Comparative evidence for costs of secondary sexual characters: adaptive vane emargination of ornamented feathers in birds

We used a comparative approach, by comparing bird species with tail ornamentation with sister taxa without ornamentation, to deduce the aerodynamic function of extravagant feather ornaments and the costs of such ornaments in birds. First, the aerodynamic function of tail feather ornaments in birds can be deduced from asymmetry in the width of tail feather vanes, since flightless birds have symmetrical vanes while flying birds without feather exaggeration by sexual selection have asymmetrical vanes. Distal inner vanes at the tip of tail feathers were more narrow in ornamented as compared to nonornamented birds, and vane asymmetry at the tip of the feather was therefore reduced in ornamented species, suggesting marginal aerodynamic function of the distal part of extravagant feather ornaments. Second, the cost of feather ornaments due to parasite drag is proportional to the area of feathers extending beyond the maximum continuous width of the tail, and aerodynamic costs of long tails could therefore be diminished by a reduction in feather width. Consistent with this prediction, the outermost tip of feather ornaments was narrower than the homologous character in nonornamented sister taxa, while the base of the feather had similar width in the two groups of birds. These results suggest that the costs of extravagant ornamentation have been diminished by a reduction in feather width, leading to a reduction in drag. Costs of feather ornaments, as demonstrated by their fine morphology, thus appear to have been extensive during the evolution of these characters.     

Population differences in density and resource allocation of ornamental tail feathers in the barn swallow

Many organisms show well‐defined latitudinal clines in morphology, which appear to be caused by spatially varying natural selection, resulting in different optimal phenotypes in each location. Such spatial variability raises an interesting question, with different prospects for the action of sexual selection on characters that have a dual purpose, such as locomotion and sexual attraction. The outermost tail feathers of barn swallows (Hirundo rustica) represent one such character, and their evolution has been a classic model subject to intense debate. In the present study, we examined individuals from four European populations to analyze geographical variation in the length and mass of tail feathers in relation to body size and wing size. Tail feather length differed between sexes and populations, and such variation was a result of the effects of natural selection, acting through differences in body size and wing size, as well as the effects of sexual selection that favours longer tails. The extra enlargement of the tail promoted by sexual selection (i.e. beyond the natural selection optimum) could be achieved by increasing investment in ornaments, and by modifying feather structure to produce longer feathers of lower density. These two separate processes accounting for the production of longer and more costly tail feathers and less dense feathers, respectively, are consistent with the hypothesis that both Zahavian and Fisherian mechanisms may be involved in the evolution of the long tails of male barn swallows. We hypothesize that the strength of sexual selection increases with latitude because of the need for rapid mating as a result of the short duration of the breeding season at high latitudes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 925–936.     

Sex-limited expression of ornamental feathers in birds

Extravagant secondary sexual characters show sexual size dimorphismin some species but are completely sex limited in others. Sexualornamentation has been hypothesized to benefit mainly malesthrough sexual selection, but the costs of secondary sexualcharacters initially would be experienced by both sexes. Theevolution of sexual size dimorphism of ornaments and, eventually, the complete sex-limited expression of these characters, willdepend on the effects of sexual and natural selection on thetwo sexes. A phylogenetic analysis controlling for similaritiesdue to common ancestry of 60 independent evolutionary originsof feather ornamentation in birds was used to investigate ecologicalfactors correlated with sexual size dimorphism and sex-limited expression of secondary sexual characters. When the size ofan ornament is large relative to body size, the trait willbe particularly costly for females, resulting in selectionfor increased sexual size dimorphism of the ornament. Indeed,sexual size dimorphism of ornaments was positively related to the relative size of male ornaments but was unrelated torelative size of female ornaments. Species with polygynousand lekking mating systems with little or no male parentalcare (in particular nest building and incubation) demonstratedsex-limited expression of ornaments as compared to monogamous species. Species with no food provisioning of offspring by themale showed a trend for increased sexual size dimorphism ofornaments. Therefore, large natural selection costs duringreproduction imposed by the expression of secondary sexualcharacters are related to the evolution of sexual size dimorphismof ornaments and eventually their complete loss from females.     

