterize the pigments and genes associated with skin color in the polymorphic lizard, Ctenophorus decresii. Throat coloration in male C. decresii may be a combination of orange, yellow, grey, or ultra-violet blue. We confirmed the presence of two biochemically different pigment classes, pteridines (self-synthesized) and carotenoids (acquired through the diet), in all skin colors. Orange skin had the highest levels of pteridine pigments while yellow skin tended to have higher levels of carotenoids, of which the vitamin A precursors β-carotene and β-cryptoxanthin have not been previously confirmed in reptiles. These results were confirmed by gene expression analyses, which detected 489 genes differentially expressed between the skin colors, including genes associated with pteridine production, provitamin A carotenoid metabolism, iridophore-specific synthesis, melanin synthesis, and steroid hormone pathways. For the majority of these 489 genes, however, our study reveals a new association with color production in vertebrates. These data represent a significant contribution to understanding the genetic basis of color variation in vertebrates and a rich resource for further studies.

A genetic approach to the rock-paper-scissors game

Polymorphisms are usually associated with defenses and mating strategies, affecting the individual's fitness. Coexistence of different morphs is, therefore, not expected, since the fittest morph should outcompete the others. Nevertheless, coexistence is observed in many natural systems. For instance, males of the side-blotched lizards (Uta stansburiana) present three morphs with throat colors orange, yellow and blue, which are associated with mating strategies and territorial behavior. The three male morphs compete for females in a system that is well described by the rock-paper-scissors dynamics of game theory. Previous studies have modeled the lizards as hermaphroditic populations whose individual's behavior were determined only by their phenotypes. Here we consider an extension of this dynamical system where diploidy and sexual reproduction are explicitly taken into account. Similarly to the lizards we represent the genetic system by a single locus with three alleles, o, y, and b in a diploid chromosome with dominance of o over y and of y over b. We show that this genotypic description of the dynamics results in the same equilibrium phenotype frequencies as the phenotypic models, but affects the stability of the system, changing the parameter region where coexistence of the three morphs is possible in a rock-paper-scissors game.

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Negative interplay of tail and throat ornaments at pair formation in male barn swallows

Pair formation is indispensable for breeding in monogamous species, generating selection for male traits that increase the probability of pairing success. Male ornamentation is one such trait, and several empirical studies have shown the importance of each of multiple ornaments. Still, it remains unclear how multiple ornaments in combination affect the probability of pair formation. Using the Japanese barn swallow, Hirundo rustica gutturalis, we studied the interplay of two sexually selected male traits, tail length and throat coloration, during pair formation. Independent of other morphological, ornamental and abiotic variables, the probability of pair formation was predicted by the negative interplay between tail length and plumage colour saturation: males possessing more-colourful plumage with shorter tails or males possessing less-colourful plumage with longer tails had a higher probability of pair formation than others. The current findings may explain spatiotemporal variation in ornamentation and sexual selection in this model species.

Relationships of morphological groups in the northern flicker superspecies complex (Colaptes auratus & C. chrysoides)

Many species complexes have diversified rapidly and recently, resulting in morphologically diverse populations; however, the rapid pace of diversification often prevents identification of clear phylogeographic structure. Recently, the use of large genomic and reduced-representation genomic datasets has improved resolution of the evolutionary histories in such species and allowed identification of lineages on distinct evolutionary trajectories. The northern flicker (Colaptes auratus) and gilded flicker (Colaptes chrysoides) form a polytypic superspecies group with a complex taxonomic history. The superspecies group includes up to 13 described subspecies, which represent slight geographic variation among five main morphological groups: red-shafted flickers of western North America (cafer group), yellow-shafted flickers of eastern North America (auratus group), Cuban flickers of the Caribbean (chrysocaulosus group), gilded flickers of the U.S. south-west and Mexican north-west (chrysoides group), and Guatemalan flickers of Central America (mexicanoides group). These groups are largely differentiable by variation in feather shaft colour, malar colour, throat colour, crown colour, and back barring. Here, using mitochondrial DNA (mtDNA) and hundreds of single nucleotide polymorphisms (SNPs), we characterized the genetic relationships and genomic distinctiveness of the five morphological groups. We found the mexicanoides group to be the most genetically distinct in both mtDNA (∼1.4% sequence divergence) and large SNP panels. The chrysocaulosus group is differentiated by a single basepair mutation in a small mtDNA fragment. In both mtDNA and SNP panels, there is little genetic distinctiveness between auratus, cafer, and chrysoides morphological groups, with evidence of admixture and a lack of fixed differences.

