Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters

The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress (Parsons 1990). Parasites and diseases are one kind of environmental stress which most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessment of phenotypic quality and thus in sexual selection.     

Evolutionary rates of secondary sexual and non-sexual characters among birds

The rate of evolutionary morphological change in secondary sexual characters among species has traditionally been assumed to exceed that for non-sexual characters, giving rise to a larger degree of divergence. We used a large data set of independent evolutionary events of exaggerated secondary sexual feather characters across all birds to test whether that was the case. Comparative analyses revealed that secondary sexual tail feather characters diverged more than wing feathers in females, and we also found that secondary sexual head feather characters diverged more than tarsi in males, when only including intra-order comparisons in the analyses. These results are in the predicted direction, with secondary sexual characters diverging more than ordinary morphological traits, partially supporting the general impression that secondary sexual characters are more variable among species than ordinary morphological characters. However, the degree of divergence among secondary sexual characters was generally not much larger than that among ordinary characters. Some non-significant differences in divergence between secondary sexual characters and ordinary characters could be explained by the cost-reducing function of ordinary morphological traits. There was no evidence of significant differences in divergence between sexes for secondary sexual characters, maybe because of genetic correlations in morphology between the sexes. However, male tarsi diverged more than female tarsi, and sexual selection might play a role in this difference in divergence. This revised version was published online in July 2006 with corrections to the Cover Date.     

Components of phenotypic variation in avian ornamental and non-ornamental feathers

Phenotypic variation, measured as the coefficient of variation (CV), is usually larger in secondary sexual characters than in ordinary morphological traits. We tested if intraspecific differences in the CV between ornamental and non-ornamental feather traits in 67 evolutionary events of feather ornamentation in birds were due to differences in (1) the allometric pattern (slope of the regression line when regressing trait size on an indicator of body size), or (2) the dispersion of observations around the regression line. We found that only dispersion of observations around the regression line contributed significantly to total variation. A large dispersion of observations around the regression line for ornamental feathers is consistent with these characters showing condition-dependence, supporting indicator models of sexual selection more strongly than a pure Fisher process. Ornamental feathers in males demonstrated negative allometry when regressed on tarsus length, which is a measure of skeletal body size. This finding is consistent with ornamental feather traits being subject to directional selection due to female mate preferences, where large body size is less important than in male–male competition. This pattern of phenotypic variation for avian secondary sexual characters contrasts with patterns of variation for insect genitalia, supposedly subject to sexual selection, since the latter traits only differ from ordinary morphology traits in allometry coefficient. The prevailing regime of selection (directional or stabilizing) and the effects of environmental factors are proposed to account for these differences among traits.     

Domesticated birds as a model for the genetics of speciation by sexual selection

In theory, even populations occupying identical environments can diverge in sexually selected traits, as a consequence of different mutational input. I evaluate the potential of this process by comparing the genetics of breeds of domesticated birds to what is known about the genetics of differences among species. Within domesticated species there is a strong correlation of time since domestication with the number of breeds. Descendants of the rock dove, Columba livia (the oldest domesticate) show differences in courtship, vocalizations, body shape, feather ornaments (crests and tails) and colors and color patterns. When nine other domesticated species are included there is a striking hierarchy, with more recent domesticates having a nested subset of these traits: the youngest domesticated species have breeds distinguished only by color. This suggests that selection of new, visible, mutations is driving the process of breed diversification, with mutations that appeal to the breeder happening the most frequently in color. In crosses among related species, color, feather ornaments and many vocalizations and displays show both intermediate dominance and pure dominance. Although the number of loci affecting each of these traits is typically unknown, limited evidence of the genetics of species differences suggests that some differences are due to the substitution of single genes of major effect. While neither the genetics of breeds nor the genetics of species provide a perfect model for the genetics of speciation, similarities between the two are sufficiently striking to infer that major, visible, mutations can provide the impetus underlying new directions of sexual selection.     