Patterns of morphometric variation in birds' tails: length, shape and variability

In Palaearctic birds, tail length was more variable than wing and tarsus, but not bill lengths. Tails of the ornamental shapes pin, lyre and graduated varied more in length than did non-ornamental shapes. Log coefficient of variation (C V) tail length showed an overall U-shaped relationship with longtailedness, but although the CV for most tail shapes increased in short-tailed species, only in ornamental shapes was C V also high in long-tailed species. C V of fork depth was lowest at a fork depth of 2, and considerably higher in shallow forked tails. CV streamer lengths were similar to CV deep fork depths. The more deeply forked tails thus seem ornamental. Phylogenetically independent contrasts confirmed in males, but not females, that long-tailed species had greater CV than medium-tailed species, and the greater CV of graduated than square tails, but the CV of short- and medium-tailed species did not differ. These comparisons, however, did not control for tail shape. The greater elongation and CV of tails with ornamental shapes are consistent with an influence of sexual/signal selection on these tails, and the increase in CV with longtailedness suggests that Weber's law applies to the perceptual threshold for tail length. Sexual selection may have a widespread, but moderate, influence on tail traits in birds.     

Variable sexual ornaments in scarlet-tufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya

In order to be elaborated by sexual selection, sexual ornaments must vary perceptibly and genetically among individuals in natural populations. Rather little is known about ornament variation in monogamous species, in which sexual selection should act more weakly than in polygynous species. We report phenotypic variation in feather ornament size (elongated tails and pectoral tufts) and body size in the scarlet-tufted malachite sunbird Nectarinia johnstoni , a monogamous, sexually dimorphic nectarivore of East African alpine zones. Fully-expressed male ornaments are highly significantly more variable (CVs = 12–29%) than are skeletal and wing measures primarily affected by natural selection (CVs = 2 4%). Female sunbirds have pectoral tufts which are significantly (22–25%) smaller than those of adult males, but more variable (CV_s= 21–22%, CV_s= 12–15%), and more variable than body size. Among males with fully-grown ornaments, those with longer tails tend to have longer wings and wider tufts. The high variation in fully-grown ornaments in malachite sunbirds is consistent with the view that the ornaments are condition-dependent sexual signals. Finally, we review studies of feather ornament variation to date, and show that ornaments are much more variable in monogamous than non-monogamous species, apparently due to the relatively weak pressure of sexual selection.     

Tail length in birds in relation to tail shape,general flight ecology and sexual selection

Relative tail length (longtailedness) of Palearctic birds was assessed by the standardized residuals of log–log regressions of tail length on wing length and tarsus length. The mean degree of tail shortening was greater than mean degree of tail lengthening, but there was a greater frequency of extreme long-tailed than short-tailed species. Longtailedness was greater in ornamental pin, lyre, deep forked and graduated shaped tails. These shapes (except graduated, for which data were lacking) were also relatively long-tailed according to shortest-rectrix lengths, this extra length potentially contributing compensatory lift. In forked tails, tail ratio increased linearly with longtailedness to above the aerodynamic optimum, and thus the most elongated forked tails were also more deeply forked. Tail shortening was marked for rounded tails, a surprising result in view of their slightly ornamental shape. Phylogenetically independent contrasts showed significantly greater longtailedness in graduated than square-tailed species, confirming the species-wide analysis. In phylogenetically independent contrasts of longtailedness and ecological factors, short-tailed species had significantly greater flight distances than medium-tailed species, but long- and medium-tailed species did not differ in migratory distance, foraging distance, overall flight distance or importance of aerial foraging. The data suggest that ecological factors, i.e. natural selection, are more important in the evolution of short-tailedness than longtailedness in birds, and that an additional influence of sexual selection on tail length and shape is also widespread.     

