Ornament and body size variation and their measurement in natural populations

Measurement of intrapopulation variation in secondary sexual traits is a priority in the testing of sexual selection models. However, it is important to take care in the choice of materials and delimitation of populations. The use of museum skins to study variation in male tail ornaments may substantially underrepresent the real degree of intrapopulation variation. Data from live animals in specific areas provide more realistic estimates, and should be used whenever possible. I use as an example field data on male ornament length and body size in Vidua macroura (Aves: Ploceidae), a promiscuous, parasitic African finch with elongated tail plumes. Individual males differ in the timing and rate of ornament growth, and females are therefore faced with a large degree of phenotypic variation in male ornament size, even though genetic variation may not be great. By correcting for seasonal variation in the ornament lengths of males caught at different times, I show that mid-season coefficients of variation in ornament length of breeding males in two populations are as high as 18% and 55%. By contrast, tarsus, wing and unornamented tail lengths of the same males vary from 2 to 4%.     

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.     

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 allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.     

Timing of ornament growth, phenotypic variation, and size dimorphism in two promiscuous African whydahs (Ploceidae: Vidua)

Variation within populations is a prerequisite for the action of selection on morphological traits. Darwin assumed that there was much greater variation in sexual ornament size than in body size, but this may not be generally true of natural populations. I analyse field data on variation in body size and the length, area and mass of tail ornaments in paradise (Vidua paradisaea) and shaft-tailed whydahs (V. regia). Whydahs are promiscuous, brood parasitic African finches with elaborate tail ornaments in breeding males. The short, unadorned tails of male shaft-tailed whydahs, which carry a wire-like tail ornament, are non-significantly (1%) longer than female tails, but male paradise whydahs, which carry a large, broad ornament, have unadorned tails 10% longer than those of conspecific females. Fully grown ornament length, mass and area vary little more (CVs = 1.8-6.4%) than male or female body size traits (CVs = 1.7-6.1%). Instead, there is high variation in the timing of ornament development during prenuptial moult (CVs = 30.8–39.5% for paradise whydahs and 12.6–23.8% for shaft-tailed whydahs when corrected to a standard date). This temporal variation in development probably has greater significance for sexual selection in whydahs than maximum ornament size.     

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.     

Age-Dependent Expression of Song in the Collared Flycatcher, Ficedula albicollis

Theory suggests that male ornaments should be reliable signals of age, with more elaborated ornaments reflecting superior quality in terms of experience and/or viability. Bird song is immensely involved in sexual selection, thus not‐surprisingly, it usually shows age‐dependent variation. Although the collared flycatcher Ficedula albicollis has been intensively studied for its sexual traits, and female preference for male age is expected to be strong, there is no quantitative information on age‐dependent expression of song in this species. Here, we fill this gap and, based on phenotypic correlations, we report the relationship between age and several song features. Repertoire size was consistently smaller in yearlings than in older males, but it also tended to increase after the second year of breeding. In a meta‐analysis of effect sizes using data from the literature, we found that the strength of the relationship between age and repertoire size in the collared flycatcher is similar to patterns observed in other passerines. Song rate was inversely related to age, as yearlings sang at higher rates than older males. Generally, effect sizes for the relationship between age and other song traits were of medium level on average, and had broad confidence intervals. Song traits covaried with survival in a direction suggesting that differences in song between age categories are unlikely to result from phenotype dependent survival. Our results generally support the hypothesis that song holds the potential to function as a reliable indicator of male age in the collared flycatcher. However, it seems that not all song traits are unambiguously more expressed in older males than in yearlings.     

Patterns of morphological variation among cardueline finches (Fringillidae: Carduelinae)

Patterns of variation in five morphological traits in cardueline finches were analysed. Among species, bill characters were the most and tail length the least variable. Species differed primarily in terms of body size, whereas genera differed in terms of bill size. Cardueline finches were far less variable compared with the amount of variation expected under a model of neutral random drift. This indicates that this group of birds is under strong stabilizing selection pressure. This could conform to models of stasis where populations are thought to travel only between adjacent adaptive peaks separated by shallow valleys. Changes in body size are correlated with speciation, whereas changes in bill morphology are correlated with divergences leading to the erection of new genera.     

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.     

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.     

