Predation,seed size partitioning and the evolution of body size in seed-eating finches

Summary I compare the relationship between bill size (depth) and body size among different taxa of seed-eating finches to test the hypothesis (Schluter, 1988a) that in habitats where seed-eating finches are vulnerable to predators, finches have larger bodies relative to their bill size. In support of this hypothesis, ground-foraging finches on continents (Emberizidae, Passeridae, Fringillidae), where predators are more common, have larger bodies relative to their bill sizes than do ground-foraging finches on islands (Emberizidae, Fringillidae). Ground-feeding finches on continents may also be more vulnerable to predators than tree- and shrub-foraging finches. As predicted, in North America, ground-feeding finches (Emberizinae) have larger bodies relative to their bill size than do tree- and shrub-foraging finches (Carduelinae). As a consequence of increased body size relative to bill size, both the range of possible bill sizes and potential seed sizes that can be eaten are reduced. Moreover, increased metabolic demands caused by larger body size may lessen the ability to specialize on a few seed types. These two factors reduce the potential for seed size partitioning. Consequently, vulnerability to predators may limit, and is inversely correlated with, seed size partitioning in seed-eating finch communities. The extent to which predation has influenced other bird communities may be considerable, and the patterns found by Schluter (1988a) and in this study indicate that future ecomorphological studies, especially on species that spend much of the day foraging, might profit by considering predator vulnerability as well as foraging behaviour.     

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。     

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

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

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.     

The evolution of the avian bill as a thermoregulatory organ

The avian bill is a textbook example of how evolution shapes morphology in response to changing environments. Bills of seed‐specialist finches in particular have been the focus of intense study demonstrating how climatic fluctuations acting on food availability drive bill size and shape. The avian bill also plays an important but under‐appreciated role in body temperature regulation, and therefore in energetics. Birds are endothermic and rely on numerous mechanisms for balancing internal heat production with biophysical constraints of the environment. The bill is highly vascularised and heat exchange with the environment can vary substantially, ranging from around 2% to as high as 400% of basal heat production in certain species. This heat exchange may impact how birds respond to heat stress, substitute for evaporative water loss at elevated temperatures or environments of altered water availability, or be an energetic liability at low environmental temperatures. As a result, in numerous taxa, there is evidence for a positive association between bill size and environmental temperatures, both within and among species. Therefore, bill size is both developmentally flexible and evolutionarily adaptive in response to temperature. Understanding the evolution of variation in bill size however, requires explanations of all potential mechanisms. The purpose of this review, therefore, is to promote a greater understanding of the role of temperature on shaping bill size over spatial gradients as well as developmental, seasonal, and evolutionary timescales.     

The impact of ten years at -20°C on gas exchange in five lichen species

Summary We examined the relative ability of multiple factors to explain variation in two interrelated life-history traits, interclutch interval and annual reproductive success, in feral pigeons. Seasonal influences, brood size, and female body mass and tarsus length explained significant amounts of variation in interclutch interval in this population, while female plumage phenotype was insignificant. These results are discussed in terms of resource allocation and responses to environmental heterogeneity. Multivariate selection analysis revealed strong directional fecundity selection on body mass, and correlated selection response on bill length. A prospective selection analysis based on estimates of the genetic variance-covariance matrix revealed that the mean change in a trait often differed in sign from the directional selection estimate. The relationship between annual reproductive success and these two traits was found only in melanic females, suggesting that selection differentials may covary with plumage pattern.     