Male barn swallows use different resource allocation rules to produce ornamental tail feathers

Sexual ornaments compete for resources with other functionaltraits. Such resource allocation trade-offs should ensure thehonesty of sexual ornaments according to the Zahavi's handicapprinciple. However, the existence of costly signals could notbe enough to guarantee honesty if different individuals investdifferent proportions of their limited resources in ornaments.Then, a certain level of sexual signaling would correspond toseveral levels of individual condition. Here, we explore whetherthere are different resource allocation rules in tail featherornaments between males within a barn swallow (Hirundo rustica)population and whether these different rules confer differentviability to males. We assessed the proportion of resourcesinvested in ornamental feathers compared with other functionalfeathers moulted and growing during the same period at expensesof the same resources. We found that 1) different males allocatea different proportion of resources to ornamental feathers inrelation to functional feathers and this proportion is repeatablebetween years and 2) male survival likelihood decreased as theproportion of resources allocated to ornamental feathers increased.Survival costs associated with increased investments in ornamentscan maintain the sexual signaling system honest at populationlevel but do not preclude the existence of an array of differentallocation rules between males. Thus, males with different viabilitycan produce ornamental feathers of the same length. These resultsshow that the relationship between male viability and ornamentexpression can be less straightforward than considered previously.     

Survival of male scarlet-tufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya and the influence of ornamentation

A prediction of handicap and signalling theories is that there should be a positive relationship between ornament size and viability. This prediction was tested in scarlet-tufted malachite sunbirds ( Nectarinia johnstoni ). These birds are endemic to the high-altitude zones of East African mountains. They are bright iridescent green with elongated central tail feathers and red pectoral tufts. The elongated tail is believed to be a mate choice cue, and the red tufts play a role in aggressive encounters between males. As adults, they feed almost exclusively on the nectar of Lobelia telekii flowers, which males defend from conspecifics. The long term survival of individually identifiable males colour-marked in 1989 and 1990 was investigated. Territorial adult males had an average annual survival rate of 72%, which is at the top of the range reported for tropical birds. The effects of morphology and territory characteristics on male survival were examined by adding covariates to the survival model. This analysis showed that male N. johnstoni with longer tails had a higher probability of survival than did short-tailed males. There was no apparent relation between tuft size or the number of L. telekii inflorescences on the territory and survival. The results presented here suggest that long-tailed males may be of intrinsically higher quality than are shorter tailed males. If this is true then females may benefit by using this trait as a mate choice cue through increased viability of their offspring.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 125–133.     

Sympatric divergence and clinal variation in multiple coloration traits of Ficedula flycatchers

Geographic variation in phenotypes plays a key role in fundamental evolutionary processes such as local adaptation, population differentiation and speciation, but the selective forces behind it are rarely known. We found support for the hypothesis that geographic variation in plumage traits of the pied flycatcher Ficedula hypoleuca is explained by character displacement with the collared flycatcher Ficedula albicollis in the contact zone. The plumage traits of the pied flycatcher differed strongly from the more conspicuous collared flycatcher in a sympatric area but increased in conspicuousness with increasing distance to there. Phenotypic differentiation (P_ST) was higher than that in neutral genetic markers (F_ST), and the effect of geographic distance remained when statistically controlling for neutral genetic differentiation. This suggests that a cline created by character displacement and gene flow explains phenotypic variation across the distribution of this species. The different plumage traits of the pied flycatcher are strongly to moderately correlated, indicating that they evolve non‐independently from each other. The flycatchers provide an example of plumage patterns diverging in two species that differ in several aspects of appearance. The divergence in sympatry and convergence in allopatry in these birds provide a possibility to study the evolutionary mechanisms behind the highly divergent avian plumage patterns.     

