Variable visual habitats may influence the spread of colourful plumage across an avian hybrid zone

Several studies have shown that hybridization can be a creative process by acting as a conduit for the spread of adaptive traits between species, but few provide the mechanism that favours this spread. In the hybrid zone between the golden- (Manacus vitellinus) and white-collared (Manacus candei) manakins, sexual selection drives the introgression of golden/yellow plumage into the white species; however, the mechanism for the yellow male's mating advantage and the reasons why yellow plumage has not swept further into the white species remain mostly speculative. We quantified the colour properties of male plumage, the background and the ambient light at the hybrid zone, and allopatric golden and white populations. As measured by the perceived difference in colour between plumage and background, we found that yellow plumage appears more conspicuous than white plumage in the hybrid zone and allopatric golden-collar habitats, whereas white plumage appears more conspicuous than yellow plumage in the allopatric white-collared habitat. These results suggest a mechanism for the unidirectional spread of yellow plumage across the hybrid zone but slowed movement beyond it.     

UNIDIRECTIONAL INTROGREESION OF A SEXUALLY SELECTED TRAIT ACROSS AN AVIAN HYBRID ZONE: A ROLE FOR FEMALE CHOICE?

Hybridization can be an evolutionary creative force by forming new polyploid species, creating novel genetic variation or acting as conduits of potentially advantageous traits between hybridizing forms. Evidence for the latter is often difficult to find because alleles under positive selection can spread rapidly across a hybrid zone and sweep to fixation. In Western Panama, an avian hybrid zone between two species of manakins in the genus Manacus exists where the unidirectional introgression of bright, yellow plumage into a white population provides evidence for the importance of hybrid zones as conduits of advantageous traits. Several lines of indirect evidence suggest that sexual selection favoring yellow plumage drives this asymmetrical spread, but more direct evidence is lacking. Along the edge of the hybrid zone, both yellow- and white-collared manakins are found in the same mating arenas or leks and compete for the same females ("mixed leks"), providing us with a unique opportunity to understand the dynamics of yellow plumage introgression. We studied these mixed leks to determine whether yellow males have a mating advantage over white males and, if so, whether the mating advantage is driven by male-male interactions, female choice, or both. We found that yellow males mated more than white males, suggesting that sexual selection favoring yellow males can, indeed, explain the spread of yellow plumage. However, we found that this advantage occurred only in mixed leks where the frequency of yellow males is greater than white males. This suggests that the advantage of yellow males may depend on the presence of other yellow males, which may slow the rate of introgression in leks where yellow frequency is low such as in areas where yellow males are beginning to colonize the white population. This, along with the geographic barrier posed by major rivers in the hybrid zone, may initially limit or slow the spread of yellow plumage. Finally, we found that yellow and white males were similar in aggression and body size, and held comparable positions within leks. Because these traits or factors are often important in or dictated by aggressive male-male interactions, these comparisons indicate that male-male interaction is not the primary mechanism for the spread of yellow plumage. However, white and yellow males received similar numbers of courtship visits from females but differed in the number of matings, suggesting that females actively rejected white in favor of yellow males. Our results indicate that sexual selection by female choice has driven the unidirectional introgression of yellow plumage into the white population, providing a mechanism for how hybrid zones act as conduits of novel and advantageous traits.     

Kin selection may contribute to lek evolution and trait introgression across an avian hybrid zone

Understanding the mechanism(s) that favour cooperation among individuals competing for the same resources provides direct insights into the evolution of grouping behaviour. In a hybrid zone between golden-/yellow-collared (Manacus vitellinus) and white-collared (Manacus candei) manakins, males form aggregations composed of white and yellow males solely to attract females ('mixed leks'). Previous work shows that yellow males in these mixed leks experience a clear mating advantage over white males, resulting in the preferential introgression of yellow plumage allele(s) into the white species. However, the yellow male mating advantage only occurs in mixed leks with high frequencies of yellow males, and only a few of these males probably mate. Hence, it remains unclear why unsuccessful males join leks. Here, we used microsatellite markers to estimate pairwise relatedness among males within and between leks to test whether indirect genetic benefits of helping kin ('kin selection') can promote grouping. We found that yellow males are significantly more related to each other within than between leks, while relatedness among white males did not differ within and between leks. This suggests that yellow males may indirectly enhance their own reproductive success by preferentially lekking with relatives because yellow plumage is under positive frequency-dependent selection (positive FDS). Our results are consistent with the hypothesis that kin selection may promote grouping and facilitate positive FDS for yellow males, mediating the movement of yellow plumage across this hybrid zone.     

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.     