SELECTION ON BILL CHARACTERS IN A POPULATION OF DARWIN'S FINCHES: GEOSPIZA CONIROSTRIS ON ISLA GENOVESA,GALÁPAGOS

Lande and Arnold's (1983) technique for measuring selection on correlated quantitative traits was used to identify the targets of selection and to reveal the direction of selection on three bill dimensions, during different stages of the life cycle in a population of Darwin's finches, Geospiza conirostris, on Isla Genovesa, Galápagos. There was a tendency towards disruptive selection during dry conditions, arising from differential survival. In terms of longevity and breeding success of females, the direction of selection was to increase bill length. For males competing for territories, selection acted to increase bill depth and bill length. The effects of male-male interactions were separated from those of female choice. Male-male interactions selected for deep and long bills, whereas females chose their mates on the basis of a male's territory position and plumage coloration. The results reveal three factors constraining changes in bill dimensions: a tendency for the mean of a dimension to shift in one direction is counteracted by selection in the opposite direction on 1) another, positively correlated, bill dimension, 2) the same dimension in the other sex, and 3) the same dimension at another stage of the life cycle. If these factors are overcome by strong directional selection at one stage of the life cycle and relaxation at another, there can be an evolutionary response because the bill dimensions in this population are known to be heritable. The results complement those found in studies of G. fortis on another island and strengthen the view that these populations of Darwin's finches are frequently subjected to natural selection.     

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.     

Fitting the bill: do different winter food resources influence juniper titmouse (Baeolophus ridgwayi) bill morphology?

Divergent adaptive selection is a prominent mechanism influencing patterns of morphological diversity. We used the juniper titmouse [Baeolophus ridgwayi (Richmond, 1902)], a nonmigratory passerine that inhabits woodlands throughout western North America, to investigate variation in bill morphology in relation to diet and geography. We gathered data from museum specimens and used morphometric techniques to determine the relative strength of support for competing hypotheses using information theoretics: (1) differences in bill morphology are predicted by a key winter food resource that each regional population consumes (seeds of different juniper tree species); or (2) bill morphology scales with body size, and both increase along a latitudinal gradient. Juniper species emerged as the variable with the most support explaining variation in bill size, supporting the hypothesis that seed sizes influence bill size, independently of body size. The shape analysis revealed no distinct patterns in bill shape variation, but employed a powerful method for evaluating the strength of support for numerous candidate models. The differences in bill size of juniper titmice across their range are likely to reflect adaptive variation, because bill morphology is highly heritable in birds, juniper titmouse gene flow appears to be relatively low, and there is a clear mechanistic explanation for why bill sizes may differ among the ranges of the three juniper species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 667–679.     

Allometric relations in three species of finches (Aves: Fringillidae)

Static nestling, adult and ontogenetic allometry were analysed in three species of finches. Static nestling allometry was very similar across age in early ontogeny and among species and could be approximated by a single matrix of phenotypic variances and covariances. The first eigenvector of this matrix showed negative allometry of bill and tarsus to mass, but positive for wing length to mass. Adult static allometry was also very similar among species, but differed from nestling pattern. In adults the bill had a positive allometry in relation to tarsus and wing, but negative to mass, while tarsus and wing were unrelated to mass. The ontogenetic allometry in each species was very similar to nestling static allometry. Viewed in relation to final size, bill characters grew more slowly than body characters, but for a longer time, which created the difference between adult and nestling allometric patterns. There were differences among species both with regard to elevation and slope of allometric coefficients, suggesting that the differences among species came about by changes in the three fundamental ontogenetic parameters namely growth rate, onset of growth and offset of growth.     

Adaptive significance of the mega-billed form in the polymorphic Black-bellied Seedcracker Pyrenestes ostrinus

The polymorphic African estrildid finch, the Black-bellied Seedcracker Pyrenestes ostrinus , exhibits extreme large-billed variants in transition zones between forest and savanna. Using field data collected between 1983 and 1995 at six sites in Cameroon, I examined the adaptive significance of bill size in this mega-billed form. In comparison with small and large morphs, body size increased more rapidly in the mega-billed form, a trend that is consistent with some other species of finches subject to avian predators in open habitats and that suggests aerodynamic constraints imposed by larger bills are compensated by increased body size. Although additional research is required, preliminary results indicate mega-billed birds may interbreed with other bill morphs and may therefore represent a third distinct morph rather than a distinct species.     