Evolution of the structure of tail feathers: implications for the theory of sexual selection

Bird tails are extraordinarily variable in length and functionality. In some species, males have evolved exaggeratedly long tails as a result of sexual selection. Changes in tail length should be associated with changes in feather structure. The study of the evolution of feather structure in bird tails could give insight to understand the causes and means of evolution in relation to processes of sexual selection. In theory, three possible means of tail length evolution in relation to structural components might be expected: (1) a positive relationship between the increase in length and size of structural components maintaining the mechanical properties of the feather; (2) no relationship; that is, enlarging feather length without changes in the structural components; and (3) a negative relationship; that is, enlarging feather length by reducing structural components. These hypotheses were tested using phylogenetic analyses to examine changes in both degree of exaggeration in tail length and structural characteristics of tail feathers (rachis width and density of barbs) in 36 species, including those dimorphic and nondimorphic in tail length. The degree of sexual dimorphism in tail length was negatively correlated with both rachis width and density of barbs in males but not in females. Reinforcing this result, we found that dimorphism in tail length was negatively associated with dimorphism in tail feather structure (rachis width and density of barbs). These results support the third hypothesis, in which the evolution of long feathers occurs at the expense of making them simpler and therefore less costly to produce. However, we do not know the effects of enfeeblement on the costs of bearing. If the total costs increased, the enfeeblement of feathers could be explained as a reinforcement of the honesty of the signal. Alternatively, if total costs were reduced, the strategy could be explained by cheating processes. The study of female preferences for fragile tail feathers is essential to test these two hypotheses. Preferences for fragile tails would support the evolution of reinforcement of honesty, whereas female indifference would indicate the existence of cheating in certain stages of the evolutionary process.     

A test of the Darwin–Fisher theory for the evolution of male secondary sexual traits in monogamous birds

The Darwin–Fisher theory proposes that the presence of male secondary sexual traits in monogamous birds is selected for by early season breeding of females that are in good condition. These early breeding females have high fecundity because of their good condition, and they select mates based on secondary sex traits. We tested whether this hypothesis may be responsible for the presence of male sexual ornaments in the great frigatebird, a socially and genetically monogamous seabird. Consistent with the Darwin–Fisher theory, we found that reproductive success declined over the season. However, males with more exaggerated ornaments were not chosen as mates earlier in the season than males with less exaggerated ornaments, and selection gradients on these ornaments were not significantly different from zero.     

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.     

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 fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

No evidence that sexual selection is an 'engine of speciation' in birds

Abstract Sexual selection has been implicated as having a role in promoting speciation, as it should increase the rate of evolution of reproductive isolation, and there is some comparative evidence that sexual selection may be related to imbalances in clade size seen in resolved phylogenies. By employing a new comparative method we are able to investigate the role of sexual selection in explaining the patterns of species richness across birds. We used data for testes size as an index of post‐mating sexual selection, and sexual size dimorphism and sexual dichromatism as indices of pre‐mating sexual selection. These measures were obtained for 1031 species representing 467 genera. None of the variables investigated explained the patterns of species richness. As sexual selection may also increase extinction rates, the net effect on species richness in any given clade will depend on the balancing effects of sexual selection upon speciation and extinction rates. We suggest that variance across clades in this balance may have resulted in the lack of a relationship between species richness and sexual selection seen in birds.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird

Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state- and context-specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition-dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus)--a species that develops a new sexual ornament once a year after breeding. Throughout males' lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season--males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post-juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition-dependence of ornamentation sharply decreased throughout a male's lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context-dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a male's life.     

