Morphological adaptation influences the evolution of a mating signal

Theory predicts that forces of natural selection can reduce the intensity of sexually selected traits. In this study, I investigate how morphological adaptation to feeding ecology influences a mating signal. In birds, changes in feeding ecology can cause rapid divergence in bill morphology. Because bills are also important for song production, feeding ecology may influence song divergence. During song, birds can rapidly change vocal tract resonance using bill movement, yet are constrained in rate and magnitude of bill movements resulting in a trade-off between trill rate and frequency bandwidth. Male swamp sparrows vary in their ability to produce rapid, broad-band trills and females prefer more physically demanding songs. Populations of swamp sparrows adapted to the feeding ecology of tidal marshes have larger bills than inland populations. Larger bills should increase the constraints of producing rapid, broad-band trills allowing for a test of how changes in feeding ecology affect a feature of song used in mate choice. I found significant differences in acoustic features of song consistent with the hypothesis that coastal males are less able to meet the physical demands of song production because of the constraints of having larger bills. As possible compensation for decreases in song performance, coastal populations exhibit an increase in song complexity. These changes support the current model of how motor constraints influence song production and suggest a mechanism by which feeding ecology can influence signal evolution.     

High summer temperature explains bill size variation in salt marsh sparrows

Physiological factors are rarely proposed to account for variation in the morphology of feeding structures. Recently, bird bills have been demonstrated to be important convective and radiant heat sinks. Larger bills have greater surface area than smaller bills and could serve as more effective thermoregulatory organs under hot conditions. The heat radiating function of bills should be more important in open habitats with little shade and stronger convective winds. Furthermore, as a means of dumping heat without increasing water loss through evaporation, bills might play a particularly important thermoregulatory role in heat loss in windy habitat where fresh water is limited. North American salt marshes provide a latitudinal gradient of relatively homogeneous habitat that is windy, open, and fresh‐water limited. To examine the potential role of thermoregulation in determining bill size variation among ten species or subspecies of tidal marsh sparrows, we plotted bill size against maximum summer and minimum winter temperatures. Bill surface areas increases with summer temperature, which explained 82–89% of the variance (depending upon sex) when we controlled for genus membership. Latitude alone predicted bill surface area much more poorly than summer temperature, and winter temperatures explained < 10% of the variance in winter bill size. Tidal marsh sparrow bill morphology may, to a large degree, reflect the role of the bill in expelling excess body heat in these unbuffered, fresh‐water‐limited environments. This new example of Allen's rule reaffirms the importance of physiological constraints on the evolution of vertebrate morphologies, even in bird bills, which have conventionally been considered as products of adaptation to foraging niche.     

Bill size variation in northern cardinals associated with anthropogenic drivers across North America

Allen's rule predicts that homeotherms inhabiting cooler climates will have smaller appendages, while those inhabiting warmer climates will have larger appendages relative to body size. Birds’ bills tend to be larger at lower latitudes, but few studies have tested whether modern climate change and urbanization affect bill size. Our study explored whether bill size in a wide‐ranging bird would be larger in warmer, drier regions and increase with rising temperatures. Furthermore, we predicted that bill size would be larger in densely populated areas, due to urban heat island effects and the higher concentration of supplementary foods. Using measurements from 605 museum specimens, we explored the effects of climate and housing density on northern cardinal bill size over an 85‐year period across the Linnaean subspecies’ range. We quantified the geographic relationships between bill surface area, housing density, and minimum temperature using linear mixed effect models and geographically weighted regression. We then tested whether bill surface area changed due to housing density and temperature in three subregions (Chicago, IL., Washington, D.C., and Ithaca, NY). Across North America, cardinals occupying drier regions had larger bills, a pattern strongest in males. This relationship was mediated by temperature such that birds in warm, dry areas had larger bills than those in cool, dry areas. Over time, female cardinals’ bill size increased with warming temperatures in Washington, D.C., and Ithaca. Bill size was smaller in developed areas of Chicago, but larger in Washington, D.C., while there was no pattern in Ithaca, NY. We found that climate and urbanization were strongly associated with bill size for a wide‐ranging bird. These biogeographic relationships were characterized by sex‐specific differences, varying relationships with housing density, and geographic variability. It is likely that anthropogenic pressures will continue to influence species, potentially promoting microevolutionary changes over space and time.     