The feeding of darwin's finches on Tribulus cistoides (L.) seeds

Food-handling skills of finches vary as a function of bill size. Geospiza magnirostris crush and shatter the woody mericarps of caltrop (Tribulus cistoides) to reach the seeds, whereas G. fortis (a smaller species) bite and tear at them. G. magnirostris accept and crack most of the mericarps picked up; fortis reject most mericarps but often feed on fragments. Energy rewards are greater for magnirostris than for fortis. Intraspecific variation in handling skills parallels interspecific variation. G. fortis individuals with large bills spend more time on mericarps and extract more seeds than do those with small bills, and they reject mericarps with a lower frequency. Those observed feeding on seeds from Tribulus mericarps were larger, particularly in bill size, than those not observed feeding on them.     

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.     

Getting a head start: diet, sub-adult growth, and associative learning in a seed-eating passerine

Developmental stress, and individual variation in response to it, can have important fitness consequences. Here we investigated the consequences of variable dietary protein on the duration of growth and associative learning abilities of zebra finches, Taeniopygia guttata, which are obligate graminivores. The high-protein conditions that zebra finches would experience in nature when half-ripe seed is available were mimicked by the use of egg protein to supplement mature seed, which is low in protein content. Growth rates and relative body proportions of males reared either on a low-protein diet (mature seed only) or a high-protein diet (seed plus egg) were determined from body size traits (mass, head width, and tarsus) measured at three developmental stages. Birds reared on the high-protein diet were larger in all size traits at all ages, but growth rates of size traits showed no treatment effects. Relative head size of birds reared on the two diets differed from age day 95 onward, with high-diet birds having larger heads in proportion to both tarsus length and body mass. High-diet birds mastered an associative learning task in fewer bouts than those reared on the low-protein diet. In both diet treatments, amount of sub-adult head growth varied directly, and sub-adult mass change varied inversely, with performance on the learning task. Results indicate that small differences in head growth during the sub-adult period can be associated with substantial differences in adult cognitive performance. Contrary to a previous report, we found no evidence for growth compensation among birds on the low-protein diet. These results have implications for the study of vertebrate cognition, developmental stress, and growth compensation.     

The scaling and selection of sexually dimorphic characters: an example using the Marbled Teal

Current theory and empirical evidence suggests that, if a character is sexually dimorphic as a result of sexual selection, it should be positively allometric (i.e. relatively larger in larger individuals), whereas if the dimorphism is the result of natural selection (e.g. niche divergence), it should be isometric. I show how this can be used to study the selective forces responsible for dimorphic morphological characters, using the monochromatic Marbled Teal Marmaronetta angustirostris as an example. In absolute terms, first-year male teals have a higher body mass, wing length, head length and bill length than females. In relative terms (controlling for body size), males still have longer wings, heads and bills. The scaling in Marbled Teal suggests that bill and head dimorphisms are due to sexual selection, whereas wing dimorphism is due to natural selection. Tail length is sexually monomorphic but positively allometric, possibly because of a display function. Such scaling studies are easy to carry out, and provide a useful complement to direct investigation of the influence of variation in the size of dimorphic characters on mating success, foraging efficiency etc.     

Evolution in Darwin's finches: a review of a study on Isla Daphne Major in the Galápagos archipelago

This paper reviews research pertaining to the problem of speciation of the finches on the Galápagos archipelago carried out by assistants, several colleagues, Peter Grant and myself. I give a brief history of the radiation, examine the process of divergence by natural selection over time, and then consider the nature of the reproductive barrier to gene flow between closely related species. Fluctuating climatic conditions have produced a continuously changing ecological landscape and altered feeding conditions for the finches over the last 30 years. Finch populations tracked these changes by natural selection and evolutionary responses to the main events. At each event significant morphological change occurred from one generation to the next generation. As a consequence of these accumulated changes, the mean bill shape and body size of the Geospiza fortis and G. scandens populations differed markedly from 1973 to 2002. Song, a learned culturally transmitted trait, acted as a barrier to reproduction between these species. Rare incidences of misimprinting on song led to hybridization and introgression. Low levels of gene flow from one species to another increased genetic variation on which selection acted. Although the major driving force of diversification was ecological change, the process of diversification involved a subtle interplay between ecology, genetic evolution and learned culturally transmitted traits. An important message for conservation is that neither the environment nor species are fixed entities, therefore a wise strategy for conserving endangered species should keep them capable of further change.     