Effects of polyandry on male phenotypic diversity

Polyandry has the potential to affect the distribution of phenotypes and to shape the direction of sexual selection. Here, we explore this potential using Trinidadian guppies as a model system and ask whether polyandry leads to directional and/or diversifying selection of male phenotypic traits. In this study, we compare the phenotypic diversity of offspring from multiply and singly sired broods. To quantify phenotypic diversity, we first combine phenotypic traits using multivariate methods, and then take the dispersion of individuals in multivariate space as our measure of diversity. We show that, when each trait is examined separately, polyandry generates offspring with a higher proportion of bright coloration, indicating directional selection. However, our multivariate approach reveals that this directionality is accompanied by an increase in phenotypic diversity. These results suggest that polyandry (i) selects for the production of sons with the preferred brighter colour phenotypes whereas (ii) enhancing the diversity of male sexual traits. Promoting phenotypic diversity may be advantageous in coping with environmental and reproductive variability by increasing long‐term fitness.     

Phenotypic and genetic variation in male genitalia in the seedbug, Lygaeus equestris (Heteroptera)

Male genitalia evolve through sexual selection and, in insects, tend to show negative static allometry, low phenotypic variation, and are usually relatively small. Much less is known about the genetic variation and heritability of male genitalia. Additionally, in instances where the intromittent organ is greatly elongated, it is unclear whether typical patterns of genital scaling and variation also apply. In the present study, we investigated the allometry, variation, and heritability of male genital length in the seedbug, Lygaeus equestris , a species with a greatly elongated intromittent organ (i.e. almost as long as male body size). We found that genital length was negatively allometric, in spite of its great length, and was no more variable than nongenital traits. Additionally, genital length was significantly heritable and had considerable evolvability.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 400–405.     

Resonating feathers produce courtship song

Male Club-winged Manakins, Machaeropterus deliciosus (Aves: Pipridae), produce a sustained tonal sound with specialized wing feathers. The fundamental frequency of the sound produced in nature is approximately 1500 Hz and is hypothesized to result from excitation of resonance in the feathers'' hypertrophied shafts. We used laser Doppler vibrometry to determine the resonant properties of male Club-winged Manakin''s wing feathers, as well as those of two unspecialized manakin species. The modified wing feathers exhibit a response peak near 1500 Hz, and unusually high Q-values (a measure of resonant tuning) for biological objects (Q up to 27). The unmodified wing feathers of the Club-winged Manakin do not exhibit strong resonant properties when measured in isolation. However, when measured still attached to the modified feathers (nine feathers held adjacent by an intact ligament), they resonate together as a unit near 1500 Hz, and the wing produces a second harmonic of similar or greater amplitude than the fundamental. The feathers of the control species also exhibit resonant peaks around 1500 Hz, but these are significantly weaker, the wing does not resonate as a unit and no harmonics are produced. These results lend critical support to the resonant stridulation hypothesis of sound production in M. deliciosus.     

Patterns of variation in tail ornament size in birds

In recent years several different kinds of sexual selection models have been developed, and tail ornaments in birds have frequently been used as an example of a sexually selected character where the models might apply. However, very little is known about intra- and interpopulation variation in ornament size. We have studied the elongated tail ornaments in four species of whydahs Vidua , the forktailed flycatcher Tyrannus savana and the Asian paradise flycatcher Terpsiphone paradisi. Ornaments were relatively longer in males with the longest tarsi ('heterogony' with positive allometry). Also, tail lengths were remarkably variable within each geographical area, the coefficient of variation (average = 11%) being three times as high as for body size characters. Models, with female preference of ornaments bearing no relation to male viability, usually generate lines of neutral equilibria. Thus, they predict extraordinary variation in ornaments between populations. However, elongated tail ornaments did not show higher geographical variation than the body size characters, suggesting that there is no line of equilibria for these ornaments.     

