Circadian clocks are centrally involved in the regulation of daily behavioural and physiological processes. These clocks are synchronized to the 24 h day by external cues (Zeitgeber), the most important of which is the light–dark cycle. In polar environments, however, the strength of the Zeitgeber is greatly reduced around the summer and winter solstices (continuous daylight or continuous darkness). How animals time their behaviour under such conditions has rarely been studied in the wild. Using a radio-telemetry-based system, we investigated daily activity rhythms under continuous daylight in Barrow, Alaska, throughout the breeding season in four bird species that differ in mating system and parental behaviour. We found substantial diversity in daily activity rhythms depending on species, sex and breeding stage. Individuals exhibited either robust, entrained 24 h activity cycles, were continuously active (arrhythmic) or showed ‘free-running’ activity cycles. In semipalmated sandpipers, a shorebird with biparental incubation, we show that the free-running rhythm is synchronized between pair mates. The diversity of diel time-keeping under continuous daylight emphasizes the plasticity of the circadian system, and the importance of the social and life-history context. Our results support the idea that circadian behaviour can be adaptively modified to enable species-specific time-keeping under polar conditions.
circadian clock; continuous daylight; mating system; arrhythmic activity; Arctic; Calidris
The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.
In vertebrates, including humans, the relative length of the second to the fourth digit correlates with sex hormone-dependent behavioural, psychological and physiological traits. However, despite a decade of research, the underlying mechanism linking digit ratio to these sex hormone-dependent traits remains unclear. Previous work suggests that during embryo development, circulating levels of plasma androgens or oestrogens may act through their receptors to affect transcription levels of posterior HOX genes in the developing digits, thereby possibly influencing their relative length. The correlation between digit ratio and sex hormone-dependent traits might thus stem from variation in expression or sensitivity of the sex hormone receptors, or from variation in sex hormone levels in the embryo. Here, we show that in a population of 1156 zebra finches Taeniopygia guttata, a polymorphism in the oestrogen receptor α gene (ESR1) explains 11.3 per cent of the variation in digit ratio, and is also associated with male and female-mating behaviour. By contrast, we found no associations between digit ratio or mating behaviours and polymorphisms in the androgen receptor gene. Thus, our results (i) provide an explanation for the observed significant genetic covariance between digit ratio and male and female mating behaviour and (ii) strongly confirm the indicator function of digit ratio through the oestrogen pathway. Finally, we note that the commonly invoked effect of foetal testosterone on human digit ratio seems to be substantially weaker than the effect described here.
2D : 4D; finger length; HOX genes; sexual behaviour; sex hormones
Bird migration is one of the most spectacular and best-studied phenomena in behavioural biology. Yet, while the patterns of variation in migratory behaviour and its ecological causes have been intensively studied, its genetic, physiological and neurological control remains poorly understood. The lack of knowledge of the molecular basis of migration is currently not only limiting our insight into the proximate control of migration, but also into its evolution. We investigated polymorphisms in the exons of six candidate genes for key behavioural traits potentially linked to migration, which had previously been identified in several bird species, and eight control loci in 14 populations of blackcaps (Sylvia atricapilla), representing the whole range of geographical variation in migration patterns found in this species, with the aim of identifying genes controlling variation in migration. We found a consistent association between a microsatellite polymorphism and migratory behaviour only at one candidate locus: the ADCYAP1 gene. This polymorphism explained about 2.6 per cent of the variation in migratory tendency among populations, and 2.7–3.5% of variation in migratory restlessness among individuals within two independent populations. In all tests, longer alleles were associated with higher migratory activity. The consistency of results among different populations and levels of analysis suggests that ADCYAP1 is one of the genes controlling the expression of migratory behaviour. Moreover, the multiple described functions of the gene product indicate that this gene might act at multiple levels modifying the shift between migratory and non-migratory states.