EVOLUTIONARY IMPLICATIONS OF DIVERGENT CLINES IN AN AVIAN (MANACUS: AVES) HYBRID ZONE

Abstract A previous study of the hybrid zone in western Panama between white‐collared (Manacus candei) and golden‐collared manakins (M. vitellinus) documented the unidirectional introgression of vitellinus male secondary sexual traits across the zone. Here, we examine the hybrid zone in greater genetic and morphological detail. Statistical comparisons of clines are performed using maximum‐likelihood and nonparametric bootstrap methods. Our results demonstrate that an array of six molecular and two morphometric markers agree in cline position and width. Clines for male collar and belly color are similar in width to the first eight clines, but are shifted in position by at least five cline widths. The result is that birds in intervening populations are genetically and morphometrically very like parental candei, but males have the plumage color of parental vitellinus. Neither neutral diffusion nor nonlinearity of color scales appear to be viable explanations for the large cline shifts. Genetic dominance of vitellinus plumage traits is another potential explanation that will require breeding experiments to test. Sexual selection remains a plausible explanation for the observed introgression of vitellinus color traits in these highly dimorphic, polygynous, lek‐mating birds. Two other clines, including a nondiagnostic isozyme locus, are similar in position to the main cluster of clines, but are broader in width. Thus, introgression at some loci is greater than that detected with diagnostic markers. Assuming that narrow clines are maintained by selection, variation in cline width indicates that selection is not uniform throughout the genome and that diagnostic markers are under more intense selective pressure. The traditional focus on diagnostic markers in studies of hybrid zones may therefore lead to underestimates of average introgression. This effect may be more pronounced in organisms with low levels of genetic divergence between hybridizing taxa.     

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice—red versus orange male back plumage colour—but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.     

High-Speed Video Analysis Reveals Individual Variability in the Courtship Displays of Male Golden-Collared Manakins

The males of the Golden-collared manakin ( Manacus vitellinus ), a passerine bird of the Neotropical region, perform elaborate courtship displays that are among the most spectacular in the animal kingdom. During a 7-mo long breeding season, male manakins aggregate in leks of up to 12 individuals, and each male clears a small 'court' on the forest floor where he spends several hours per day performing his displays either with or without the presence of a female. Like males of other manakin species, males of M. vitellinus produce loud mechanical sounds with their wings during the displays. The elaborate displays of the manakins are thought to be the result of sexual selection, which is particularly intense in lekking species in which females choose their mate mainly on the basis of behavioural and morphological features. However, we know little about differences in display between male manakins which may be related to individual differences in reproductive success. A quantitative, detailed analysis of the courtship displays has been difficult because the birds' movements are too fast to be studied with standard video recording techniques. For the first time, we recorded the displays of male Golden-collared manakins in the forest of Panama with a high-speed camera that allows a time resolution 5–40 times higher than that of a standard video camera. We found that several elements of the displays differed significantly between individuals. In addition, the slow-motion analysis revealed the features of the displays that had not been described in previous studies. Individually different features of the displays may form the basis for female choice and will allow testing hypotheses about the evolution of the manakin displays by sexual selection and their importance for speciation mechanisms in the genus Manacus .     

Female choice for male motor skills

Sexual selection was proposed by Darwin to explain the evolution of male sexual traits such as ornaments and elaborate courtship displays. Empirical and theoretical studies have traditionally focused on ornaments; the reasons for the evolution of elaborate, acrobatic courtship displays remain unclear. We addressed the hypothesis that females choose males on the basis of subtle differences in display performance, indicating motor skills that facilitate survival. Male golden-collared manakins (Manacus vitellinus) perform elaborate, acrobatic courtship displays. We used high-speed cameras to record the displays of wild males and analysed them in relation to male reproductive success. Females preferred males that performed specific display moves at greater speed, with differences of tens of milliseconds strongly impacting female preference. In additional males, we recorded telemetrically the heart rate during courtship using miniature transmitters and found that courtship is associated with profoundly elevated heart rates, revealing a large metabolic investment. Our study provides evidence that females choose their mates on the basis of subtle differences in motor performance during courtship. We propose that elaborate, acrobatic courtship dances evolve because they reflect motor skills and cardiovascular function of males.     