Heat Loss May Explain Bill Size Differences between Birds Occupying Different Habitats

Background

Research on variation in bill morphology has focused on the role of diet. Bills have other functions, however, including a role in heat and water balance. The role of the bill in heat loss may be particularly important in birds where water is limiting. Song sparrows localized in coastal dunes and salt marsh edge (Melospiza melodia atlantica) are similar in size to, but have bills with a 17% greater surface area than, those that live in mesic habitats (M. m. melodia), a pattern shared with other coastal sparrows. We tested the hypotheses that sparrows can use their bills to dissipate “dry” heat, and that heat loss from the bill is higher in M. m. atlantica than M. m. melodia, which would indicate a role of heat loss and water conservation in selection for bill size.

Methodology/Principal Findings

Bill, tarsus, and body surface temperatures were measured using thermal imaging of sparrows exposed to temperatures from 15–37°C and combined with surface area and physical modeling to estimate the contribution of each body part to total heat loss. Song sparrow bills averaged 5–10°C hotter than ambient. The bill of M. m atlantica dissipated up to 33% more heat and 38% greater proportion of total heat than that of M. m. melodia. This could potentially reduce water loss requirements by approximately 7.7%.

Conclusions/Significance

This >30% higher heat loss in the bill of M. m. atlantica is independent of evaporative water loss and thus could play an important role in the water balance of sparrows occupying the hot and exposed dune/salt marsh environments during the summer. Heat loss capacity and water conservation could play an important role in the selection for bill size differences between bird populations and should be considered along with trophic adaptations when studying variation in bill size.     

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.     

Song is a reliable signal of bill morphology in Darwin's small tree finch Camarhynchus parvulus, and vocal performance predicts male pairing success

The shape and movement of the vocal tract are known to influence bird song. Current theory predicts that large bill and body size are correlated with low frequency song and slow trill rate. It is also widely accepted that song characteristics are important for mate choice by females. We investigated the relationship between bill morphology, song characteristics, and pairing success in Darwin's small tree finch Camarhynchus parvulus , on the Galapagos Islands. Contrary to predictions from a previous cross-species study on Darwin's finches, we found that individuals with larger bill size produced songs with slow trill rate, high dominant frequency, and broad frequency bandwidth, indicating that song is a reliable signal of bill morphology. Vocal performance as indicated by the deviation from an upper performance limit was higher in paired than unpaired males. Pairing was not skewed in favour of a particular bill size, and both small and large billed males that sang high performance song had high pairing success. The reliable signalling function of song has implications for female choice and territorial defence, given that both females and conspecific competitors can assess the relative size of males' bills through song, while females may use vocal performance as a signal of male quality.     

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.     

Both natural selection and isolation by distance explain phenotypic divergence in bill size and body mass between South Australian little penguin colonies

Morphological variation between populations of the same species can arise as a response to genetic variation, local environmental conditions, or a combination of both. In this study, I examined small‐scale geographic variation in bill size and body mass in little penguins (Eudyptula minor) across five breeding colonies in South Australia separated by <150 km. To help understand patterns driving the differences, I investigated these variations in relation to environmental parameters (air temperature, sea surface temperature, and water depth) and geographic distances between the colonies. I found substantial morphological variation among the colonies for body mass and bill measurements (except bill length). Colonies further located from each other showed greater morphological divergence overall than adjacent colonies. In addition, phenotypic traits were somewhat correlated to environmental parameters. Birds at colonies surrounded by hotter sea surface temperatures were heavier with longer and larger bills. Birds with larger and longer bills were also found at colonies surrounded by shallower waters. Overall, the results suggest that both environmental factors (natural selection) and interpopulation distances (isolation by distance) are causes of phenotypic differentiation between South Australian little penguin colonies.     

