Carry‐over effects of conditions at the wintering grounds on breeding plumage signals in a migratory bird: roles of phenotypic plasticity and selection

To understand the consequences of ever‐changing environment on the dynamics of phenotypic traits, distinguishing between selection processes and individual plasticity is crucial. We examined individual consistency/plasticity in several male secondary sexual traits expressed during the breeding season (white wing and forehead patch size, UV reflectance of white wing patch and dorsal melanin coloration) in a migratory pied flycatcher (Ficedula hypoleuca) population over an 11‐year period. Furthermore, we studied carry‐over effects of three environmental variables (NAO, a climatic index; NDVI, a vegetation index; and rainfall) at the wintering grounds (during prebreeding moult) on the expression of these breeding plumage traits of pied flycatcher males at individual and population levels. Whereas NAO correlates negatively with moisture in West Africa, NDVI correlates positively with primary production. Forehead patch size and melanin coloration were highly consistent within individuals among years, whereas the consistency of the other two traits was moderate. Wing patch size decreased with higher NAO and increased with higher rainfall and NDVI at the individual level. Interestingly, small‐patched males suffered lower survival during high NAO winters than large‐patched males, and vice versa during low NAO winters. These counteracting processes meant that the individual‐level change was masked at the population level where no relationship was found. Our results provide a good example of how variation in the phenotypic composition of a natural population can be a result of both environment‐dependent individual plasticity and short‐term microevolution. Moreover, when plasticity and viability selection operate simultaneously, their impacts on population composition may not be evident.     

Lifetime offspring production in relation to breeding lifespan, attractiveness, and mating status in male collared flycatchers

As a comprehensive fitness parameter, lifetime reproductive success (LRS) is influenced by many different environmental and genetic factors, among which longevity is one of the most important. These factors can be reflected in secondary sexual characters, which may affect the life histories of individuals via social relations with conspecifics. Facultative polygyny in birds is another conspicuous reproductive trait that potentially increases male reproductive success, but lifetime success data in relation to polygyny are scarce. Here, we used 17?years of breeding data to quantify the LRS of male collared flycatchers (Ficedula albicollis) on the basis of lifetime recruitment of offspring. Breeding lifespan showed a positive relationship with LRS, and it was also significantly associated with mean recruitment of offspring per breeding year. Body size and sexually selected forehead patch size did not predict the number of recruits. Polygyny was positively associated with LRS, but when we corrected for lifespan, this relationship disappeared. Our results demonstrate that the relationship between longevity and LRS is not explained by the higher number of reproductive attempts when living longer, and question the adaptive value of polygyny in this population. The lack of association between forehead patch size and recruitment suggests that forehead patch is a poor indicator of phenotypic quality in our birds.     

Sexual selection resulting from extrapair paternity in collared flycatchers

Extrapair paternity has been suggested to represent a potentially important source of sexual selection on male secondary sexual characters, particularly in birds with predominantly socially monogamous mating systems. However, relatively few studies have demonstrated sexual selection within single species by this mechanism, and there have been few attempts to assess the importance of extrapair paternity in relation to other mechanisms of sexual selection. We report estimates of sexual selection gradients on male secondary sexual plumage characters resulting from extrapair paternity in the collared flycatcher Ficedula albicollis, and compare the importance of this form of sexual selection with that resulting from variation in mate fecundity. Microsatellite genotyping revealed that 15% of nestlings, distributed nonrandomly among 33% of broods (N=79), were the result of extrapair copulations. Multivariate selection analyses revealed significant positive directional sexual selection on two uncorrelated secondary sexual characters in males (forehead and wing patch size) when fledgling number was used as the measure of fitness. When number of offspring recruiting to the breeding population was used as the measure of male fitness, selection on these traits appeared to be directional and stabilizing, respectively. Pairwise comparisons of cuckolded and cuckolding males revealed that males that sired young through extrapair copulations had wider forehead patches, and were paired to females that bred earlier, than the males that they cuckolded. Path analysis was used to partition selection on these traits into pathways via mate fecundity and sperm competition, and suggested that the sperm competition pathway accounted for between 64 and 90% of the total sexual selection via the two paths. The selection revealed in these analyses is relatively weak in comparison with many other measures of selection in natural populations. We offer some explanations for the relatively weak selection detected. Copyright 1999 The Association for the Study of Animal Behaviour.     