Correlates of timing of spring migration in birds: a comparative study of trans-Saharan migrants

The evolution of migratory strategies in birds is likely to have been influenced by ecological as well as socio-sexual factors in both wintering and breeding areas. In this comparative study, we analysed timing of spring passage of 38 long-distance migratory bird species that winter south of the Sahara desert and breed in Europe, in relation to wintering and breeding latitudes, moult strategy, nesting site (open vs. cavity), and sexual dimorphism in size and coloration, which may reflect intensity of sexual selection. We employed a large data set consisting of more than 190 000 individuals ringed during spring migration in the Mediterranean Sea. We found that the species that migrated earlier were those wintering farther north, nesting in cavities and showing the largest degree of sexual size dimorphism (SSD). However, sexual dichromatism was not related to migration date. Among passerine species, moulting wing-feathers in Africa delayed migration. We found no support for the energetic constraint hypothesis, which proposes that early arrival selects for large male size, since early arriving species were not larger than late arriving ones. Thus, the observed associations suggest that variation in migration schedules at the interspecific level may have evolved in relation to ecological factors and SSD, possibly reflecting the intensity of mating competition.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 199–210.     

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.     

Diversity and evolution of male secondary sexual characters in African squeakers and long-fingered frogs

The African frog genera Arthroleptis and Cardioglossa are unique among vertebrates in having males with extremely long third fingers. In some species, this sexual dimorphism is impressive, with male third fingers approaching 40% of body length. However, the diversity of this trait has not been documented thoroughly and several species appear to lack this trait. The present study documents the diversity of male secondary sexual traits in Arthroleptis and Cardioglossa , including elongate third fingers and digital and inguinal spines. Furthermore, it explores hypotheses of trait evolution, including explanations for the absence of male traits. Analyses of covariance suggest that the functional relationship between finger length and snout–vent length (SVL), both within and among species, is different for male finger III than for male fingers I, II, and IV, or for female finger III. Ancestral state reconstruction suggests that all male traits were present in the most recent common ancestor of Arthroleptis and Cardioglossa and that reduction or loss of traits occurred later. Across species, independent contrast analyses find no correlation between SVL and either male relative third digit length or dimorphism in relative third digit length. The number of spines on male fingers II and III are positively correlated but spine number is not correlated with SVL and only weakly correlated with relative third digit length. The diversity of male traits is evolutionarily labile and is not explained by simple hypotheses of character evolution. Arthroleptis and Cardioglossa may thus provide an interesting study system for understanding how changes in sexual selection forces produce male trait diversity.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 553–573.     

Sexual selection for size and symmetry in a diversifying secondary sexual character in Drosophila bipectinata Duda (Diptera: Drosophilidae)

Results of intrapopulation studies of sexual selection and genetic variation and covariation underlying elements of the sex comb of Drosophila bipectinata are presented. The magnitude of the sex comb, a sexual ornament, varies significantly among Australasian populations, motivating research into the evolutionary mechanisms responsible for its incipient diversification. The comb is composed of stout black teeth on the front legs of males arranged in three distinct segments: C1, C2, and C3. Significant sexual selection in field populations in northeastern Queensland, Australia, was detected for increasing C2 and body size, and simultaneously for reducing comb positional fluctuating asymmetry. In contrast, sexual selection was not detected for other comb segments, nor for sternopleural bristle number or symmetry. Selection intensities for C2 and comb positional fluctuating asymmetry were similar in magnitude, and although they were opposite in sign, values across twelve sampling dates, or selection episodes, were uncorrelated. Heritability estimates for C2 were high and significant across years, whereas heritability estimates for comb positional asymmetry were small, and generally nonsignificant. The major sex comb segments (C1 and C2) were significantly and positively correlated genetically, indicating the potential for correlated evolution of these components of the comb under sexual selection. The original finding of a significant positive genetic correlation between the magnitude of this sex trait and its positional asymmetry indicates that the counteracting and independent selection pressures detected could contribute to the maintenance of genetic variation sustaining sexual selection. The study documents the simultaneous presence of sexual selection in nature and of heritable genetic variation underlying expression of the sex comb, fundamental conditions necessary for its adaptive diversification. Drosophila bipectinata may be a valuable model for studies of adaptive diversification and incipient speciation by sexual selection.     

