Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Bill colour and immunocompetence in the European blackbird

The level of expression of secondary sexual characters has been suggested to signal male ability to resist parasitic infestations. To test this idea, several studies have examined the link between sexual signals and immunocompetence in birds. However, most of them have used only a single aspect of immune response to evaluate immunocompetence. We investigated the relation between bill colour and immunocompetence in captive male European blackbirds, Turdus merula, during the breeding season by assessing both cell-mediated and humoral components of the immune system. The blackbird is a sexually dimorphic species with bill colour varying from yellow to orange in males. Humoral immunity was assessed by measuring both primary and secondary responses to sheep red blood cell inoculation. Cell-mediated immunity was estimated with a delayed cutaneous hypersensitivity response to an injection of a mitogen (phytohaemagglutinin). No relation was found between male bill colour and the primary humoral response. However, males with orange bills showed a lower secondary humoral response but a higher cell-mediated immune response than males with yellow bills. Thus, the relation between immunocompetence and a secondary sexual trait may differ markedly depending on which component of the immune system is under consideration. We discuss our results in relation to mechanisms involved in sexual selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Is natural selection promoting sexual dimorphism in the Green-backed Firecrown Hummingbird ( Sephanoides Sephaniodes )?

In many hummingbird species there is an opposite pattern of sexual dimorphism in bill length and other morphometric measures of body size. These differences seem to be closely related with differences in foraging ecology directly associated with a different resource exploitation strategy. The aim of this study was to assess if natural selection is acting on wing length and bill size in hummingbird males and females with different resource exploitation strategies (i.e., territorial males and non-territorial females). If competition for resources promotes sexual dimorphism as a selective pressure, males should be subjected to negative directional selection pressure for wing length and no selection pressure over bill size, while females should undergo positive directional selection pressure for both bill size and wing length. The morphometric data we collected suggests that there is no selection for wing length and bill size in male hummingbirds. In contrast, our females exhibited positive directional selection for both wing length and bill size. Although we cannot reject sexual selection acting on sexually dimorphic traits, this study suggests that natural selection may promote sexual dimorphism in traits that are closely related with hummingbird foraging ecology and resource exploitation strategies.     

Stabilizing survival selection on presenescent expression of a sexual ornament followed by a terminal decline

Senescence is a decrease in functional capacity, increasing mortality rate with age. Sexual signals indicate functional capacity, because costs of ornamentation ensure signal honesty, and are therefore expected to senesce, tracking physiological deterioration and mortality. For sexual traits, mixed associations with age and positive associations with life expectancy have been reported. However, whether these associations are caused by selective disappearance and/or within‐individual senescence of sexual signals, respectively, is not known. We previously reported that zebra finches with redder bills had greater life expectancy, based on a single bill colour measurement per individual. We here extend this analysis using longitudinal data and show that this finding is attributable to terminal declines in bill redness in the year before death, with no detectable change in presenescent redness. Additionally, there was a quadratic relationship between presenescent bill colouration and survival: individuals with intermediate bill redness have maximum survival prospects. This may reflect that redder individuals overinvest in colouration and/or associated physiological changes, while below‐average bill redness probably reflects poorer phenotypic quality. Together, this pattern suggests that bill colouration is defended against physiological deterioration, because of mate attraction benefits, or that physiological deterioration is not a gradual process, but accelerates sharply prior to death. We discuss these possibilities in the context of the reliability theory of ageing and sexual selection.     

Sexual selection and genetic colour polymorphisms in animals

Genetic colour polymorphisms are widespread across animals and often subjected to complex selection regimes. Traditionally, colour morphs were used as simple visual markers to measure allele frequency changes in nature, selection, population divergence and speciation. With advances in sequencing technology and analysis methods, several model systems are emerging where the molecular targets of selection are being described. Here, we discuss recent studies on the genetics of sexually selected colour polymorphisms, aiming at (i) reviewing the evidence of sexual selection on colour polymorphisms, (ii) highlighting the genetic architecture, molecular and developmental basis underlying phenotypic colour diversification and (iii) discuss how the maintenance of such polymorphisms might be facilitated or constrained by these. Studies of the genetic architecture of colour polymorphism point towards the importance of tight clustering of colour loci with other trait loci, such as in the case of inversions and supergene structures. Other interesting findings include linkage between colour loci and mate preferences or sex determination, and the role of introgression and regulatory variation in fuelling polymorphisms. We highlight that more studies are needed that explicitly integrate fitness consequences of sexual selection on colour with the underlying molecular targets of colour to gain insights into the evolutionary consequences of sexual selection on polymorphism maintenance.     