Males in seemingly female‐like plumage do not mimic females: UV reflectance reveals temporal cryptic dimorphism in a manakin species exhibiting delayed plumage maturation

Manakins (Pipridae) are neotropical birds that usually exhibit delayed plumage maturation (DPM). Thus, while plumage of most adult male manakins is brightly conspicuous, subadult males and females are basically dull‐olive green. Although sexual dichromatism in some bird species may be evident only through UV reflectance, this phenomenon, known as hidden sexual dichromatism, has not been previously studied in manakins to compare subadult males and females. Within this framework, we carried out spectrophotometric analyses in searching for hidden sexual dichromatism in the white‐bearded manakin Manacus manacus, through comparison of UV spectra in females and subadult males in green plumage. Our results revealed UV reflectance in both sexes in green plumage. Moreover, we found UV spectral differences in homologous color patches between sexes, particularly at belly. Since the observed differences may allow intraspecific sex recognition of individuals in green plumage, our results do not support the female‐mimicry hypothesis to explain delayed plumage maturation in the white‐bearded manakin. Although our findings dismiss the female mimicry hypothesis, we cannot state whether these results support the non‐mutually exclusive cryptic and status signaling hypotheses. We propose then, that dull coloration of subadult males may serve both as a cryptic trait and to limit the energetic costs of acquiring the adult plumage before sexual maturity. Meanwhile, differential UV color traits between sexes in green plumage may allow adult males to avoid unnecessary energy expenditures in courtship displays in the presence of males near leks, and to selectively focus their the courtship displays on females. In accordance with the status signaling hypothesis, subadult males can be recognized both as males and subordinates and consequently may practice courtship displays without suffering aggressions by adult males. Our results highlight the importance to include a wider range of spectrophotometric information analyses for testing hypotheses regarding delayed plumage maturation.     

Plumage brightness predicts male mating success in the lekking golden-collared manakin, Manacus vitellinus

The evolution of colorful plumage has been dramatic in lekkingspecies. Several studies show that the size of colorful traitsinfluence female choice in leks; however, relatively littleis known about the specific function of color, in particularits spectral properties, in lekking taxa. To determine the importanceof color in a lekking species, we monitored the mating successof male golden-collared manakins, Manacus vitellinus, and relatedthis to spectral measures of their colorful plumage, as wellas other morphological and behavioral traits shown to be importantin other lekking species. We found that lek centrality, malebody size, and plumage brightness were associated with malemating success. Only plumage brightness, however, entered amultiple regression model, indicating that plumage is the overallbest predictor of mating success. These results provide evidencethat the spectral properties of colorful plumage predict malemating success in a lekking species and provide important insightinto why many lekking birds are dichromatic and elaborate incoloration.     

GENOMIC AND MORPHOLOGICAL ANALYSIS OF A SEMIPERMEABLE AVIAN HYBRID ZONE SUGGESTS ASYMMETRICAL INTROGRESSION OF A SEXUAL SIGNAL

Hybrid zones are geographic regions where differentiated taxa meet and potentially exchange genes. Increasingly, genomic analyses have demonstrated that many hybrid zones are semipermeable boundaries across which introgression is highly variable. In some cases, certain alleles penetrate across the hybrid zone in only one direction, recombining into the alternate genome. We investigated this phenomenon using genomic (genotyping‐by‐sequencing) and morphological (plumage reflectance spectrophotometry) analyses of the hybrid zone between two subspecies of the red‐backed fairy‐wren (Malurus melanocephalus) that differ conspicuously in a sexual signal, male back plumage color. Geographic cline analyses revealed a highly variable pattern of differential introgression, with many narrow coincident clines combined with several significantly wider clines, suggesting that the hybrid zone is a semipermeable tension zone. The plumage cline was shifted significantly into the genomic background of the orange subspecies, consistent with sexual selection driving asymmetrical introgression of red plumage alleles across the hybrid zone. This interpretation is supported by previous experimental work demonstrating an extra‐pair mating advantage for red males, but the role of genetic dominance in driving this pattern remains unclear. This study highlights the potential for sexual selection to erode taxonomic boundaries and promote gene flow, particularly at an intermediate stage of divergence.     

Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus)

In order to attract females, male golden-collared manakins gather in leks and perform a complex display consisting of acrobatics accompanied by loud "wingsnapping". During this display, males show off their yellow beard and yellow, black, and green plumage that is striking in comparison to the dull green plumage of young males and females. We investigated the role of testosterone (T) in activating the display of manakins and in stimulating the growth of the adult male plumage. T regulates song, copulation, and territorial aggression in temperate species. In tropical species, however, T levels can be relatively low year round, which has raised questions about the involvement of T in courtship display and male aggression in these species. In neither temperate nor tropical species has the role of hormones in the shift from juvenile to adult plumage been well studied. Therefore, we implanted green-plumaged birds and adult males with either a T pellet or an inert pellet (controls) and observed the display behaviors of these birds in the field and in captivity. In captive birds, we also plucked feathers from sexually dimorphic regions and observed color and regeneration rate of new feathers. We found that birds implanted with T increased several display behaviors compared to controls. All plucked feathers grew back the same color as prior to treatment; however, we observed some differences in feather growth rate between T-treated birds and controls.     

