The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors

We studied the evolution of colour polymorphism in diurnal raptors, owls and nightjars, the avian taxa in which this trait is most widespread, in relation to species ecological niche width and diet. Two main mechanisms have been put forward to explain the maintenance of polymorphism, namely apostatic selection and disruptive selection. The niche variation hypothesis states that species with broader ecological niches should be more variable compared with those with narrow niches because of the action of disruptive selection; the apostatic selection hypothesis conversely suggests that intraspecific colour variation should be promoted in predators by prey forming an avoidance image for the more common colour morph. Our aim was to determine if colour polymorphism occurrence was associated with broad ecological niches as predicted by the niche variation hypothesis, or with predation on intelligent and sharp‐sighted prey as predicted by the avoidance image hypothesis. Pairwise comparisons were made between pairs of closely related species differing in variables expected to influence the occurrence of polymorphism. We found that polymorphic species of all three groups showed wider and more continuous distribution ranges, frequented many different habitats, both open and closed, and lived in seasonally alternating dry/wet climates. Polymorphic species were more migratory compared with monomorphic ones, and they showed an activity pattern covering both day and night. Conversely, colour polymorphism was not higher in species preying on birds and mammals. All these findings support the hypothesis that colour polymorphism evolved in bird species with wider niche breadth and not in species preying on intelligent prey. Therefore, we propose that disruptive selection may be the main mechanism maintaining colour polymorphism in these bird groups by favouring different morphs in different environmental conditions. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 237–248.     

Covariation of sexual dichromatism and plumage colours in lekking and non-lekking birds: A comparative analysis

The extreme polygyny expressed by male lekking birds leads to the expectation that sexual dimorphism should be greater in lekkers than related non-lekkers. However, evidence for this association is weak, and many lekkers are actually monomorphic in size and plumage. To better understand the kinds of plumages associated with lekking, I characterized plumage variation for combinations of sexual dichromatism and colourfulness-and-conspicuousness (COCO) among lekking and related non-lekking birds. Compared in this way, the plumages of lekkers and non-lekkers differ dramatically for both sexes. Correlations between sexual dichromatism and COCO for phylogenetically independent contrasts are significant for male lekkers (positive) and female non-lekkers (negative), but not for female lekkers or male non-lekkers. Moreover, the total number of character–state combinations, and multivariate measures of variability, are greater in non-lekkers than lekkers.The characteristic plumages of lekkers (duller monochromatic, brighter dichromatic and intermediate between these extremes) comprise just a subset of those observed among non-lekkers, and exclude extremely dull dichromatic and extremely bright monochromatic plumages. I suggest that predation, and foraging behaviours compatible with lekking, may restrict plumage variation among lekkers. Thus ecological rather than overt sexual characteristics may explain monomorphism in birds under intense mate competition, as well as the paradox of strong female mate preferences on leks, where males appear to contribute only sperm to female reproductive efforts.     

Ecological factors influencing the occurrence of 'flash marks' in wading birds

1. Although the plumage of birds is important for flight and thermoregulation, it is also employed in inter- and intraspecific communication. The role in communication of particular plumage features can be studied by experiment or, as here, by correlational analysis.
2. The study was carried out on the 210 species of wading birds, such as plovers, sandpipers, thick-knees and allies, that are placed within the traditional order Charadriiformes.
3. Species differ in the location and extent of 'flash marks', patches of white on the plumage that are typically conspicuous when the bird flies. These patches occur, in various permutations in different species, on the wing (primaries, secondaries, coverts), back, rump and tail.
4. Within a phylogenetic framework, it was asked which of several broad ecological variables (migration, habitat choice, feeding technique, propensity to flock) were correlated with the occurrence of flash marks. Only flocking correlated significantly. In particular, taxa that flock have flashier backs and coverts than their non-flocking relatives.
5. Three non-exclusive explanations for this correlation are: (i) individuals that take flight to avoid a predator may benefit from signalling their take-off to flock mates which themselves then take flight; (ii) flash marks could enhance the confusion effect within flocks, making it more difficult for a predator to single out an individual; and (iii) flash marks may facilitate co-ordinated flight within flocks.     