Bill Color Preferences of Zebra Finches

Bill color varies with age and sex in zebra finches. Among birds of similar age and condition, males' bills tend to be redder and darker than those of females, but there is overlap in the phenotypic expression of the sexes. The bills of young birds are paler and less red than those of older birds. There is also interindividual variation within age and sex class. Experiments were performed to measure heterosexual and isosexual (= same sex) preferences of finches. Females preferred to associate with males with the reddest, brightest bills; they even preferred males whose bills were exaggerated through color applications of non-toxic marking pen. Males preferred to associate with females with bill colors in the middle of the phenotypic range. Females thus have “directional” preferences for male bill color, whereas male preference is “stabilizing” with regard to female bill color. In isosexual tests, neither sex showed a consistent preference for particular bill colors. Both sexes, however, displayed a tendency toward individual variability in preference. Bill color appears to be more important in heterosexual than in isosexual interactions. Several authors have recently suggested that organisms prefer brightly colored mates because bright coloration indicates superior physical condition. Results reported here do not support this hypothesis. Alternative functional explanations for the observed preferences are that bill color signals mating status, age or reproductive value. None of these appears to be a cogent explanation for the trends. Preferences do not appear to result from sexual imprinting. The possibility that the preferences are aesthetic and non-functional is discussed.     

Population variation and hybridization: Comparison of finches from two archipelagos

Summary Some populations of Darwin's Finches (Emberizinae) are exceptionally variable in body size and beak traits as a result of introgressive hybridization. A study of museum specimens of honeycreeper-finches (Carduelinae) from the Hawaiian islands was undertaken to see if the same phenomenon was manifested by a different phyletic group of finches in a different archipelago. Five hundred and twenty-four specimens of the seven species with finch-like bills were measured and their coefficients of variation were compared with those of the ground finch group (six species) of Darwin's Finches. Coefficients were smaller in the Hawaiian finches. Sympatric and, hence, potentially hybridizing species on the island of Hawaii were not consistently more variable than the allopatric species on other islands in the archipelago. The one species with both sympatric and allopatric populations did not show greater variation in the sympatric population. There is little evidence from these comparisons of hybridization occurring in the last 100 years. The difference between the two finch faunas can be explained in terms of two factors. Finches have been present for a longer time in the Hawaiian archipelago than in the Galápagos archipelago and have had more time to not only diversify but to evolve pre- and post-zygotic isolating mechanisms. In the generally less seasonal and floristically richer Hawaiian islands they have evolved greater dietary specializations. Beak traits adapted to specialist feeding may have been under stronger stabilizing selection and hybrids (if formed) may have been at a strong disadvantage in the absence of an ecological niche intermediate between the niches of the two parental species. Results of published electrophoretic studies of genetic variation suggest that the early phase of differentiation, involving occasional introgressive hybridization, may last for up to 5 million years.     

Divergence and evolution in Darwin's finches

The medium and large ground finches of the Galapagos archipelago Geospiza fortis and G. magnirostris are distinguished by their different body size and bill dimensions on most of the islands where they both occur. On the island of Indefatigable this distinction is not complete and a group of birds with intermediate bill dimensions is present. The origin of this group could be explained by sympatric divergence of G. fortis or by hybridization, between this species and G. magnirostris . Although the conditions for sympatric divergence are severe it seems likely that strong disruptive selection for different optimal bill sizes may be operating on G. fortis , due to the presence of several ecological niches, separate categories of size and hardness of seeds the birds eat. It is suggested that islands in the Galapagos archipelago, and perhaps other oceanic islands, may provide conditions extremely conducive to sympatric divergence, or even sympatric speciation.