Forehead Patch Size Predicts the Outcome of Male–Male Competition in the Pied Flycatcher

Males of many animal species express ornaments that affect their reproduction opportunities through male–male competition or female mate choice. Such ornaments can, for example, inform conspecifics about the fighting ability, condition or territory ownership of the bearer. Pied flycatcher (Ficedula hypoleuca) males have a conspicuous white forehead patch that varies greatly in size. We examined whether the white forehead patch is an intrasexually selected trait in a Finnish population. We artificially manipulated forehead patch size to represent two naturally occurring extremes and competed males against each other in the presence of a female. Males with a large forehead patch were more aggressive than males with a small patch, whereas the original patch size of the male had no influence on aggression. Neither manipulated nor original patch size influenced resource dominance (over female or nest box). These results indicate that forehead patch signals fighting ability of the bearer in the pied flycatcher. The next step is to find out what kind of costs may maintain the honesty of this signal.     

Patterns of morphological and geographic variation in trophic bill morphs of the African finch Pyrenestes

Intra- and inter-population variability was studied in three species of tropical African estrildid finches comprising the genus Pyrenestes. Eleven characters were measured on P. ostrinus captured on a study area in Cameroon. Most of these same characters were also measured on museum specimens of this species and P. saguineus and P. minor. Data were analysed using univariate and multivariate statistical methods in order to characterize variation within and between populations and species.
Variation in all three species of Pyrenestes is greatest in bill size, resulting from an exceptional non-sex-linked polymorphism. Bill size differences between morphs are as high as between congeneric species, with extremely large coefficients of variation, while other body characters show comparatively little variation. Sexual dimorphisms and differences in size due to age occur, but contribute little to overall size variation. Distributions of bill characters in each age and sex class are bimodal or greatly skewed, and in some geographical regions tend to be trimodal. Distributions of other body characters tend not to be significantly different from normal. Bill morphs differ in both shape and size and may be separated using principal component analysis. Static allometries of bill morphs differ significantly: relative to body size, bill size increases more rapidly in the large morph. Bill size and shape also vary geographically. The three species differ in mean size but show much overlap. Bill size is negatively correlated with total annual rainfall. In regions characterized by ecotonal transition zones between forest and savanna, tentative evidence suggests that a third, yet larger bill mode occurs. This third mode apparently results from the presence of a distinct larger species of hard-seeded sedge found only in these regions. The taxonomic implications of the polymorphism are discussed.     

Haematocrit correlates with tail ornament size in three populations of the Barn Swallow (Hirundo rustica)

1. Handicap models of sexual selection propose that male ornaments are indicators of male quality and that honesty is enforced by the costs imposed by the exaggerated ornamental traits. In long-distance migratory birds that feed on the wing, the aerodynamic cost of exaggerated ornamental characters should be particularly high because the size of the ornaments deviates from the natural selection optimum. During migration, birds are expected to raise their oxygen consumption in relation to the energetic demands imposed by their morphology. An increase of haematocrit is an adaptive response to enhance oxygen uptake and efficiency of transfer to the muscular tissues during spells of intense muscular activity.
2. The change of haematocrit of Barn Swallows ( Hirundo rustica ) after their arrival to the breeding sites, and the relationships between haematocrit values recorded after migration and the size of ordinary and sexually selected morphological characters in three Barn Swallow populations were analysed.
3. Males had higher haematocrit values than females. Individual haematocrit values declined after arrival to the breeding sites. Haematocrit values of males were significantly and positively correlated with the size of their ornamental tail but not correlated with other characters, thus suggesting that well-ornamented males, in order to arrive early, have to raise their haematocrit above the level of short-tailed males.
4. Males and females of similar tail length did not differ in their haematocrit, thus suggesting that sexual dimorphism in haematocrit might be functionally related to dimorphism in tail length.
5. Our results are consistent with the handicap principle because long-tailed males experience lower mortality and larger seasonal reproductive success compared with short-tailed males.     

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.     

Environmental factors, regional body size distributions and spatial variation in body size of local avian assemblages