Variation in ultraviolet reflectance by carotenoid-bearing feathers of tanagers (Thraupini: Emberizinae: Passeriformes)

Avian visual sensitivity encompasses both the human visible range (400–700 nm) and also near‐ultraviolet (UV) wavelengths (320–400 nm) invisible to normal humans. I used reflectance spectrophotometry to assess variation in UV reflectance for yellow, orange and red plumage in 67 species of tanager (Passeriformes). Previous chemical studies, and my analysis of reflectance minima, suggest that carotenoids are the dominant pigments in yellow, orange and red tanager plumage. Spectra recorded over the range of wavelengths to which birds are sensitive (320–700 nm) were invariably bimodal, with both a plateau of high reflectance at longer (> 500 nm) wavelengths and a distinct secondary peak at UV (< 400 nm) wavelengths. Within this overall framework, variation in UV reflectance was expressed within well‐defined quantitative limits: (1) peak reflectance was always lower than the corresponding plateau of reflectance at longer visible wavelengths; (2) the intensity of peak reflectance declined steadily below 350 nm; (3) wavelengths of peak reflectance clustered between 350 and 370 nm. Significant correlations were detected between various measures of total reflectance in the UV and visible wavebands, but not between various measures of spectral location of UV and visible reflectance. I propose that the strong absorption band at short visible wavelengths (～ 380–550 nm) responsible for bimodal spectra of carotenoids in vitro is also responsible for bimodal reflectance by carotenoid‐based plumage colours. The construction of the UV and visible reflectance bands from different sides of this same absorbance band provides a mechanism for the observed covariation between UV and visible wavelengths. Lack of an association between the spectral locations of the UV and visible reflectance bands may result from the limited variation in spectral location of the UV band. These patterns suggest that plumage colours are subject to constraints, just as are more traditional morphological characters. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 243–257.     

Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors

Genetically based variation in coloration occurs in populations of many organisms belonging to various taxa, including birds, mammals, frogs, molluscs, insects and plants. Colour polymorphism has evolved in raptors more often than in any other group of birds, suggesting that predator–prey relationships was a driving evolutionary force. Individuals displaying a new invading colour morph may enjoy an initial foraging advantage because prey have difficulties in learning the colour of a rare morph (apostatic selection), or because morphs provide alternative foraging benefits allowing differently coloured individuals to exploit distinct food niches (disruptive selection). Plumage polymorphism should therefore have evolved in species that prey upon animals having the physiological ability to distinguish between differently coloured predators but also to flee once a predator has been detected. From this assumption, we can predict that closely related polymorphic and monomorphic species prey upon different animals. They may also differ in morphology, because foraging upon different prey may require different foraging modes, and in turn different morphological structures. We tested these two predictions in a comparative study of raptors. As expected, polymorphic and monomorphic species had a different diet, and there was a difference in wing length between polymorphic and monomorphic species within two genera ( Buteo and Accipiter ). Across all raptors for which phylogenetic relationships are known, polymorphic species preyed more often upon mammals than did monomorphic ones. These two types of raptor did not differ in the frequency of birds, insects and reptiles in their diets. We discuss these results in the light of the hypothesis that predator–prey relationships played a role in the evolution of colour polymorphism. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 565–578.     

A Comparative Test of Adaptive Explanations for Hypsodonty in Ungulates and Rodents

Hypsodonty has long been recognized as an adaptation for grazing: grazing is suggested to increase tooth wear due to endogenous (e.g., fiber, silica) and/or exogenous (e.g., dust, grit) properties of ingested food. However, it is unknown whether tooth crown height is correlated with the mastication of high fiber or silica in grasses, the ingestion of external abrasives, or both. Furthermore, comparative studies of hypsodonty have not explicitly taken into account phylogenetic biases due to shared ancestry in tooth morphology and/or feeding behavior. This study highlights the relationship between molar crown height and feeding habits in African ungulates and South American rodents when phylogenetic effects are controlled. Among ungulates, high hypsodonty indices are significantly associated with specific plant and foraging height preferences, while habitat and climate show no correlation with tooth crown height. For rodents, grass-eating species are significantly more hypsodont than frugivorous or folivorous species, and arboreal rodents are less hypsodont than terrestrial species. These results as well as those of a posteriori analyses controlling for aspects of the behavioral ecology (e.g., grass-eating, substrate preference) of the sample species confirm the role of both diet and grit in shaping the evolution of cheek tooth crown height in herbivorous mammals.     