Exposure to pesticides impairs the expression of fish ornaments reducing the availability of attractive males

Ornament magnitude often reflects a local balance between sexual selection and other sources of natural selection opposing their elaboration. Human activity may disrupt this balance if it modifies the costs of producing, maintaining or displaying the ornaments. When costs are increased, a shortage of acceptable partners may ensue, with consequences commensurate with how stringent (and effective) the process of mate choice is. Here, we show that the expression of ornaments in the viviparous amarillo fish (Girardinichthys multiradiatus) is influenced by embryonic exposure to low concentrations of an organophosphorus insecticide. Male ornamental fin size, dimorphic yellow coloration and display rates were all compromised in exposed fish, but unaffected in their paternal half-sibling controls and in their sisters (morphology and colour). Exposure resulted in smaller fish of both sexes, thus the differential effect by sex was restricted to attributes such as fin size only above the naturally selected magnitude shown by females. Father phenotype predicted offspring morphology of controls, but not of exposed males, which were discriminated against by both control and exposed females. Since stringent female mate choice can result in females refusing to mate with suboptimal mates, this sub-lethal developmental effect can reduce the effective population size of amarillo fish populations.     

Natural variation in the sexually selected feather ornaments of crested auklets (Aethia cristatella) does not predict future survival

We evaluated whether sexually selected crest and auricular plumefeather ornaments of crested auklet (Aethia cristatella) adultscovaried with individual local survival over 11 years (1991–2001).Crested auklets (n = 364 total) were captured near breedingsites, marked with color rings, and local survival estimateswere based on color ring resightings at a breeding colony. Survivalestimates and relationships among local survival and crest length,auricular plume length, mass and tarsus were evaluated usingthe program MARK. The best models included four groups, definedby sex and ease of resighting, that differed in resighting rate(p) but not local survival rate (). This model structure effectivelyexplained sources of variation in local survival and resightabilityamong individuals. The best fitting model showed local survivalrate varying annually, while accounting for differences in resightabilityof marked individuals between the sexes and groups ([t], p[sex*easeof resighting]). Annual local survival varied from 0.940 ±0.029 (SE) in 1993–1994 to 0.767 ± 0.034 in 1997–1998and averaged 0.859 ± 0.019. We found no evidence thatcrested auklet local survival covaried with continuous variationin individuals' ornaments. Simulations indicated that our dataset was sufficient to detect a relationship between local survivaland a covariate that equaled or exceeded a range of 8%. Theimplications for competing sexual selection mechanisms of empiricallymeasured survival–ornament relationships are controversial,but our study emphasizes that survival estimates for such investigationsmust control for confounding factors such as resighting rateas well as have sufficient statistical power and time scaleto be biologically meaningful. Our results are most consistentwith the idea that the conspicuous variation in crested auklet'sshowy ornaments is arbitrary with respect to individual viabilityas quantified by their long-term survival.     

Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

The allometry of fluctuating asymmetry in southern African plants: flowers and leaves

Several studies of fluctuating asymmetry (FA) in animals show that secondary sexual characters used in signalling have a negative relationship between size and asymmetry. Larger sexual traits are presumably more costly to produce, which should lead to greater developmental stress and corresponding increases in asymmetry. In the absence of among individual variation in the ability to handle these costs, the relationship between size and asymmetry should thus be positive. A negative relationship therefore suggests that expression of these traits is condition-dependent. In plants, flowers act as signals for pollinators and may show similar trends to animal signals. Leaves which are uninvolved in signalling should not. Moller & Eriksson (1994) found that 89% of species ( n = 16 of 18) with insect-pollinated flowers showed a negative relationship between petal size and asymmetry, while 79% of species ( n = 15 of 19) showed a positive relationship between leaf size and asymmetry. I carried out a similar study of 18 plant species. The average relationship between petal size and asymmetry did not differ significantly from zero in those species showing measurable FA in flowers ( n = 12). The relationship was significantly negative in one species, and significandy positive in another. On average, leaves in species with FA did not show a significant positive relationship between size and asymmetry ( n = 7). There was no significant difference in the slopes of the relationship between size and asymmetry for leaves and flowers. Levels of floral asymmetry for species with FA were significandy repeatable on individual plants in 33% ( n = 4 of 12) of species, but leaf asymmetry was not significantly repeatable in any species. It is argued that condition-dependence of traits need not result in a negative relationship between size and asymmetry.     