GENOTYPE-BY-ENVIRONMENT INTERACTIONS IN THE DETERMINATION OF THE SIZE OF A SECONDARY SEXUAL CHARACTER IN THE COLLARED FLYCATCHER (FICEDULA ALBICOLLIS)

Although genetic variation in characters closely related to fitness is expected to either become depleted by selection or masked by environmental variation, “good gene” models of sexual selection require moderate to high heritabilities of secondary sexual characters to explain the occurrence of costly female mate preferences. In this study, I investigated whether the estimated heritability of a condition-dependent secondary sexual character (i.e., the white forehead badge) in the collared flycatcher varied depending on environmental conditions experienced during offspring growth. The data were collected over a period of 14 years making it possible to exploit natural variation in natal conditions. In addition, natal conditions were experimentally altered through brood size manipulations. During unfavorable conditions caused by generally poor weather or experimentally enlarged brood size, no significant heritability based on father-sons regressions could be demonstrated (0.19 ? h² ? 0.27). In contrast, sons reared during years with favorable weather or in experimentally reduced broods significantly resembled their fathers (0.44 ? h² ? 0.65). In addition, the heritability estimates declined with increasing maternal age. The strong effect of natal environmental condition on the estimated heritability of forehead badge size suggests that the potential genetic benefit from mate choice vary according to environmental conditions (e.g., the benefit is reduced during unfavorable rearing conditions). Because sons reared during poor conditions have probably experienced a natal environment different from that experienced by their fathers, the low heritability estimates obtained under poor conditions seem to be caused by low additive genetic variation expressed in such environments and/or a low genetic correlation between the expression of the trait in the two different environments (i.e., good vs. bad). Both of these explanations imply the presence of genotype-by-environment interactions. If such interactions frequently affect the expression of secondary sexual characters, this may offer an explanation of the high heritabilites sometimes reported for such traits, despite their exposure to long-term directional selection.     

The effect of parental quality and malaria infection on nestling performance in the Collared Flycatcher (Ficedula albicollis)

Plumage ornamentation often signals the quality of males and, therefore, female birds may choose elaborately ornamented mates to increase their fitness. Such mate choice may confer both direct and indirect benefits to the offspring. Males with elaborate ornaments may provide good genes, which can result in better nestling growth, survival or resistance against parasitic infections. However, these males may also provision their offspring with more food or food of better quality, resulting in nestlings growing at a higher rate or fledging in better condition. In this study, we examined if there was an association between male ornamentation and malaria infection in Collared Flycatchers (Ficedula albicollis). We also investigated offspring performance in relation to malaria infection in the parents and the quality of the genetic and rearing fathers (assessed by the size of two secondary sexual characters) under simulated good and bad conditions (using brood size manipulation). We found that secondary sexual characters did not signal the ability of males to avoid parasitic infections, and malaria infection in the genetic and the rearing parents had no effect on nestling growth and fledging size. Our results do show, however, that it may be beneficial for the females to mate with males with a large forehead patch because wing feathers of nestlings reared by large-patched males grew at a higher rate. Fast feather growth can result in earlier fledging which, in turn, could improve nestling survival in highly variable environments or under strong nest predation.     

Sexual selection and conservation: a Palearctic-African perspective

Møller, A. Pape. 2000. Sexual selection and conservation: a Paleartic-African perspective. Ostrich 71 (1): 361

Sexual selection may give rise to an increased general level of stress, either because intense directional selection reduces the ability of individuals to control the stable development of their phenotype, or because extravagant secondary sexual characters by themselves impose stress on their bearers. Sexual selection often acts against individuals with deviant, asymmetric phenotypes, particularly if such phenotypic deviance occurs in secondary sexual characters. Such characters also appear to be more affected by adverse environmental conditions than ordinary morphological characters. Sexual selection may give rise to relatively large body size, exaggeration of costly secondary sexual characters, an overall increase in body size within a lineage, and an increased risk of extinction. Reduced stress resistance caused by intense sexual selection may contribute to this trend. In accordance with this hypothesis, introductions of birds to islands are more likely to fail if the species is sexually dichromatic. Species that have gone extinct worldwide and threatened species are also more often dichromatic than expected by chance. These observations suggest that sexual selection may increase the risks of extinction, and that highly sexually selected may birds deserve more attention in conservation.     