Male bill colour and competition in zebra finches

Several studies have assessed the role of bill colour in sexual selection and especially with respect to sexual preferences. Even though there are indications that bill colour is related to male quality, so far it has not been shown that bill colour influences male-male interaction. We used male zebra finches with artificially coloured bills in a competitive context to measure the effect of bill colour. In these tests the experimental bird could choose between two feeding sites, each near a stimulus bird with a different bill colour. We tested orange against red, no bird against orange/red and orange/red against green respectively. We found no difference in behaviour towards an orange compared to a red billed stimulus. However the birds spent relatively more time eating when alone compared to being close to a potential competitor. In addition, more time was spent eating than on other behaviours when the birds were close to the orange/red billed stimulus compared to the green billed stimulus. So, although no effect was found in the orange against red test, the results suggest that bill colour may play some role in male-male interaction.     

Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.     

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.     

Selection underlies phenotypic divergence in the insular Azores woodpigeon

The study of phenotypic evolution in island birds following colonization is a classic topic in island biogeography. However, few studies explicitly test for the role of selection in shaping trait evolution in these taxa. Here, we studied the Azores woodpigeon (Columba palumbus azorica) to investigate differences between island and mainland populations, between females and males, and interactions between geographical origin and sex, by using spectrophotometry to quantify plumage colour and linear measurements to examine external and skeletal morphology. We further tested if selection explains the observed patterns by comparing phenotypic differentiation to genome‐wide neutral differentiation. Our findings are consistent with several predictions of morphological evolution in island birds, namely differences in bill, flight and leg morphology and coloration differences between island and mainland birds. Interestingly, some plumage and morphological traits that differ between females and males respond differently according to geographical origin. Sexual dimorphism in colour saturation is more pronounced in the mainland, but this is driven by selection on female plumage coloration. Differences in flight morphology between females and males are also more pronounced in the mainland, possibly to accommodate contrasting pressures between migration and flight displays. Overall, our results suggest that phenotypic differentiation between mainland and island populations leading to divergent sexual dimorphism patterns can arise from selection acting on both females and males on traits that are likely under the influence of natural and sexual selection.     

Assortative mating,sexual size dimorphism and sex determination in a seabird with plumage polymorphism

Intraspecific plumage polymorphism in seabirds is often attributed to advantages in foraging activities and escape from predators, but its role in sexual selection is not well understood. The Trindade petrel (Pterodroma arminjoniana) presents morphs varying from pale to whole dark, with no apparent sexual size dimorphism (SSD). We tested assortative mating in Trindade petrels based on plumage colours and body size. In addition, genders of Trindade petrels were identified molecularly aiming to test SSD based on morphometrics, which was also used to generate a discriminant function for sex assignment. Within-pair consistency in plumage colour (i.e. birds paired with mates of the same morph) was detected in 9 out of 10 pairs, but not in morphometric traits. Minimum bill depth and bill depth at unguis were traits significantly larger in males. The best model was adjusted with Bill depth at unguis, wing chord and body mass, with global discriminatory power of 78.4%. Our results suggest that plumage colours may be sexually selected in Trindade petrels, which brings evolutionary implications on the persistence of plumage polymorphism. Discriminatory power of the best discriminant function was similar to those found in other Procellariiformes and also among datasets obtained by distinct researchers, demonstrating its robustness.     

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre‐reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency‐dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency‐independent pre‐reproductive selection that operate earlier during ontogeny of these female morphs.     