ADCYAP1; PACAP; migratory restlessness; bird migration; neuropeptide
Possibly due to the small size of the olfactory bulb (OB) as compared to rodents, it was generally believed that songbirds lack a well-developed sense of smell. This belief was recently revised by several studies showing that various bird species, including passerines, use olfaction in many respects of life. During courtship and nest building, male European starlings (Sturnus vulgaris) incorporate aromatic herbs that are rich in volatile compounds (e.g., milfoil, Achillea millefolium) into the nests and they use olfactory cues to identify these plants. Interestingly, European starlings show seasonal differences in their ability to respond to odour cues: odour sensitivity peaks during nest-building in the spring, but is almost non-existent during the non-breeding season.
This study used repeated in vivo Manganese-enhanced MRI to quantify for the first time possible seasonal changes in the anatomy and activity of the OB in starling brains. We demonstrated that the OB of the starling exhibits a functional seasonal plasticity of certain plant odour specificity and that the OB is only able to detect milfoil odour during the breeding season. Volumetric analysis showed that this seasonal change in activity is not linked to a change in OB volume. By subsequently experimentally elevating testosterone (T) in half of the males during the non-breeding season we showed that the OB volume was increased compared to controls.
By investigating the neural substrate of seasonal olfactory sensitivity changes we show that the starlings' OB loses its ability during the non-breeding season to detect a natural odour of a plant preferred as green nest material by male starlings. We found that testosterone, applied during the non-breeding season, does not restore the discriminatory ability of the OB but has an influence on its size.
GIS; Moran's I; spatial analysis
Although studies on the evolution and function of female ornaments have become more numerous in the last years, the majority of these studies were carried out in cases where female ornaments were a smaller and duller version of the ornaments found in males. There are substantially fewer studies on species with female-specific ornaments. However, no study so far investigated the potential of female-specific colouration as a quality signal in birds with conventional sex roles. We studied female-specific ornamentation in a strongly sexually dichromatic species, the upland goose Chloephaga picta leucoptera, in two consecutive years. Male upland geese have white head and breast feathers and black legs, whereas females have reddish-brown head and breast feathers and conspicuous yellow-orange legs. We found that female-specific colouration in upland geese can reliably indicate different aspects of female phenotypic quality. Females with more orange coloured legs and more red-like head colours had higher clutch and egg volumes than females with a paler leg and head colouration, and a more reddish plumage colouration was related to a higher body condition. These relationships provide the theoretic possibility for males to assess female phenotypic quality on the basis of colouration. Furthermore, the females with a more orange-like tarsus colouration had higher plasma carotenoid levels. Both tarsus colouration and carotenoid concentrations of individual females were highly correlated across years, indicating that tarsus colour is a stable signal. Despite this correlation, small individual differences in plasma carotenoid concentrations between the two study years were related to differences in tarsus colouration. We thus show for the first time in a wild bird and under natural conditions that carotenoid-based integument colouration remains consistent between individuals in consecutive years and is also a dynamic trait reflecting individual changes in carotenoid levels. In this species, where pairs form life-long bonds, the honesty of the carotenoid-based integument colouration suggests that it may be a sexually selected female ornament that has evolved through male mate choice.
Electronic supplementary material
The online version of this article (doi:10.1007/s00265-010-0990-4) contains supplementary material, which is available to authorized users.
Upland goose; Chloephaga picta leucoptera; Female-specific colouration; Signalling; Carotenoids; Individual quality
The honesty of ornamental signals of quality is often argued to be enforced via costs associated with testosterone. It is still poorly understood, however, how seasonal variation of testosterone within individuals is related to the timing and extent of ornament development. Here, we studied inter- and intra-individual variability of plasma testosterone levels in a population of 150 captive male house sparrows (Passer domesticus) through the course of a full year. We further analyzed the relationship between plasma testosterone levels and two sexually dimorphic ornaments: badge size and bill coloration. Also, because of a known negative relation between molt and circulating testosterone levels, we analyzed the relationship between ornamentation and molt status during the fall. We found that testosterone levels increased towards the breeding season and decreased before the onset of annual molt. However, within individuals, relative testosterone titers demonstrated low repeatability between seasons. Plasma testosterone levels were not correlated with badge size in any season but were correlated strongly with bill coloration during all periods, except the breeding season when variation in bill color was low. Finally, we found that bill coloration strongly correlated with molt status during fall. Our results indicate that bill coloration, not badge size, is the best ornamental indicator of a “running average” of male testosterone in house sparrows and therefore the best potential indicator of qualities and/or behavioral strategies associated with testosterone.