Strong selection on male plumage in a hybrid zone between a hybrid bird species and one of its parents

Homoploid hybrid speciation (HHS) requires reproductive barriers between hybrid and parent species, despite incomplete reproductive isolation (RI) between the parents. Novel secondary sexual trait values in hybrids may cause prezygotic isolation from both parents, whereas signals inherited by the hybrid from one parent species may cause prezygotic isolation with the other. Here we investigate whether differences in male plumage function as a premating barrier between the hybrid Italian sparrow and one of its parent species, the house sparrow, in a narrow Alpine hybrid zone. Italian sparrow male plumage is a composite mosaic of the parental traits, with its head plumage most similar to its other parent, the Spanish sparrow. We use geographical cline analysis to examine selection on three plumage traits, 75 nuclear single nucleotide polymorphisms (SNPs) and hybrid indices based on these SNPs. Several SNPs showed evidence of restricted introgression in the Alps, supporting earlier findings. Crown colour exhibited the narrowest plumage cline, representing a 37% (range 4–65%) drop in fitness. The cline was too narrow to be due to neutral introgression. Only crown colour was significantly bimodal in the hybrid zone. Bimodality may be due to RI or a major QTL, although fitness estimates suggest that selection contributes to the pattern. We discuss the implications with respect to HHS and the species status of the Italian sparrow.     

TARGETS OF SEXUAL SELECTION: SONG AND PLUMAGE OF WOOD WARBLERS

Extant hypotheses predict that, in the face of sexual selection, avian song and plumage may evolve in a concerted fashion, in an antagonistic fashion, or in ways unrelated to each other. To test these ideas regarding which traits sexual selection targets, and the consequences for other traits, we analyzed patterns of song complexity and plumage dimorphism in 56 species of wood warblers (Parulinae). Overall, males of more dimorphic species sang shorter songs more often, but did not have more complex songs. However, when monomorphic species were excluded from the analysis, we found that the total time spent singing and repertoire size increased with plumage dimorphism. Monomorphic species are predominantly ground-nesters and the greater risk of nest predation for these species may constrain males from becoming more visually conspicuous. Thus, sexual selection may have been restricted to targeting song in these species. Even though song may have been the only target of sexual selection in ground-nesting species, overall, song in those species is not more complex than in species that nest above the ground. We propose that traits targeted by sexual selection evolve in concert, except when constrained by some ecological factor.     

Populations with elevated mutation load do not benefit from the operation of sexual selection

Theory predicts that if most mutations are deleterious to both overall fitness and condition-dependent traits affecting mating success, sexual selection will purge mutation load and increase nonsexual fitness. We explored this possibility with populations of mutagenized Drosophila melanogaster exhibiting elevated levels of deleterious variation and evolving in the presence or absence of male-male competition and female choice. After 60 generations of experimental evolution, monogamous populations exhibited higher total reproductive output than polygamous populations. Parental environment also affected fitness measures - flies that evolved in the presence of sexual conflict showed reduced nonsexual fitness when their parents experienced a polygamous environment, indicating trans-generational effects of male harassment and highlighting the importance of a common garden design. This cost of parental promiscuity was nearly absent in monogamous lines, providing evidence for the evolution of reduced sexual antagonism. There was no overall difference in egg-to-adult viability between selection regimes. If mutation load was reduced by the action of sexual selection in this experiment, the resultant gain in fitness was not sufficient to overcome the costs of sexual antagonism.     

Neuromuscular and endocrine control of an avian courtship behavior

In many species of birds, males perform complex visual and acoustic courtship displays to attract and stimulate females. Some of these displays involve considerable use of the wings and legs, suggesting that they may be controlled by sexually dimorphic spinal motoneurons and their target muscles. Sex steroid hormones are known to organize and activate many sexually dimorphic phenotypes, so these neuromuscular systems may also be steroid sensitive. To test these ideas, we have begun studies of wild golden-collared manakins (Manacus vitellinus) in Central America. Males of this species establish a courtship arena in the forest, where they perform an elaborate dance that includes use of their wings to generate loud snapping sounds. Here we describe male golden-collared manakin courtship behavior, including the various "wingsnaps." We also review our studies, and those of others, showing sexually dimorphic properties of manakin wings, the wing musculature, and sex steroid accumulation in the spinal cord. These data suggest that manakins are useful models for evaluating steroid control of complex peripheral neuromuscular systems.     