SEXUAL SELECTION AND SURVIVAL SELECTION ON WING COLORATION AND BODY SIZE IN THE RUBYSPOT DAMSELFLY HETAERINA AMERICANA

I review methodological problems that can lead to false evidence for selection on secondary sexual characters and present a study of selection in rubyspot damselflies (Hetaerina americana) that avoids these pitfalls. Male rubyspots have a large red spot on each wing that grows to a terminal size after sexual maturity. Selection gradient analyses revealed evidence for positive sexual and survival selection on both terminal wing spot size and body size. Phenotype manipulations confirmed that wing spot size was subject to direct sexual selection, but showed that the positive slope of survival on wing spot size was an indirect effect of selection on unmeasured traits. This study provides the strongest evidence yet for sexual selection on coloration in Odonata, but also provides clear examples of why phenotypic selection statistics must be calculated and interpreted cautiously.     

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.     

Rapid temporal change in the expression and age-related information content of a sexually selected trait

The expression of sexual signals is often phenotypically plastic and also evolves rapidly. Few studies have considered the possibility that proximate determination -- the pathway between genes and trait expression -- may also be subject to both phenotypic plasticity and evolutionary change. We examined long-term patterns in size, condition- and age-dependence, repeatability and heritability of forehead patch size, a sexually selected plumage trait in male collared flycatchers. We also estimated survival and sexual selection on the phenotypic value of the trait. Forehead patch size linearly declined during the 15 years, probably due to the significantly negative survival selection. In addition, the expression of genetic variation for the ornament apparently underwent an age-limited change, which implies a change in the information content of the signal to receivers. The persistent lack of condition-dependence makes phenotypic plasticity an unlikely explanation to our results. This raises the possibility of a microevolutionary change of both expression and proximate determination during the study period.     

The extent of variation in male song, wing and genital characters among allopatric Drosophila montana populations

Drosophila montana, a species of the Drosophila virilis group, has distributed around the northern hemisphere. Phylogeographic analyses of two North American and one Eurasian population of this species offer a good background for the studies on the extent of variation in phenotypic traits between populations as well as for tracing the selection pressures likely to play a role in character divergence. In the present paper, we studied variation in the male courtship song, wing and genital characters among flies from Colorado (USA), Vancouver (Canada) and Oulanka (Finland) populations. The phenotypic divergence among populations did not coincide with the extent of their genetic divergence, suggesting that the characters are not evolving neutrally. Divergence in phenotypic traits was especially high between the Colorado and Vancouver populations, which are closer to each other in terms of their mtDNA genotypes than they are to the Oulanka population. The males of the Colorado population showed high divergence especially in song traits and the males of the Vancouver population in wing characters. Among the male song traits, two characters known to be under sexual selection and a trait important in species recognition differed clearly between populations, implying a history of directional and/or diversifying rather than balancing selection. The population divergence in wing characters is likely to have been enhanced by natural selection associated with environmental factors, whereas the male genitalia traits may have been influenced by sexual selection and/or sexual conflict.     