Reproductive advantages of multiple female ornaments in the Asian Barn Swallow Hirundo rustica gutturalis

Recent research has increasingly focused on female ornamentation, with several studies having investigated female ornaments in relation to reproduction. However, most previous studies have focused on single female ornaments, while females of numerous species, particularly birds, possess multiple ornaments. It is still unclear whether multiple female ornaments are linked to reproductive performance, though this information is crucial for understanding how these ornaments have been maintained. In this study, we examined the signaling function of multiple female ornaments in the Asian Barn Swallow Hirundo rustica gutturalis in Japan. First, females with previous breeding experience in the study population had longer tails and more colorful throat patches than other females. This indicates that these ornaments can provide information about the breeding experience of females to conspecifics. In contrast to males, the size of white tail spots was not significantly related to breeding experience in females, partly because females with larger white spots were less likely to return to breed after a failed clutch. Second, females with longer tails and more colorful throats started breeding earlier than others, even after controlling for confounding factors, and they paired with attractive males (thereby obtaining their direct and indirect benefits too), suggesting a mating advantage for females with such ornaments. In addition, males paired with long-tailed females invested more in paternal care. These observed patterns differed from those of males, for whom the throat coloration and the size of white tail spots, rather than tail length, were significant predictors. In fact, a sex-combined analysis of breeding date demonstrated significant interactions of sex in relation to tail length and the size of white tail spots, indicating differential selection between the sexes. Our data suggest that selection on females may facilitate the evolution and maintenance of some female ornaments, partially independently of male ornaments.

The genetic basis of discrete and quantitative colour variation in the polymorphic lizard, Ctenophorus decresii.

BackgroundColour polymorphic species provide invaluable insight into processes that generate and maintain intra-specific variation. Despite an increasing understanding of the genetic basis of discrete morphs, sources of colour variation within morphs remain poorly understood. Here we use the polymorphic tawny dragon lizard Ctenophorus decresii to test simple Mendelian models for the inheritance of discrete morphs, and to investigate the genetic basis of continuous variation among individuals across morphs. Males of this species express either orange, yellow, orange surrounded by yellow, or grey throats. Although four discrete morphs are recognised, the extent of orange and yellow varies greatly. We artificially elevated testosterone in F0 females and F1 juveniles to induce them to express the male throat colour polymorphism, and quantified colour variation across the pedigree.ResultsInheritance of discrete morphs in C. decresii best fit a model whereby two autosomal loci with complete dominance respectively determine the presence of orange and yellow. However, a single locus model with three co-dominant alleles for orange, yellow and grey could not be definitively rejected. Additionally, quantitative expression of the proportion of orange and yellow on the throat was strongly heritable (orange: h2 = 0.84 ± 0.14; yellow: h2 = 0.67 ± 0.19), with some evidence for covariance between the two.ConclusionsOur study supports the theoretical prediction that polymorphism should be governed by few genes of major effect, but implies broader genetic influence on variation in constituent morph traits.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0757-2) contains supplementary material, which is available to authorized users.

Structural- and carotenoid-based throat colour patches in males of Lacerta schreiberi reflect different parasitic diseases

Host species in populations under strong pressures from parasitic diseases may evolve ornaments to signal individual host quality to conspecifics. Colour ornaments in lizards result from the interaction of different layers in the skin. When inner layers of melanin and well-arranged iridophores are combined, UV-blue structural colouration results. On the other hand, when layers of erythrophores are densely loaded with carotenoids, a UV-yellow colouration is seen. The expression of carotenoid-based traits has been frequently studied in relation to parasite infections. However, few studies have explored the relationship between parasitic diseases and structural colouration. In this study, we investigated the expression of UV-blue and UV-yellow throat colour patches in males of Lacerta schreiberi in relation to infection by haemoparasites, ixodid ticks and intestinal nematodes. The brightness of the UV-yellow throat patch (a carotenoid-based ornament) was positively correlated with body condition and negatively correlated with the number of attached ticks, supporting Hamilton and Zuk’s hypothesis. Additionally, individuals that passed nematode eggs in the faeces had UV-yellow throat patches with higher hue values (more greenish colouration). Strikingly, the individuals infected by haemoparasites of the genus Schellackia showed UV-blue throat patches (a melanin-based ornament) with higher values of both UV-blue chroma and hue (i.e., UV-biased throats) than did uninfected individuals, suggesting a key role for melanin in the nuptial colouration of this lizard species. Thus, the combined information from both UV-blue and UV-yellow throat patches may convey integrative information about individual quality in this lacertid species.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour.