Evolutionary consequences of human disturbance in a rainforest bird species from Central Africa

Relatively little attention has been directed towards understanding the impacts of human disturbance on evolutionary processes that produce and maintain biodiversity. Here, we examine the influence of anthropogenic habitat changes on traits typically associated with natural and sexual selection in the little greenbul (Andropadus virens), an African rainforest bird species. Using satellite remote-sensing and field survey data, we classified habitats into nonhuman-altered mature and human-altered secondary forest. Mature rainforest consisted of pristine rainforest, with little or no human influence, and secondary forest was characterized by plantations of coffee and cacao and high human impacts. Andropadus virens abundance was higher in secondary forest, and populations inhabiting mature rainforest were significantly larger in wing and tarsus length and bill size; characters often correlated with fitness. To assess the extent to which characters important in sexual section and mate choice might be influenced by habitat change, we also examined differences in plumage colour and song. Plumage colour and the variance in plumage luminance were found to differ between forest types, and song duration was found to be significantly longer in mature forest. The possible adaptive significance of these differences in traits is discussed. Despite relatively high levels of gene flow across habitats, amplified fragment length polymorphism analysis revealed that a small proportion of high-F(ST) loci differentiated mature from secondary forest populations. These loci were significant outliers against neutral expectations in a simulation analysis, suggesting a role for divergent selection in differentiation across habitats. A distance-based redundancy analysis further showed that forest type as defined by remote-sensing variables was significantly associated with genetic dissimilarities between habitats, even when controlling for distance. The observed shifts in morphology, plumage and song were consistent with divergent selection on heritable variation, but a role for plasticity cannot be ruled out. Results suggest that anthropogenic habitat changes may have evolutionary consequences, with implications for conservation and restoration.     

Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly

Although colour polymorphisms in adult organisms of many taxa are often adaptive in the context of sexual selection or predation, genetic correlations between colour and other phenotypic traits expressed early in ontogeny could also play an important role in polymorphic systems. We studied phenotypic and genetic variation in development time among female colour morphs in the polymorphic damselfly Ischnura elegans in the field and by raising larvae in a common laboratory environment. In the field, the three different female morphs emerged at different times. Among laboratory-raised families, we found evidence of a significant correlation between maternal morph and larval development time in both sexes. This suggests that the phenotypic correlation between morph and emergence time in the field has a parallel in a genetic correlation between maternal colour and offspring development time. Maternal colour morph frequencies could thus potentially change as correlated responses to selection on larval emergence dates. The similar genetic correlation in male offspring suggests that sex-limitation in this system is incomplete, which may lead to an ontogenetic sexual conflict between selection for early male emergence (protandry) and emergence times associated with maternal morph.     

A test of a corollary of Allen's rule suggests a role for population density

A body of research by Russell Greenberg, Glenn Tattersall and their colleagues has proposed a corollary of Allen's Rule: that in freshwater‐limited environments, bill surface area increases with temperature. Increases in both population density and sexual dimorphism, however, could also explain increases in bill surface area. After controlling for the effects of a hybrid zone, we tested whether temperature or population density in the saltmarsh sparrow Ammospiza caudacuta, a sexually monomorphic estuarine specialist, explained greater variance in bill surface area. This allowed us to examine multiple potential selective mechanisms underlying the Greenberg–Tattersall corollary. We found that saltmarsh sparrows follow the general pattern of the corollary (larger bills in warmer summer climates) but only after controlling for population density. The relationship between bill surface area and temperature varied inversely with population density. We discuss the relative abilities of sexual selection and ecological competition to explain these results.     

The evolution of sexual size dimorphism in the house finch. III. Developmental basis

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.     

Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards

Female mate choice is often based on exaggerated sexual traits, signals of male qualities that females cannot assess directly. Two such key qualities are male immune and/or sexual competence, whereby honesty in signalling could be maintained by physiological trade-offs. Carotenoid-based ornaments likely constitute such honest signals, as there is direct competition for (limited) carotenoids between ornament deposition and anti-oxidant support of immune or sperm functioning. Using spectrometry, we assessed the potential signalling function of the yellow, carotenoid-based colour of the bill of male mallards, a target of female mate choice. Here we demonstrate that bill reflectance varied with plasma carotenoid level, indicating antioxidant reserves. Moreover, lower relative UV reflectance during autumn pairing predicted immune responsiveness and correlated positively with sperm velocity during breeding, a trait that affects fertility. Our data provide support for current theories that females could use carotenoid-based sexual signals to detect immune vigour and fertilizing ability of prospective mates.     