Phenotypic plasticity in breeding plumage signals in both sexes of a migratory bird: responses to breeding conditions

Adaptive phenotypic plasticity may respond to present ambient conditions. Sexual and social signals in both sexes may express phenotype performance. Plumage signals that change discontinuously allow relating discrete variation to previous performance. Both sexes of the pied flycatcher Ficedula hypoleuca present white patches on the wings and on the forehead, which constitute sexual and social signals. Forehead patches are moulted together with body plumage in Africa, while wing patches are partly moulted in Africa and partly in the breeding area soon after breeding. We studied individual inter‐year changes (corrected for regression to the mean) in the size of forehead and wing patches of both sexes in seven years for females or six years for males in two nearby study areas in central Spain. We found that initial signal extent strongly delimits the possible subsequent changes negatively. There is a negative association of male age with forehead patch changes. Cold and rainy springs are associated in females with decreases in both patch areas and vice versa, while no association with climate is observed in male wing patch changes. Cold pre‐breeding conditions predict positive changes in female wing and male forehead patches. Breeding success is positively associated with forehead patch changes in females. Late‐breeding males experience more positive changes in forehead patch size than early‐breeding males. Some of these trends can be explained by variable costs of breeding in certain conditions for subsequent signal production and/or maintenance, while absence of trends in some cases may be explained by sex differences in costs of breeding and interactions with phenotypic quality of breeders.     

Sexual selection and condition‐dependence

The handicap theory of sexual selection suggests that females prefer mates who display extravagant ornaments that advertise their quality or condition. It is often assumed that as such ornamental traits undergo sexually‐selected exaggeration, they must inevitably become more sensitive to condition, and thus more informative. Here, we show that this is not necessarily the case. Depending on the precise form of the relationship between trait size and cost, expression may become more or less condition‐dependent as the trait undergoes exaggeration, or may remain unchanged. This leads us to question how much of the information content of sexual signals can be attributed to sexual selection, and how much to pre‐existing, naturally‐selected condition‐dependence.     

硬叶兜兰居群表型变异研究

为了揭示硬叶兜兰表型变异的规律,以滇东南核心分布地区7个硬叶兜兰居群113个体的18个表型数量性状进行研究,通过变异系数、巢式方差分析、相关性和聚类分析,结果显示:除了叶长、叶宽、花梗粗、苞片长和苞片宽5个数量性状不存在显著差异外,其余数量性状在居群水平上都存在显著差异。各性状变异系数在0.088~0.189之间,花梗长、叶长、叶长宽比、附毛长的变异系数较大,而中萼高、花囊高和宽、花梗粗、合萼高、花瓣宽和长相对变异不大;18个性状表型分化系数(Vst)在2.05%~50.62%之间,平均值达到22.02%,暗示有77.98%表型变异存在于居群内。除雄蕊长和宽表现居群内和居群间的变异相当外,果蒴长、花瓣长和宽、中萼高和宽、合萼高和宽的分化系数分别为36.03%、23.74%、24.55%、28.13%、18.00%、20.56%和18.12%,叶长最小,为2.05%,居群间的变异明显小于居群内。性状关联性研究表明:花瓣、合萼、中萼高、花梗长和叶长宽比高度相关,而叶宽、苞片长、雄蕊性状和中萼高与其余性状关联性不密切,这些性状相对独立,稳定性较高;基于数量指标的欧氏距离聚类表明:7个居群可分为2大类:杨柳井居群和马固居群为近缘支;其余5个居群(斗咀、小坝子、夹寒箐、古林箐和田坝)为一类。