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment-dependent sexual selection has played an important role. Here, we describe a very young (~90years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment-dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Female Attraction to Higher Pitched Male Enticement Calls in Barn Swallows

AbstractCurrent sexual selection studies demonstrate that female mate preference almost always favors exaggerated male traits, such as colorful plumage and elongated tails. However, such studies focused mainly on secondary sexual characteristics, i.e., traits that are fully developed at maturation, while ignoring others, which precludes generalization of the findings. We studied the expression of the male enticement call, a nestling‐like courtship trait, in relation to female attraction and to the expression of secondary sexual ornaments in the Japanese barn swallowHirundo rustica gutturalis. First, we showed that the peak amplitude frequency of male enticement calls was, on average, lower than that of nestling food‐begging calls, indicating that higher pitched calls are more similar to nestling food‐begging calls than are lower pitched calls. Second, we conducted an experimental playback of male enticement calls during the courtship period with the female's mate removed, and found that females were more attracted to heightened‐pitch calls than to control calls. Lastly, the peak amplitude frequency of male enticement calls was negatively related to the ornamentation, as measured by throat coloration. Taken together, these findings suggest the following: (1) females are attracted to a more nestling‐like trait, and (2) similarity to nestling food‐begging calls increases with decreasing secondary sexual ornaments. Nestling‐like male traits that are not secondary sexual characteristics should be considered when studying the general pattern of female attraction to male traits.

Genetic Architecture of Conspicuous Red Ornaments in Female Threespine Stickleback.

Explaining the presence of conspicuous female ornaments that take the form of male-typical traits has been a longstanding challenge in evolutionary biology. Such female ornaments have been proposed to evolve via both adaptive and nonadaptive evolutionary processes. Determining the genetic underpinnings of female ornaments is important for elucidating the mechanisms by which such female traits arise and persist in natural populations, but detailed information about their genetic basis is still scarce. In this study, we investigated the genetic architecture of two ornaments, the orange-red throat and pelvic spine, in the threespine stickleback (Gasterosteus aculeatus). Throat coloration is male-specific in ancestral marine populations but has evolved in females in some derived stream populations, whereas sexual dimorphism in pelvic spine coloration is variable among populations. We find that ornaments share a common genetic architecture between the sexes. At least three independent genomic regions contribute to red throat coloration, and harbor candidate genes related to pigment production and pigment cell differentiation. One of these regions is also associated with spine coloration, indicating that both ornaments might be mediated partly via pleiotropic genetic mechanisms.

Long incubation off-bouts of females paired with colorful males in Barn Swallows (Hirundo rustica)

ABSTRACT Among several types of parental care behavior, incubation behavior in passerine birds offers an ideal opportunity to study the link between female parental care and male ornamentation, because males generally lack an incubation patch, and thus rarely incubate. Although preceding studies have focused mainly on on-bout duration (or its total amount, i.e., nest attentiveness), it has recently been established that off-bout durations, independent of on-bout durations, are also important for embryo development and thus for efficient incubation. Using Barn Swallows Hirundo rustica, we found that the duration of female incubation off-bouts increased with a sexually selected trait, male throat coloration, independent of female nest attentiveness. A longer female off-bout was positively correlated with the incubation period, indicating that colorful males had reproductive disadvantage because of their mates’ inefficient incubation. Together with a previous study in which females demonstrated a higher amou...