Badge size; Bill color; Honest signaling; Melanin; Strategy signals; Testosterone
In animals, competition for space and resources often results in territorial behaviour. The size of a territory is an important correlate of fitness and is primarily determined by the spatial distribution of resources and by interactions between competing individuals. Both of these determinants, alone or in interaction, could lead to spatial non-independence of territory size (i.e. spatial autocorrelation). We investigated the presence and magnitude of spatial autocorrelation (SAC) in territory size using Monte Carlo simulations of the most widely used territory measures. We found significant positive SAC in a wide array of competition-simulated conditions. A meta-analysis of territory size data showed that SAC is also a feature of territories mapped based on behavioural observations. Our results strongly suggest that SAC is an intrinsic trait of any territory measure. Hence, we recommend that appropriate statistical methods should be employed for the analysis of data sets where territory size is either a dependent or an explanatory variable.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-009-1509-4) contains supplementary material, which is available to authorized users.
Home range; Thiessen polygons; Dirichlet tessellation; Monte Carlo simulation; Bivariate kernel
The detection of odorants is mediated by olfactory receptors (ORs). ORs are G-protein coupled receptors that form a remarkably large protein superfamily in vertebrate genomes. We used data that became available through recent sequencing efforts of reptilian and avian genomes to identify the complete OR gene repertoires in a lizard, the green anole (Anolis carolinensis), and in two birds, the chicken (Gallus gallus) and the zebra finch (Taeniopygia guttata).
We identified 156 green anole OR genes, including 42 pseudogenes. The OR gene repertoire of the two bird species was substantially larger with 479 and 553 OR gene homologs in the chicken and zebra finch, respectively (including 111 and 221 pseudogenes, respectively). We show that the green anole has a higher fraction of intact OR genes (~72%) compared with the chicken (~66%) and the zebra finch (~38%). We identified a larger number and a substantially higher proportion of intact OR gene homologs in the chicken genome than previously reported (214 versus 82 genes and 66% versus 15%, respectively). Phylogenetic analysis showed that lizard and bird OR gene repertoires consist of group α, θ and γ genes. Interestingly, the vast majority of the avian OR genes are confined to a large expansion of a single branch (the so called γ-c clade). An analysis of the selective pressure on the paralogous genes of each γ-c clade revealed that they have been subjected to adaptive evolution. This expansion appears to be bird-specific and not sauropsid-specific, as it is lacking from the lizard genome. The γ-c expansions of the two birds do not intermix, i.e., they are lineage-specific. Almost all (group γ-c) OR genes mapped to the unknown chromosome. The remaining OR genes mapped to six homologous chromosomes plus three to four additional chromosomes in the zebra finch and chicken.
We identified a surprisingly large number of potentially functional avian OR genes. Our data supports recent evidence that avian olfactory ability may be better developed than previously thought. We hypothesize that the radiation of the group γ-c OR genes in each bird lineage parallels the evolution of specific olfactory sensory functions.
Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male–male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (Imales). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7–44%, n=6 years) of the total Imales was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44–58% of the total Imales was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.
sexual selection; reproductive skew; lek; cooperation; mate choice; male–male competition
In vertebrates, the molecular basis of the sense of smell is encoded by members of a large gene family, namely olfactory receptor (OR) genes. Both the total number of OR genes and the proportion of intact OR genes in a genome may indicate the importance of the sense of smell for an animal. There is behavioral, physiological, and anatomical evidence that some bird species, in particular nocturnal birds, have a well developed sense of smell. Therefore, we hypothesized that nocturnal birds with good olfactory abilities have evolved (i) more OR genes and (ii) more intact OR genes than closely related and presumably less 'olfaction-dependent' day-active avian taxa.