系统比较方法的原理及应用

物种的大部分性状与其系统进化过程相联系,亲缘关系近的物种,其性状差异通常较小.因此在种间或更高分类单元层次研究性状之间的关系,或性状与环境间关系时需要考虑系统进化的影响,以满足常规统计分析对于样本独立性的要求.自20世纪80年代以来国际上已经陆续推出一系列的系统比较方法,其共同原理是:在推断物种间系统关系的基础上,在种间水平上比较,将原本不符合样本独立性的物种性状或环境变量数据,将其转化为适用于常规统计分析方法的彼此独立的数据,然后运用常规统计方法分析,得到排除了系统进化历史影响的物种性状间或者物种性状与环境变量间的关系.首先简单介绍了运用系统比较方法之前的建立系统关系和数据诊断这两个步骤,在此基础上阐述简单独立对比分析、Felsenstein的独立比较方法和自回归方法这3种常用的系统比较方法的基本原理、各自的特点以及它们在生态学、进化生物学等领域的应用.系统比较方法已经获得广泛的应用和认可,发现了应用常规统计分析所没有能发现的问题和规律,但在构建准确反映系统进化过程的系统关系、进化模型的选择等方面仍具有一定的局限性;而生物信息学、生物系统学的发展,以及各种相关软件的开发为系统比较方法的进一步完善发展和更为广泛的应用创造了条件.     

Colour polymorphism is associated with lower extinction risk in birds

Colour polymorphisms have played a major role in enhancing current understanding of how selection and demography can impact phenotypes. Because different morphs often display alternative strategies and exploit alternative ecological niches, colour polymorphism can be expected to promote adaptability to environmental changes. However, whether and how it could influence populations' and species' response to global changes remains debated. To address this question, we built an up‐to‐date and complete database on avian colour polymorphism based on the examination of available data from all 10,394 extant bird species. We distinguished between true polymorphism (where different genetically determined morphs co‐occur in sympatry within the same population) and geographic variation (parapatric or allopatric colour variation), because these two patterns of variation are expected to have different consequences on populations' persistence. Using the IUCN red list, we then showed that polymorphic bird species are at lesser risk of extinction than nonpolymorphic ones, after controlling for a range of factors such as geographic range size, habitat breadth, life history, and phylogeny. This appears consistent with the idea that high genetic diversity and/or the existence of alternative strategies in polymorphic species promotes the ability to adaptively respond to changing environmental conditions. In contrast, polymorphic species were not less vulnerable than nonpolymorphic ones to specific drivers of extinction such as habitat alteration, direct exploitation, climate change, and invasive species. Thus, our results suggest that colour polymorphism acts as a buffer against environmental changes, although further studies are now needed to understand the underlying mechanisms. Developing accurate quantitative indices of sensitivity to specific threats is likely a key step towards a better understanding of species response to environmental changes.     

Mating systems, sperm competition, and the evolution of sexual dimorphism in birds

Comparative analyses suggest that a variety of factors influence the evolution of sexual dimorphism in birds. We analyzed the relative importance of social mating system and sperm competition to sexual differences in plumage and body size (mass and tail and wing length) of more than 1,000 species of birds from throughout the world. In these analyses we controlled for phylogeny and a variety of ecological and life-history variables. We used testis size (corrected for total body mass) as an index of sperm competition in each species, because testis size is correlated with levels of extrapair paternity and is available for a large number of species. In contrast to recent studies, we found strong and consistent effects of social mating system on most forms of dimorphism. Social mating system strongly influenced dimorphism in plumage, body mass, and wing length and had some effect on dimorphism in tail length. Sexual dimorphism was relatively greater in species with polygynous or lekking than monogamous mating systems. This was true when we used both species and phylogenetically independent contrasts for analysis. Relative testis size was also related positively to dimorphism in tail and wing length, but in most analyses it was a poorer predictor of plumage dimorphism than social mating system. There was no association between relative testis size and mass dimorphism. Geographic region and life history were also associated with the four types of dimorphism, although their influence varied between the different types of dimorphism. Although there is much interest in the effects of sperm competition on sexual dimorphism, we suggest that traditional explanations based on social mating systems are better predictors of dimorphism in birds.     