POPULATION DIVERGENCE IN SEXUAL ORNAMENTS: THE WHITE FOREHEAD PATCH OF NORWEGIAN PIED FLYCATCHERS IS SMALL AND UNSEXY

Models of sexual selection suggest that populations may easily diverge in male secondary sexual characters. Studies of a Spanish population of the pied flycatcher, Ficedula hypoleuca, and a Swedish population of the closely related collared flycatcher, F. albicollis, have indicated that the white forehead patch of males is a sexually selected trait. We studied the white forehead patch of male pied flycatchers (n = 487) in a Norwegian population over seven years. Males with large forehead patches were in general more brightly colored, but patch height was not correlated to body mass, body size, or parasite loads. Conditions during the nestling period did not seem to influence patch height as an adult. Patch height increased slightly from the first to the second year as adults, but then remained relatively constant at higher ages. Patch height was not related to survival. Year-to-year changes showed that males who increased in patch height also increased in body mass, suggesting that expression of the forehead patch may be partly condition dependent. However, changes in body mass explained only a small proportion of the variance in patch height between males. Thus, patch height would not be a good indicator of male quality. Furthermore, patch size was also not related to male ability to feed nestlings, indicating that females would not obtain direct benefits by choosing males with large patches. However, patch height could be a Fisher trait, but this requires heritability and there was no significant father-son resemblance in patch height. Comparisons of the males visited by each female during the mate sampling period indicated that chosen males did not have larger forehead patches than rejected males. Experimental manipulation of patch height did not affect male mating success. These results indicate that females do not use patch size as a mate choice cue. Finally, patch height did not predict the outcome of male contests for nestboxes, suggesting that the forehead patch is not an intrasexually selected cue of status. Norwegian pied flycatchers have smaller forehead patches than both Spanish pied flycatchers and Swedish collared flycatchers. We suggest that this pattern may be explained by the lack of sexual selection on the forehead patch in the Norwegian population as compared to the other populations, where the patch is apparently sexually selected. We discuss possible reasons for these population divergences, such as female choice on an alternative secondary sexual character (general plumage color) and speciation among Ficedula flycatchers.     

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.     

The cost of secondary sexual characters and the evolution of cost-reducing traits

Secondary sexual traits are characterized by their exaggerated expression relative to homologous nonsexual characters in other species. All models of sexual selection assume that sex traits are costly to produce and maintain, and individuals with reduced costs of production and maintenance of secondary sexual characters would be at a selective advantage. A number of morphological, physiological and behavioural traits may have evolved as a result of their cost-reducing properties: (1) body size, which does not change throughout life, that allows certain individuals to develop exaggerated sex traits, (2) cost-reducing traits, such as muscle size, that improve with practice and (3) actual cost-reducing traits, such as wing size in birds with song flight, which are produced in advance of or simultaneously with the sex trait. Cost-reducing traits may coevolve with secondary sexual characters and allow more extreme sexual signalling than would otherwise have been possible in their absence or in reduced versions.     

The cost of secondary sexual characters and the evolution of cost-reducing traits

Secondary sexual traits are characterized by their exaggerated expression relative to homologous nonsexual characters in other species. All models of sexual selection assume that sex traits are costly to produce and maintain, and individuals with reduced costs of production and maintenance of secondary sexual characters would be at a selective advantage. A number of morphological, physiological and behavioural traits may have evolved as a result of their cost-reducing properties: (1) body size, which does not change throughout life, that allows certain individuals to develop exaggerated sex traits, (2) cost-reducing traits, such as muscle size, that improve with practice and (3) actual cost-reducing traits, such as wing size in birds with song flight, which are produced in advance of or simultaneously with the sex trait. Cost-reducing traits may coevolve with secondary sexual characters and allow more extreme sexual signalling than would otherwise have been possible in their absence or in reduced versions.     

Interspecific aggression causes negative selection on sexual characters

Interspecific aggression originating from mistaken species recognition may cause selection on secondary sexual characters, but this hypothesis has remained untested. Here we report a field experiment designed to test directly whether interspecific aggression causes selection on secondary sexual characters, wing spots, in wild damselfly populations. Males of Calopteryx virgo are more aggressive toward males of C. splendens with large than with small wing spots. This differential interspecific aggression may cause negative selection on wing spot size. Indeed, our results show that directional survival selection on wing spot size of C. splendens males was changed by experimental removal of C. virgo males. Without removal, directional selection went from positive to negative with increasing relative abundance of C. virgo males. In populations where C. virgo males were removed, this relationship disappeared. These results verify that interspecific aggression can cause negative selection on sexual characters. Thus, interspecific aggression has the potential to cause divergence on these characters between two species offering an alternative explanation for reinforcement for generating character displacement in secondary sexual characters.     