We used both non-radioactive Southern hybridization and PCR with degenerate primers to investigate whether two nocturnal bird species that are known to rely on olfactory cues, the brown kiwi (Apteryx australis) and the kakapo (Strigops habroptilus), have evolved a larger OR gene repertoire than their day-active, closest living relatives (for kiwi the emu Dromaius novaehollandiae, rhea Rhea americana, and ostrich Struthio camelus and for kakapo the kaka Nestor meridionalis and kea Nestor notabilis). We show that the nocturnal birds did not have a significantly higher proportion of intact OR genes. However, the estimated total number of OR genes was larger in the two nocturnal birds than in their relatives.
Our results suggest that ecological niche adaptations such as daily activity patterns may have shaped avian OR gene repertoires.
Among vertebrates, the sense of smell is mediated by olfactory receptors (ORs) expressed in sensory neurons within the olfactory epithelium. Comparative genomic studies suggest that the olfactory acuity of mammalian species correlates positively with both the total number and the proportion of functional OR genes encoded in their genomes. In contrast to mammals, avian olfaction is poorly understood, with birds widely regarded as relying primarily on visual and auditory inputs. Here, we show that in nine bird species from seven orders (blue tit, Cyanistes caeruleus; black coucal, Centropus grillii; brown kiwi, Apteryx australis; canary, Serinus canaria; galah, Eolophus roseicapillus; red jungle fowl, Gallus gallus; kakapo, Strigops habroptilus; mallard, Anas platyrhynchos; snow petrel, Pagodroma nivea), the majority of amplified OR sequences are predicted to be from potentially functional genes. This finding is somewhat surprising as one previous report suggested that the majority of OR genes in an avian (red jungle fowl) genomic sequence are non-functional pseudogenes. We also show that it is not the estimated proportion of potentially functional OR genes, but rather the estimated total number of OR genes that correlates positively with relative olfactory bulb size, an anatomical correlate of olfactory capability. We further demonstrate that all the nine bird genomes examined encode OR genes belonging to a large gene clade, termed γ-c, the expansion of which appears to be a shared characteristic of class Aves. In summary, our findings suggest that olfaction in birds may be a more important sense than generally believed.
olfaction; bird; olfactory bulb; pseudogene; nocturnality; ecological adaptation
The steroid hormone testosterone (T) plays a central role in the regulation of breeding in males, because many physiological, morphological and behavioural traits related to reproduction are T dependent. Moreover, in many seasonally breeding vertebrates, male plasma T levels typically show a pronounced peak during the breeding season. While such population-level patterns are fairly well worked out, the sources and the implications of the large variability in individual T levels within the seasonal cycle remain surprisingly little understood. Understanding the potential sources of individual variation in T levels is important for behavioural and evolutionary ecologists, for at least two reasons. First, in ‘honest signalling’ theory, T is hypothesized to play a critical role as the assumed factor that enforces honesty of the expression of sexually selected quality indicators. Second, T is often considered a key mediator of central life-history trade-offs, such as investment in survival versus reproduction or in mating versus parental care. Here, we discuss the patterns of within- and between-individual variation in male plasma T levels in free-living populations of birds. We argue that it is unclear whether this variability mainly reflects differences in underlying individual quality (intrinsic factors such as genetic or maternal effects) or in the environment (extrinsic factors including time of day, individual territorial status and past experience). Research in avian behavioural endocrinology has mainly focused on the effects of extrinsic factors, while other sources of variance are often ignored. We suggest that studies that use an integrative approach and investigate the relative importance of all potential sources of variation are essential for the interpretation of data on individual plasma T levels.