Habitat type and ambient temperature contribute to bill morphology

Avian bills are iconic structures for the study of ecology and evolution, with hypotheses about the morphological structure of bills dating back to Darwin. Several ecological and physiological hypotheses have been developed to explain the evolution of the morphology of bill shape. Here, we test some of these hypotheses such as the role of habitat, ambient temperature, body size, intraspecific competition, and ecological release on the evolution of bill morphology. Bill morphology and tarsus length were measured from museum specimens of yellow warblers, and grouped by habitat type, sex, and subspecies. We calculated the mean maximum daily temperature for the month of July, the hottest month for breeding specimens at each collecting location. Analysis of covariance models predicted total bill surface area as a function of sex, habitat type, body size, and temperature, and model selection techniques were used to select the best model. Habitat, mangrove forests compared with inland habitats, and climate had the largest effects on bill size. Coastal wetland habitats and island populations of yellow warblers had similar bill morphology, both of which are larger than mainland inland populations. Temperate but not tropical subspecies exhibited sexual dimorphism in bill morphology. Overall, this study provides evidence that multiple environmental factors, such as temperature and habitat, contribute to the evolution of bill morphology.     

Bill colour and correlates of male quality in blackbirds: an analysis using canonical ordination

Carotenoid-dependent plumage displays are widely assumed to be honest indicators of individual health or quality, which are used as cues during mate choice and/or agonistic signalling. Despite the fact that red, yellow and orange pigmentation of bills is common, and also variable between individuals, comparatively little is known about bill colouration as a condition-dependent trait. Furthermore, many studies of avian colouration are confounded by the lack of objective colour quantification and the use of overly simplistic univariate techniques for analysis of the relationship between the condition-dependent trait and individual quality variables. In this study, we correlated male blackbird bill colour (a likely carotenoid-dependent sexually selected trait) with body/condition variables that reflect male quality. We measured bill colour using photometric techniques, thus ensuring objectivity. The data were analysed using the multivariate statistical techniques of canonical ordination. Analyses based on reflectance spectra of male blackbird bill samples and colour components (i.e. hue, chroma and brightness) derived from the reflectance spectra were very similar. Analysing the entire reflectance spectra of blackbird bill samples with Redundancy Analysis (RDA) allowed examination of individual wavelengths and their specific associations with the body/condition variables. However, hue, chroma and brightness values also provided useful information to explain colour variation, and the two approaches may be complimentary. We did not find any significant associations between male blackbird bill colour and percent incidence of ectoparasites or cloaca size. However, both the colour component and full spectral analyses showed that culmen length explained a significant amount of variation in male blackbird bill colour. Culmen length was positively associated with greater reflectance from the bill samples at longer wavelengths and a higher hue value (i.e. more orange-pigmented bills). Larger males may have larger territories or be better at defending territories during male-male interactions, ensuring access to carotenoid food sources. Future studies should elucidate the relationship between bill colour and behavioural measures such as aggressiveness, territory size, song rate and nest attendance.     

Relationships of song structure to phylogenetic history,habitat, and morphology in the vireos,greenlets, and allies (Passeriformes: Vireonidae)

Acoustic signals show immense variation among passerines, and several hypotheses have been proposed to explain this diversity. In this study, we tested, for the first time, the relationships of song structure to phylogeny, habitat type, and morphology in the vireos and allies (Vireonidae). Every measure of song structure considered in this study had moderate and significant phylogenetic signal. Furthermore, two song-constraining morphological traits, bill shape and body mass, also exhibited significant phylogenetic signal. Song length showed the largest within-clade similarity; longer songs were highly conserved in part of the greenlet (Hylophilus) clade, whereas shorter songs characterized the remaining seven genera. We found no differences in song structure among vireonids living in different habitat types. However, vireonids with shorter, stouter bills and larger bodies sang songs with lower minimum and maximum peak frequency, compared with species with longer, thinner bills and smaller bodies. We conclude that Vireonidae song evolution is driven partially by phylogenetically conserved morphological traits. Our findings support the phylogenetic signal and morphological constraints hypotheses explaining structural diversity in avian acoustic signals.     