Seasonal dimorphism in the horny bills of sparrows

Bill size is often viewed as a species‐specific adaptation for feeding, but it sometimes varies between sexes, suggesting that sexual selection or intersexual competition may also be important. Hypotheses to explain sexual dimorphism in avian bill size include divergence in feeding niche or thermoregulatory demands, intrasexual selection based on increased competition among males, or female preference. Birds also show seasonal changes in bill size due to shifts in the balance between growth rate and wear, which may be due to diet or endogenous rhythms in growth. Insight into the function of dimorphism can be gained using the novel approach of digital x‐ray imaging of museum skins to examine the degree to which the skeletal core or the rhamphotheca contribute to overall dimorphism. The rhamphotheca is ever‐growing and ever‐wearing, varying in size throughout life; whereas the skeletal core shows determinant growth. Because tidal marsh sparrows are more dimorphic in bill size than related taxa, we selected two marsh taxa to investigate dimorphism and seasonality in the size of the overall bill, the skeletal core, and the rhamphotheca. Bill size varied by sex and season, with males having larger bills than females, and bill size increasing from nonbreeding to breeding season more in males. Skeletal bill size varied with season, but not sex. The rhamphotheca varied primarily with sex; males had a larger rhamphotheca (corrected for skeletal bill size), which showed a greater seasonal increase than females. The rhamphotheca, rather than the skeletal bill, was responsible for sexual dimorphism in overall bill size, which was particularly well developed in the breeding season. The size of the rhamphotheca may be a condition‐based character that is shaped by sexual selection. These results are consistent with the evidence that bill size is influenced by sexual selection as well as trophic ecology.     

Condition-dependent expression of red colour differs between stickleback species

Sexual isolation may arise when male mating traits and female preferences differ between species. Such divergence in mating traits is likely to occur when the strength or targets of sexual selection differ. Therefore, by comparing the traits under sexual selection in closely related species and the nature of preference for those traits, we can gain insight into when sexual selection contributes to sexual isolation and how it does so. Collecting these data is no easy undertaking. To simplify this comparison, I use the presence and extent of condition dependence in traits to determine whether directional sexual selection is acting on them. Condition dependence thus serves as a signature of sexual selection. I investigate differences in sexual selection on red nuptial colour in limnetic-benthic species pairs of three-spined sticklebacks. I evaluate condition dependence by comparing the strength of the relationship between colour and condition, and the magnitude of variance in red nuptial colour to other colour traits and to nonsexual traits. I find that limnetic males have strong condition-dependent expression of red nuptial colour whereas benthic males have at most weak condition-dependent expression. Ancestral anadromous males show no condition dependence. This suggests that colour is under strong directional sexual selection only in limnetics and that this is the derived state. Moreover, I find that the strength of female preference for red is related to the extent of condition dependence. The extent of condition dependence is also associated with the importance of colour differences to mate recognition. These results show that differences between these species in the action of sexual selection underlie their sexual isolation.     

Covariation between bill colouration and fitness components in a nocturnal bird

Vividly coloured chromatic signals play a key role in social and sexual signalling in diurnal birds, but their role is considered negligible in favour of achromatic (i.e. white, pure grey and black colourations) signals in nocturnal species. Here we studied colour variation and potential signalling of the yellow bill – a trait functioning as sexual signal in diurnal raptors during the breeding season in females of a truly nocturnal raptor, the little owl Athene noctua. We found that yellow‐red chroma of the bill was highly variable between individuals and positively correlated with female fitness prospects (i.e. brood size at fledging). In addition, we found that females with brighter bills were larger in size and produced owlets with a higher mass at fledging. This study suggests that yellow bill colouration in female little owls may potentially play a role in sexual signalling and may constitute the first evidence of chromatic colour signalling in a nocturnal bird.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.