Aim To determine how well variation in median body size of avian assemblages is predicted by (1) the environmental models usually employed in analyses of Bergmann's rule and (2) random sampling from the regional body size frequency distribution. If body size frequency distributions of local assemblages represent a random sample of a regional frequency distribution, then geographical variation in body sizes of assemblages might be a consequence of the determinants of spatial variation in species richness rather than direct influences on body size per se. Location Southern Africa. Methods Median body masses (as a measure of body size) of avian assemblages were calculated for quarter‐degree grid cells across South Africa and Lesotho. The relationship between median body mass and four environmental variables (minimum and maximum monthly temperatures, precipitation and seasonality in the normalized difference vegetation index, as a measure of seasonality in productivity) was examined using general linear models first without taking spatial autocorrelation into account, and then accounting for it by fitting an exponential spatial covariance structure. Model fit was assessed using the Akaike information criterion and Akaike weights. At each species richness value, random assemblages were sampled by either drawing species randomly from the regional body mass frequency distribution, or drawing species from the regional body mass frequency distribution with a probability proportional to their geographical distribution in the area. The ability of randomizations to predict actual body masses was examined using two‐tailed Fisher exact tests. Results Seasonality in productivity was the only environmental variable that remained a significant predictor of body mass variation in spatially explicit models, though the positive relationship was weak. When species richness was included in the models it remained the only significant predictor of size variation. Randomizations predicted median body mass poorly at low species richness, but well at high richness. Main conclusions Environmental models that have previously been proposed explain little of the variation in body mass across avian assemblages in South Africa. However, much of the variation in the median mass of assemblages could be predicted by randomly drawing species from the regional body mass frequency distribution, particularly using randomizations in which all species were drawn from the regional body mass frequency distribution with equal probability and at high species richness values. This outcome emphasizes the need to consider null expectations in investigations of the geographical variation in body size together with the probable environmental mechanisms underlying spatial variation in average size. Moreover, it suggests that in the South African avifauna, spatial variation in the body sizes of assemblages may be determined indirectly by the factors that influence geographical variation in species richness.     

Body size variation and sexual size dimorphism across climatic gradients in the widespread treefrog Scinax fuscovarius (Anura,Hylidae)

Variation in body size represents one of the crucial raw materials for evolution. However, at present, it is still being debated what is the main factor affecting body size or if the final body size is the consequence of several factors acting synergistically. To evaluate this, widespread species seem to be suitable models because the different populations occur along a geographical gradient and under contrasted climatic and environmental conditions. Here we describe the spatial pattern of variation in body size and sexual size dimorphism in the snouted treefrog Scinax fuscovarius (Anura, Hylidae) along a 10° range in latitude, 25° longitude, and 2000 m in altitude from Argentina, Brazil and Paraguay using an information‐theoretic approach to evaluate the support of the data for eight a priori hypotheses proposed in the literature to account for geographical body size, and three hypotheses for sexual size dimorphism variation. Body size of S. fuscovarius varied most dramatically with longitude and less so with latitude; frogs were largest in the northwestern populations. Body size was positively related with precipitation seasonality, and negatively with annual precipitation. Furthermore, the degree of sexual size dimorphism was greatest in the western populations with less annual precipitation, as the increase in body size was stronger for females. Our results on body size variation are consistent with two ecogeographical hypotheses, the starvation resistance and the water availability hypotheses, while our results on sexual size dimorphism in S. fuscovarius supports the differential‐plasticity hypothesis but the inverse to Rensch's rule and the parental investment hypothesis. Due to the weak association between environmental variables and body size and sexual size dimorphism variation, we stress that there are other factors, mainly those related to the life history, driving the geographical variation of S. fuscovarius.     

Karyological and morphometric variation of the North African green frog Pelophylax saharicus (Anura) in northeastern Africa

Morphometric variation of Pelophylax saharicus was analysed using univariate and multivariate statistics, with both traditional and geometric morphometries, based on 148 specimens from four different geographical localities in Tunisia and Algeria. The results show the existence of three morphotypes in Tunisia and one in Algeria, and indicate a significant degree of variation in morphometric characters between regions. Specimens from the southernmost region have the smallest body size and the greatest morpho...     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

An investigation of mate choice based on manipulation of multiple ornaments in Kentish plovers

Many animals have multiple sexual ornaments, a fact variously explained as signalling of multiple attributes, or nonadaptive retention of now redundant, but previously informative, signals. Despite the widespread occurrence of multiple ornaments, and the theoretical interest in how they are maintained by selection, there have been few experimental studies of the phenomenon. We investigated the role of two ornaments, each plausibly signalling different male attributes, in attracting a new mate in the Kentish plover, Charadrius alexandrinus. Previously we have shown that male Kentish plovers vary in how long they take to acquire a new mate, and we hypothesized that this variation may relate to their attractiveness or parental ability. We created single males by removing their mate and clutch, and then manipulated both their badge size (a presumed signal of either their genetic quality or their dominance status and hence defensive abilities) and the length of their flank feathers (a presumed signal of their parental quality in incubation) in a 2×2 factorial design. We found no difference in remating times between manipulated and control males. Furthermore, neither body size nor body condition of males was related to their remating times, although males with enlarged badges spent less time fighting than control males. Taken together, our results suggest that female Kentish plovers do not use either badge size or the length of flank feathers as cues in their mate choice decisions. However, badge size may influence male-male competition.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.