Effects of early nutrition on growth rate and adult size in song sparrows Melospiza melodia

We manipulated the quantity of food provided to hand-reared song sparrows Melospiza melodia from 3 to 18 days post-hatching, a period when young birds in the wild are especially likely to experience nutritional stress. A control group was given unlimited food, while an experimental group was limited to 60% of the intake of the controls. Both groups showed excellent survival. The controls had significantly higher growth rates than the experimentals and fledged significantly earlier. At the end of treatment, controls were significantly larger than experimentals in body mass, tarsus length, and length of the third primary. After treatment ended, when all birds were receiving the same diet, both groups showed a recession in body mass, but the amount of mass lost was significantly greater in the controls. Consequently the difference in body mass between the treatment groups was much reduced after the period of weight recession. As adults, the controls were significantly larger than experimentals in a principal component measure of size that combined six post-mortem bone measurements. Controls and experimentals did not differ in the number of fault bars in tail feathers grown in part during the period of nutritional manipulation, nor did they differ in the degree of asymmetry in bone measurements. We conclude that early nutrition affects growth rates in young song sparrows, with effects on skeletal size that carry over into adulthood. These results are consistent with the nutritional stress hypothesis, which posits that early nutrition affects adult phenotypic quality as well as display attributes.     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

NATURAL SELECTION ON BILL CHARACTERS IN THE TWO BILL MORPHS OF THE AFRICAN FINCH PYRENESTES OSTRINUS

Evidence for natural selection on seven bill and body characters is examined in the two bill morphs of the African estrildid finch Pyrenestes ostrinus. Two regression methods are used in examining natural selection in association with survivorship: a parametric (Lande and Arnold, 1983) and a non-parametric (Schluter, 1988) method. Selection was estimated in adult males, females and juveniles over a four-year period in a population in south-central Cameroon. Selection was common among groups but patterns differed and depended on the method used in detecting selection. The non-parametric method revealed evidence for disruptive selection occurring on bill width and is explained within the context of known feeding efficiencies and the hardness of important seeds in finch diets. Directional selection was common on bill characters in all groups, but infrequent on other characters. There was no evidence of selection on generalized size or shape characters. Selection on bill characters was common across groups despite low annual variation in rainfall. This contrasts with studies of Galápagos finches in which selection is frequently associated with dramatic changes in food supply caused by high variance in annual rainfall. Patterns of selection on bill traits in P. ostrinus also differ from those in song sparrows and Galápagos finches by exhibiting evidence for natural selection on all bill dimensions.     

澳大利亚Floreana岛达尔文小树雀喙型与其鸣唱的不相关性

鸟类鸣唱的功能通常是吸引配偶,对于建立繁殖隔离也是非常重要的。现有的研究认为鸟类鸣唱表演可能受到鸟类喙型变化的影响。达尔文鸣雀是一类用来验证喙型和鸣唱表演关系的模型物种,前人的研究认为较低的元音演奏与更大的喙相关。本文用在Floreana岛屿生活的达尔文小树雀(Camarhynchus parvulus)来验证喙型和元音演奏的关系。结果显示,喙型大小与元音演奏之间无相关性。这个发现与过去对小树雀中的研究结果相似,但却与达尔文鸣雀中更大体型的鸟类研究结果相反。讨论了研究结果在物种的生态分化和生态变异之间的前后关系。     

DIVERSITY‐DEPENDENT CLADOGENESIS AND TRAIT EVOLUTION IN THE ADAPTIVE RADIATION OF THE AUKS (AVES: ALCIDAE)

Through the course of an adaptive radiation, the evolutionary speed of cladogenesis and ecologically relevant trait evolution are expected to slow as species diversity increases, niches become occupied, and ecological opportunity declines. We develop new likelihood‐based models to test diversity‐dependent evolution in the auks, one of only a few families of seabirds adapted to underwater “flight,” and which exhibit a large variety of bill sizes and shapes. Consistent with the expectations of adaptive radiation, we find both a decline in rates of cladogenesis (a sixfold decline) and bill shape (a 64‐fold decline) evolution as diversity increased. Bill shape diverged into two clades at the basal cladogenesis event with one clade possessing mostly long, narrow bills used to forage primarily on fish, and the other with short thick bills used to forage primarily on plankton. Following this initial divergence in bill shape, size, a known correlate of both prey size and maximum diving depth, diverged rapidly within each of these clades. These results suggest that adaptive radiation in foraging traits underwent initial divergence in bill shape to occupy different food resources, followed by size differentiation to subdivide each niche along the depth axis of the water column.     