Local anesthesia with monitored anesthesia care for patients undergoing thyroidectomy: a case series

Because the current trend favors minimally invasive surgery for thyroid disease, increasing interest has developed for thyroidectomy under local anesthesia with monitored anesthesia care (MAC). Here, we retrospectively reviewed 18 cases of thyroidectomy performed under local anesthesia with MAC in a single center. All of the procedures were performed by a single surgeon, using local lidocaine infiltration around the incisional site and propofol plus remifentanil target-controlled infusion. Sore throat (4/18), hypocalcemia (1/18), and transient voice color change (1/18) were observed, but the patients recovered during the follow-up period. No cases of postoperative nausea and vomiting, hematoma, wound problems, or vocal cord paralysis were observed. Local anesthesia with MAC provided satisfactory sedation in most patients without conversion to general anesthesia.

Testosterone-Induced Expression of Male Colour Morphs in Females of the Polymorphic Tawny Dragon Lizard, Ctenophorus decresii.

Many colour polymorphisms are present only in one sex, usually males, but proximate mechanisms controlling the expression of sex-limited colour polymorphisms have received little attention. Here, we test the hypothesis that artificial elevation of testosterone in females of the colour polymorphic tawny dragon lizard, Ctenophorus decresii, can induce them to express the same colour morphs, in similar frequencies, to those found in males. Male C. decresii, express four discrete throat colour morphs (orange, yellow, grey and an orange central patch surrounded by yellow). We used silastic implants to experimentally elevate testosterone levels in mature females to induce colour expression. Testosterone elevation resulted in a substantial increase in the proportion and intensity of orange but not yellow colouration, which was present in a subset of females prior to treatment. Consequently, females exhibited the same set of colour morphs as males, and we confirmed that these morphs are objectively classifiable, by using digital image analyses and spectral reflectance measurements, and occur in similar frequencies as in males. These results indicate that the influence of testosterone differs for different colours, suggesting that their expression may be governed by different proximate hormonal mechanisms. Thus, caution must be exercised when using artificial testosterone manipulation to induce female expression of sex-limited colour polymorphisms. Nevertheless, the ability to express sex-limited colours (in this case orange) to reveal the same, objectively classifiable morphs in similar frequencies to males suggests autosomal rather than sex-linked inheritance, and can facilitate further research on the genetic basis of colour polymorphism, including estimating heritability and selection on colour morphs from pedigree data.

Females sample more males at high nesting densities, but ultimately obtain less attractive mates.

BackgroundSexual selection is largely driven by the availability of mates. Theory predicts that male competition and female choice should be density-dependent, with males competing more intensely at relatively high density, and females becoming increasingly discriminating when there are more males from whom to choose. Evidence for flexible mating decisions is growing, but we do not understand how environmental variation is incorporated into mate sampling strategies. We mimicked threespine stickleback (Gasterosteus aculeatus) breeding conditions in pools with high and low densities of nesting males and allowed females to search for mates to determine whether 1) mate search strategies change with the density of breeding males and 2) pre-copulatory components of mate choice (signalling, competition, search patterns, and mating decisions) are modified in parallel.ResultsWhile females sampled more males at high male density, suggesting greater opportunity for sexual selection, the expanded search did not result in females choosing males with more attractive sexual signals. This is likely because red throat colouration was twice as great when half as many males competed. Instead, females chose similarly at high and low male density, using a relative strategy to compare male traits amongst potential suitors. Reduced throat colour could reflect a trade-off with costly male competition. However, we did not observe more intense competition at higher relative density. Density-dependent signalling appears largely responsible for females associating with males who have more attractive signals at low density. If we lacked knowledge of plasticity in signalling, we might have concluded that females are more discriminating at low male density.ConclusionsTo understand interactions between mate choice and population dynamics, we should consider how components of mate choice that precede the mating decision interact.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0481-3) contains supplementary material, which is available to authorized users.

Environment, but not genetic divergence, influences geographic variation in colour morph frequencies in a lizard.

BackgroundIdentifying the causes of intraspecific phenotypic variation is essential for understanding evolutionary processes that maintain diversity and promote speciation. In polymorphic species, the relative frequencies of discrete morphs often vary geographically; yet the drivers of spatial variation in morph frequencies are seldom known. Here, we test the relative importance of gene flow and natural selection to identify the causes of geographic variation in colour morph frequencies in the Australian tawny dragon lizard, Ctenophorus decresii.ResultsPopulations of C. decresii are polymorphic for male throat coloration and all populations surveyed shared the same four morphs but differed in the relative frequencies of morphs. Despite genetic structure among populations, there was no relationship between genetic similarity or geographic proximity and similarity in morph frequencies. However, we detected remarkably strong associations between morph frequencies and two environmental variables (mean annual aridity index and vegetation cover), which together explained approximately 45 % of the total variance in morph frequencies.ConclusionsSpatial variation in selection appears to play an important role in shaping morph frequency patterns in C. decresii. Selection associated with differences in local environmental conditions, combined with relatively low levels of gene flow, is expected to favour population divergence in morph composition, but may be counteracted by negative frequency-dependent selection favouring rare morphs.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0442-x) contains supplementary material, which is available to authorized users.