hormone; heritability; behavioural syndrome; plasticity; genetic effects; maternal effects
Polymorphisms in several neurotransmitter-associated genes have been associated with variation in human personality traits. Among the more promising of such associations is that between the human dopamine receptor D4 gene (Drd4) variants and novelty-seeking behaviour. However, genetic epistasis, genotype–environment interactions and confounding environmental factors all act to obscure genotype–personality relationships. Such problems can be addressed by measuring personality under standardized conditions and by selection experiments, with both approaches only feasible with non-human animals. Looking for similar Drd4 genotype–personality associations in a free-living bird, the great tit (Parus major), we detected 73 polymorphisms (66 SNPs, 7 indels) in the P. major Drd4 orthologue. Two of the P. major Drd4 gene polymorphisms were investigated for evidence of association with novelty-seeking behaviour: a coding region synonymous single nucleotide polymorphism (SNP830) and a 15 bp indel (ID15) located 5′ to the putative transcription initiation site. Frequencies of the three Drd4 SNP830 genotypes, but not the ID15 genotypes, differed significantly between two P. major lines selected over four generations for divergent levels of ‘early exploratory behaviour’ (EEB). Strong corroborating evidence for the significance of this finding comes from the analysis of free-living, unselected birds where we found a significant association between SNP830 genotypes and differing mean EEB levels. These findings suggest that an association between Drd4 gene polymorphisms and animal personality variation predates the divergence of the avian and mammalian lineages. Furthermore, this work heralds the possibility of following microevolutionary changes in frequencies of behaviourally relevant Drd4 polymorphisms within populations where natural selection acts differentially on different personality types.
personality; Drd4; dopamine receptor; polymorphisms; Parus major; novelty seeking
In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.
Sexual-selection theory assumes that there are costs associated with ornamental plumage coloration. While pigment-based ornaments have repeatedly been shown to be condition dependent, this has been more difficult to demonstrate for structural colours. We present evidence for condition dependence of both types of plumage colour in nestling blue tits (Parus caeruleus). Using reflectance spectrometry, we show that blue tit nestlings are sexually dichromatic, with males having more chromatic (more 'saturated') and ultraviolet (UV)-shifted tail coloration and more chromatic yellow breast coloration. The sexual dimorphism in nestling tail coloration is qualitatively similar to that of chick-feeding adults from the same population. By contrast, the breast plumage of adult birds is not sexually dichromatic in terms of chroma. In nestlings, the chroma of both tail and breast feathers is positively associated with condition (body mass on day 14). The UV/blue hue of the tail feathers is influenced by paternally inherited genes, as indicated by a maternal half-sibling comparison. We conclude that the expression of both carotenoid-based and structural coloration seems to be condition dependent in blue tit nestlings, and that there are additional genetic effects on the hue of the UV/blue tail feathers. The signalling or other functions of sexual dichromatism in nestlings remain obscure. Our study shows that nestling blue tits are suitable model organisms for the study of ontogenetic costs and heritability of both carotenoid-based and structural colour in birds.
Although elaborate bird song provides one of the prime examples of a trait that evolved under sexual selection, it is still unclear whether females judge the quality of males by attributes of their song and whether these song features honestly signal a male's genetic quality. We measured the ability of male dusky warblers Phylloscopus fuscatus to maintain a high sound amplitude during singing, which probably reflects an individual's physiological limitations. This new measure of singing performance was correlated with male longevity and with extra-pair paternity, indicating that females who copulated with better singers obtained 'good genes' for their offspring. Our findings are consistent with the idea that females assess male quality by subtle differences in their performance during the production of notes, rather than by the quantity or versatility of song. In addition, observations on territorial conflicts indicate that attractive males invest less in competition over territories because they can reproduce via extra-pair paternity.
Under many circumstances, it might be adaptive for parents to bias the investment in offspring in relation to sex. Recently developed molecular techniques that allow sex determination of newly hatched offspring have caused a surge in studies of avian sex allocation. Whether females bias the primary brood sex ratio in relation to factors such as environmental and parental quality is debated. Progress is hampered because the mechanisms for primary sex ratio manipulation are unknown. Moreover, publication bias against non-significant results may distort our view of adaptive sex ratio manipulation. Despite this, there is recent experimental evidence for adaptive brood sex ratio manipulation in birds. Parental care is a particularly likely candidate to affect the brood sex ratio because it can have strong direct effects on the fitness of both parents and their offspring. We investigate and make predictions of factors that can be important for adaptive brood sex ratio manipulation under different patterns of parental care. We encourage correlational studies based on sufficiently large datasets to ensure high statistical power, studies identifying and experimentally altering factors with sex-differential fitness effects that may cause brood sex ratio skew, and studies that experimentally manipulate brood sex ratio and investigate fitness effects.