Developmental instability as phenodeviance in a secondary sexual trait increases sharply with thermal stress

Abstract We test for effects of thermal stress applied to pupal flies from Noumea (New Caledonia) and Taipei (Taiwan) on developmental instability (DI) in the male sex comb of Drosophila bipectinata, as well as on pre‐adult survivorship and adult body size. The temperature treatments were Low (25 °C), High (29 °C) and Variable (18 h at 29 °C, 6 h at 34 °C). Although the Variable treatment reduced survivorship and body size, absolute comb size and fluctuating asymmetry generally were invariant across treatments. In contrast, comb phenodeviance increased with stress in both populations. Phenodeviance in one comb segment (C2) increased sharply with stress, whereas phenodeviance in a second major segment (C1) also increased with stress but only in Noumea flies. A major conclusion is that phenodeviations induced in a secondary sexual trait reflect the developmental environment that also damages fitness components, a foundation stone of the hypothesis that expressions of DI reveal phenotypic quality in sexual selection.     

Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants

Characters in animals used in signalling and subjected to strong directional selection often demonstrate (i) an elevated level of fluctuating asymmetry (small random deviations from bilateral symmetry) and (ii) a negative relationship between the degree of individual fluctuating asymmetry and the size of a given character. We tested these two predictions in plants since flowers are subjected to strong directional selection and are involved in signalling to pollinators, whereas leaves are supposed not to be directly involved in signalling. The overall level of fluctuating asymmetry in a number of plant species with bilaterally or radially symmetric flowers was not generally higher in floral traits than in leaves. The level of fluctuating asymmetry in plants was sometimes significantly consistent within individuals. The absolute degree of individual fluctuating asymmetry in floral traits was generally negatively related to the size of the trait, while there was a positive relationship for leaves. The degree of individual fluctuating asymmetry in floral traits was marginally negatively related to the degree of individual fluctuating asymmetry in leaf traits. These patterns of fluctuating asymmetry in plants suggest that (i) the degree of asymmetry in flowers signals different aspects of quality than does the degree of asymmetry in leaves, and that (ii) fluctuating asymmetry in flowers often reflects the phenotypic quality of individual plants.     

The large X‐effect on secondary sexual characters and the genetics of variation in sex comb tooth number in Drosophila subobscura

Genetic studies of secondary sexual traits provide insights into whether and how selection drove their divergence among populations, and these studies often focus on the fraction of variation attributable to genes on the X‐chromosome. However, such studies may sometimes misinterpret the amount of variation attributable to the X‐chromosome if using only simple reciprocal F₁ crosses, or they may presume sexual selection has affected the observed phenotypic variation. We examined the genetics of a secondary sexual trait, male sex comb size, in Drosophila subobscura. This species bears unusually large sex combs for its species group, and therefore, this trait may be a good candidate for having been affected by natural or sexual selection. We observed significant heritable variation in number of teeth of the distal sex comb across strains. While reciprocal F₁ crosses seemed to implicate a disproportionate X‐chromosome effect, further examination in the F₂ progeny showed that transgressive autosomal effects inflated the estimate of variation associated with the X‐chromosome in the F₁. Instead, the X‐chromosome appears to confer the smallest contribution of all major chromosomes to the observed phenotypic variation. Further, we failed to detect effects on copulation latency or duration associated with the observed phenotypic variation. Overall, this study presents an examination of the genetics underlying segregating phenotypic variation within species and illustrates two common pitfalls associated with some past studies of the genetic basis of secondary sexual traits.     

Colourful traits in female birds relate to individual condition,reproductive performance and male-mate preferences: a meta-analytic approach

Colourful traits in females are suggested to have evolved and be maintained by sexual selection. Although several studies have evaluated this idea, support is still equivocal. Evidence has been compiled in reviews, and a handful of quantitative syntheses has explored cumulative support for the link between condition and specific colour traits in males and females. However, understanding the potential function of females'' colourful traits in sexual communication has not been the primary focus of any of those previous studies. Here, using a meta-analytic approach, we find that evidence from empirical studies in birds supports the idea that colourful female ornaments are positively associated with residual mass and immune response, clutch size and male-mate preferences. Hence, colourful traits in female birds likely evolved and are maintained by sexual selection as condition-dependent signals.