Testosterone levels in relation to size and UV reflectance of achromatic plumage traits of female pied flycatchers

In a substantial number of species, females show some development of secondary sexual characters. These traits can function as signals of individual phenotypic or genetic qualities and status to conspecifics. Individuals may benefit potentially from expressing signals or badges of status if they are reliable and honest signals of individual quality. In many species, badge sizes have been shown to correlate with dominance rank, which may be mediated by testosterone (T) levels. Here, we explored geographic variation in the size and properties of the white wing patch of female pied flycatchers Ficedula hypoleuca and its relation to circulating T levels in three populations (two southern populations in central Spain and a northern population in Finland). Furthermore, we aimed at detecting if the size of the white wing patch and its ultraviolet (UV) reflectance indicate individual quality. We found that females in Spain had larger, brighter and more UV reflecting wing patches than those in Finland. Females with higher UV reflectance and larger primary white patches bred earlier. Younger females and females with larger primary white wing patches showed higher T levels. In contrast, higher values of UV reflectance in feathers from these patches were associated with low T levels. Despite genetic differentiation and differences in trait expression between populations, female pied flycatchers from different populations may converge and use the size of white wing patches to signal their T levels and thereby their social dominance.     

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.     

Molecular population divergence and sexual selection on morphology in the banded demoiselle (Calopteryx splendens)

The importance of sexual selection in population divergence is of much interest, mainly because it is thought to cause reproductive isolation and hence could lead to speciation. Sexually selected traits have been hypothesized to diverge faster between populations than other traits, presumably because of differences in the strength, mechanism or dynamics of selection. We investigated this by quantifying population divergence in eight morphological characters in 12 south Swedish populations of a sexually dimorphic damselfly, the banded demoiselle (Calopteryx splendens). The morphological characters included a secondary sexual character, the male melanized wing spot, which has an important function in both inter- and intrasexual selection. In addition, we investigated molecular population divergence, revealed by amplified fragment length polymorphism (AFLP) analysis. Molecular population divergence was highly significant among these Northern European populations (overall F(st)=0.054; pairwise population F(st)'s ranged from approximately 0 to 0.13). We found evidence for isolation-by-distance (r=0.70) for the molecular markers and a significant correlation between molecular and phenotypic population divergence (r=0.39). One interpretation is that population divergence for the AFLP loci are affected by genetic drift, but is also indirectly influenced by selection, due to linkage with loci for the phenotypic traits. Field estimates of sexual and natural selection from two of the populations revealed fairly strong sexual selection on wing spot length, indicating that this trait has the potential to rapidly diverge, provided that variation is heritable and the observed selection is chronic.     

THE EVOLUTION OF SEXUAL DIMORPHISM BY SEXUAL SELECTION: THE SEPARATE EFFECTS OF INTRASEXUAL SELECTION AND INTERSEXUAL SELECTION

Libellula luctuosa, a pond dragonfly found in eastern North America, is apparently sexually dimorphic. Previous studies of the mating behavior in this species suggested that both male-male competition and female mate choice are important influences. Males compete for territories, where they attract females and where mating occurs. Female behavior influences both the copulation success and the fertilization success of males. Because of temporal and spatial separation of these episodes of sexual selection, multivariate and nonparametric statistical techniques could be used to investigate the influence of components of sexual selection on various sexually dimorphic traits. Sexual dimorphism in L. luctuosa was first quantified; then the direct effects and the form of selection were estimated. Sexually dimorphic wing size, body size, wing coloration, and body coloration are distributed either continuously or discontinuously between the sexes in L. luctuosa. These traits have apparently diverged between the sexes as a result of directional sexual selection. Body size is further influenced by stabilizing selection. Intrasexual selection (success in gaining access to a territory) and intersexual selection (success in copulation and fertilization) can influence the same or different sexually dimorphic characters. Body size is influenced by directional selection during the intrasexual phase of sexual selection and is also influenced by stabilizing selection during intersexual selection. The size of the brown wing patch is influenced by directional selection, primarily during the intersexual phase of sexual selection. There is directional selection on the white wing patch during both phases. Thus, the different proximate mechanisms of sexual selection may jointly or separately affect the evolution of sexually dimorphic characters. Further empirical and theoretical investigations into the differences in the effects of intrasexual selection and intersexual selection are needed to clarify the circumstances leading to separate consequences of these two mechanisms of sexual selection.