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds' bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting that the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.     

Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows

In seasonally breeding songbirds, brain nuclei of the song control system that act in song perception change in size between seasons. It has been hypothesized that seasonal regression of song nuclei may impair song discrimination. We tested this hypothesis in song sparrows (Melospiza melodia), a species in which males share song types with neighbors and must discriminate between similar songs in territorial interactions. We predicted that song sparrows with regressed song systems would have greater difficulty in discriminating between similar songs. Sparrows were housed either on short days (SD) and had regressed song circuits, or were exposed to long days and implanted with testosterone (LD+T) to induce full growth of the song circuits. We conducted two experiments using a GO/NO-GO operant conditioning paradigm to measure song discrimination ability of each group. Birds learned four (experiment 1) or three (experiment 2) pairs of song types sequentially, with each pair more similar in the number of shared song elements and thus more difficult to discriminate. Circulating T levels differed between the SD and LD+T groups. The telencephalic song nuclei HVc, RA, and area X were larger in the LD+T birds. The two groups of sparrows did not differ, however, in their ability to learn to discriminate between shared song types, regardless of the songs' similarity. These results suggest that seasonal changes in the song control system do not affect birds' ability to make difficult song discriminations.     

A biogeographic pattern in sparrow bill morphology: parallel adaptation to tidal marshes

The study of ecological convergence, the evolution of similar traits on multiple occasions in response to similar conditions, is a powerful method for developing and testing adaptive hypotheses. However, despite the great attention paid to geographic variation and the foraging ecology of birds, surprisingly few cases of convergent or parallel feeding adaptations have been adequately documented. In this study, we document a biogeographic pattern of parallel bill morphology across 10 sparrow taxa endemic to tidal marshes. All North American tidal marsh sparrows display parallel differentiation from close relatives in other habitats, suggesting that selection on bill morphology is strong. Relative to their body mass, tidal marsh sparrows have longer, thinner bills than their non-tidal marsh counterparts, which is likely an adaptation for consuming more invertebrates and fewer seeds, as well as for probing in sediment crevices to capture prey. Published data on tidal marsh food resources and diet of the relevant taxa support this hypothesis. This morphological differentiation is most pronounced between sister taxa with the greatest estimated divergence times, but is found even in taxa that show little or no structure in molecular genetic markers. We, therefore, speculate that tidal marsh ecosystems are likely settings for ecological speciation.     

Song characteristics track bill morphology along a gradient of urbanization in house finches (<Emphasis Type="Italic">Haemorhous mexicanus</Emphasis>)

Introduction

Urbanization can considerably impact animal ecology, evolution, and behavior. Among the new conditions that animals experience in cities is anthropogenic noise, which can limit the sound space available for animals to communicate using acoustic signals. Some urban bird species increase their song frequencies so that they can be heard above low-frequency background city noise. However, the ability to make such song modifications may be constrained by several morphological factors, including bill gape, size, and shape, thereby limiting the degree to which certain species can vocally adapt to urban settings. We examined the relationship between song characteristics and bill morphology in a species (the house finch, Haemorhous mexicanus) where both vocal performance and bill size are known to differ between city and rural animals.

Results

We found that bills were longer and narrower in more disturbed, urban areas. We observed an increase in minimum song frequency of urban birds, and we also found that the upper frequency limit of songs decreased in direct relation to bill morphology.

Conclusions

These findings are consistent with the hypothesis that birds with longer beaks and therefore longer vocal tracts sing songs with lower maximum frequencies because longer tubes have lower-frequency resonances. Thus, for the first time, we reveal dual constraints (one biotic, one abiotic) on the song frequency range of urban animals. Urban foraging pressures may additionally interact with the acoustic environment to shape bill traits and vocal performance.