Population-Specific Covariation between Immune Function and Color of Nesting Male Threespine Stickleback.

Multiple biological processes can generate sexual selection on male visual signals such as color. For example, females may prefer colorful males because those males are more readily detected (perceptual bias), or because male color conveys information about male quality and associated direct or indirect benefits to females. For example, male threespine stickleback often exhibit red throat coloration, which females prefer both because red is more visible in certain environments, and red color is correlated with male immune function and parasite load. However, not all light environments favor red nuptial coloration: more tannin-stained water tends to favor the evolution of a melanic male phenotype. Do such population differences in stickleback male color, driven by divergent light environments, lead to changes in the relationship between color and immunity? Here, we show that, within stickleback populations, multiple components of male color (brightness and hue of four body parts) are correlated with multiple immune variables (ROS production, phagocytosis rates, and lymphocyte:leukocyte ratios). Some of these color-immune associations persist across stickleback populations with very different male color patterns, whereas other color-immune associations are population-specific. Overall, lakes with red males exhibit stronger color-immune covariance while melanic male populations exhibit weak if any color-immune associations. Our finding that color-immunity relationships are labile implies that any evolution of male color traits (e.g., due to female perceptual bias in a given light environment), can alter the utility of color as an indicator of male quality.

The Cellular Basis of Polymorphic Coloration in Common Side-Blotched Lizards,Uta stansburiana

Diurnal lizards are useful model organisms for the study of color polymorphisms. The cellular basis of nonavian reptilian coloration and dermal chromatophores, as well as the different pigments contained therein, is relatively well understood. Nonetheless, specific predictions cannot be made for the biochemical chromatophore constituents of individual species a priori. Despite well-documented associations between throat coloration and behavioral, physiological, and life history traits, the cellular basis of throat coloration in polymorphic Common Side-Blotched Lizards, Uta stansburiana, has never been studied. We used a combination of chromatographic techniques in conjunction with transmission electron microscopy and a thin-layer reflectance model to determine the cellular basis of polymorphic coloration in U. stansburiana. We found that different morphs express coloration through varying spatial arrangements of dietary xanthophylls (lutein and zeaxanthin), differential synthesis of drosopterins, differential melanin synthesis, and morph-specific iridophore reflecting platelets. Our results indicate that chromatic variations in this polymorphism cannot be attributed to alternative xanthophore pigmentation or structural reflectance alone. Instead, the chromatophores of U. stansburiana are multicomponent color signals.

Conspicuous female ornamentation and tests of male mate preference in threespine sticklebacks (Gasterosteus aculeatus).

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.

Genetics and Anthocyanin Analysis of Flower Color in Mexican Petunia

The genetics and anthocyanins responsible for flower color were studied in Ruellia simplex Wright (mexican petunia). An F2 population with 153 individuals segregating for four flower colors was developed from a cross between a maternal individual with white corolla with purple throat (WP) and a paternal individual with pink corolla (PK). All the F1 generation had fully purple flowers (P). The F2 generation segregated 94 P:30 PK:24 WP:5 WPK (WPK is a new color combination of white corolla limb and pink throat). These data were separated into groups for corolla limb color and for throat color. The ratio for corolla limb color segregated 94 P:30 PK:29 W, which fits a 9:3:4 recessive epistasis interaction (P = 0.22). The data for corolla throat segregated 118 P:35 PK, which fits a 3:1 ratio (P = 0.54). High-performance liquid chromatography mass spectrometry analyses were performed to elucidate the anthocyanins responsible for the four obtained flower colors. We found that delphinidin derivatives conferred purple corolla color, whereas pelargonidin derivatives were responsible for the pink corolla color. Purple corolla throat color was the result of delphinidin derivatives, whereas the pink color was the result of peonidin derivatives.