Aposematic signal variation predicts male-male interactions in a polymorphic poison frog

Many species use conspicuous "aposematic" signals to communicate unpalatability/unprofitability to potential predators. Although aposematic traits are generally considered to be classic examples of evolution by natural selection, they can also function in the context of sexual selection, and therefore comprise exceptional systems for understanding how conspicuous signals evolve under multifarious selection. We used males from a highly territorial poison frog species in a dichotomous choice behavioral test to conduct the first examination of how aposematic signal variation influences male-male interactions. Our results reveal two behavioral patterns: (1) male dorsal brightness influences the behaviors of male conspecifics such that males approach and call to brighter males more frequently and (2) a male's dorsal brightness predicts his own behavior such that bright males approach stimulus frogs faster, direct more calls to bright stimulus frogs, and exhibit lower advertising call pulse rates (a fitness-related trait). These findings indicate the potential for sexual selection by male-male competition to impact aposematic signal evolution.     

Androgen and the elaborate courtship behavior of a tropical lekking bird

In most bird species, male courtship behavior is controlled by testosterone (T) and its metabolites. In species breeding in temperate and arctic regions T circulates at high levels during a relatively short courtship period because high levels of T can be costly in terms of immunocompetence and parental care. Few studies have investigated androgen modulation of courtship behavior in tropical birds. Male golden-collared manakins (Manacus vitellinus) aggregate in leks for several months and perform spectacular, acrobatic courtship displays. Here we examined whether T is elevated in golden-collared manakins during the displaying period and if courtship behavior is modulated by androgen action on androgen receptors. We measured T levels in displaying males at the beginning of the breeding season and again, one month later. In addition, both wild and captive males were treated with the anti-androgen, flutamide, and their courtship behavior was recorded for several weeks. T levels were relatively high shortly after leks were established but decreased substantially a month later, even though the amount of courtship did not change. Flutamide reduced male courtship activity for one week, but display behavior then increased after two weeks of flutamide treatment. Our studies show that androgens modulate male manakin courtship, but the amount of courtship is not directly correlated with the concentration of circulating T. These results suggest that the relationships between androgen and courtship might differ between tropical and temperate birds.     

Sequence variation in the coding region of the melanocortin-1 receptor gene (MC1R) is not associated with plumage variation in the blue-crowned manakin (Lepidothrix coronata)

Avian plumage traits are the targets of both natural and sexual selection. Consequently, genetic changes resulting in plumage variation among closely related taxa might represent important evolutionary events. The molecular basis of such differences, however, is unknown in most cases. Sequence variation in the melanocortin-1 receptor gene (MC1R) is associated with melanistic phenotypes in many vertebrate taxa, including several avian species. The blue-crowned manakin (Lepidothrix coronata), a widespread, sexually dichromatic passerine, exhibits striking geographic variation in male plumage colour across its range in southern Central America and western Amazonia. Northern males are black with brilliant blue crowns whereas southern males are green with lighter blue crowns. We sequenced 810 bp of the MC1R coding region in 23 individuals spanning the range of male plumage variation. The only variable sites we detected among L. coronata sequences were four synonymous substitutions, none of which were strictly associated with either plumage type. Similarly, comparative analyses showed that L. coronata sequences were monomorphic at the three amino acid sites hypothesized to be functionally important in other birds. These results demonstrate that genes other than MC1R underlie melanic plumage polymorphism in blue-crowned manakins.     

Evolutionary changes in color patches of blackbirds are associated with marsh nesting

Fully unraveling the mechanisms of sexual selection requiresan understanding of the variation in secondary sexual traitsacross species in a monophyletic assemblage and an understandingof the evolutionary relationships between those species. Therole of red and yellow male plumage coloration in territorydefense and sexual selection has been well studied in the red-winged blackbird (Agelaius phoeniceus), and males of many other close relatives of this species also have what appear to be carotenoid-pigmented patches in their plumage. We explored variation in male plumagecoloration across species of New World blackbirds (family Icteridae):traits known to be involved in sexual selection in this group.We document that blackbird lineages in which extant speciesbreed in marshes tend to have evolved from an all-black ancestralplumage to one exhibiting carotenoid plumage patches. The twomost likely hypotheses to explain this pattern are (1) increasedsexual selection intensity in marshes because of increasedvariance in territory quality and (2) increased frequency ofmale-male territorial interactions because of an increaseddensity of territories in marshes, but other hypotheses cannotbe ruled out. This pattern is consistent with either intersexualor intrasexual selection and warrants further investigation.