Dietary constraints on encephalization in primates

Encephalization, and its relationship to potential selective forces, have been a focus of many studies of primate adaptation. It has been argued that gut size may constrain brain mass because these two types of "expensive tissue" (among others) compete in their metabolic requirements (Aiello and Wheeler [1995] Curr. Anthropol. 36:199-221). Following from the inverse correlation of gut size with diet quality, the expensive tissue hypothesis predicts that differences in diet quality are positively correlated with differences in brain mass, once the correlation of each variable with body mass is taken into account. We tested this prediction using both nonphylogenetic and phylogenetic methods. The results of both methods are consistent with predictions made by the expensive tissue hypothesis. We also discuss several examples of independent contrasts that are consistent with the hypothesis (e.g., Colobinae vs. Cercopithecinae), as well as some that are not (e.g., Tarsius vs. anthropoidea). Overall, the results indicate that improved diet quality, by allowing reduction in relative gut mass, is one mechanism involved in increased encephalization.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

Why colour in subterranean vertebrates? Exploring the evolution of colour patterns in caecilian amphibians

The proximate functions of animal skin colour are difficult to assign as they can result from natural selection, sexual selection or neutral evolution under genetic drift. Most often colour patterns are thought to signal visual stimuli; so,their presence in subterranean taxa is perplexing. We evaluate the adaptive nature of colour patterns in nearly a third of all known species of caecilians, an order of amphibians most of which live in tropical soils and leaf litter. We found that certain colour pattern elements in caecilians can be explained based on characteristics concerning above-ground movement. Our study implies that certain caecilian colour patterns have convergently evolved under selection and we hypothesize their function most likely to be a synergy of aposematism and crypsis, related to periods when individuals move overground. In a wider context, our results suggest that very little exposure to daylight is required to evolve and maintain a varied array of colour patterns in animal skin.     

DEGREE OF SPECIALIZATION IS RELATED TO BODY SIZE IN HERBIVOROUS INSECTS: A PHYLOGENETIC CONFIRMATION

Numerous studies have suggested a general relationship between the degree of host specialization and body size in herbivorous animals. In insects, smaller species are usually shown to be more specialized than larger‐bodied ones. Various hypotheses have attempted to explain this pattern but rigorous proof of the body size–diet breadth relationship has been lacking, primarily because the scarceness of reliable phylogenetic information has precluded formal comparative analyses. Explicitly using phylogenetic information for a group of herbivores (geometrid moths) and their host plant range, we perform a comparative analysis to study the body size–diet breadth relationship. Considering several alternative measures of body size and diet breadth, our results convincingly demonstrate without previous methodological issues—a first for any taxon—a positive association between these traits, which has implications for evaluating various central aspects of the evolutionary ecology of herbivorous insects. We additionally demonstrate how the methods used in this study can be applied in assessing hypotheses to explain the body size–diet breadth relationship. By analyzing the relationship in tree‐feeders alone and finding that the positive relationship remains, the result suggests that the body size–diet breadth relationship is not solely driven by the type of host plant that species feed on.     

Colour variation is incongruent with mitochondrial lineages: cryptic speciation and subsequent diversification in a Gulf of California reef fish (Teleostei: Blennioidei)

The Gulf of California endemic reef fish, Acanthemblemaria crockeri (Blennioidei, Chaenopsidae), reportedly has two colour morphs, one with melanic lateral spots ('Gulf' morph) and one with orange spots ('Cape' morph). In this study, we recorded colour morph in both males and females and collected mitochondrial DNA sequence data for cytochrome c oxidase I (COI) and tRNA-Pro/D-loop of specimens from throughout the Gulf to explore the genetic basis of the colour morphs. Two highly divergent (HKY + I distance = 11.9% for COI), reciprocally monophyletic lineages were identified, consistent with the presence of two parapatric species. A 30-km gap between the distributions of mitochondrial lineages roughly corresponds to a hypothesized former seaway across the Baja California peninsula north of La Paz, although the estimated divergence time (1.84 million years ago) is more recent than the hypothetical seaway (3–4 million years ago). Surprisingly, the distribution of mitochondrial species is not congruent with the distribution of either male or female colour morphs. Our analysis also revealed significant population differentiation within both species and no shared haplotypes among populations. The northern Gulf species includes four populations (NB, CB, NM and CM) corresponding to northern and central Baja and northern and central mainland sites, while the Cape species includes two populations (SB and SM) corresponding to the Baja and mainland sides of the southern Gulf. The NB/CB division corresponds to a hypothesized Plio–Pleistocene mid-peninsular seaway. The level of genetic divergence documented in this lineage is extraordinary for a marine fish with a pelagic larval stage within a semi-enclosed basin.     

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.     

Comparative body size relationships in pocket gophers and their chewing lice

In this paper, we use the method of independent contrasts to study body size relationships between pocket gophers and their chewing lice, a host-parasite system in which both host and parasite phylogcnies are well studied. The evolution of body size of chewing lice appears to be dependent only on the body size of their hosts, which confirms the 1991 findings of Harvey and Keymer. We show that there is a positive relationship between body size and hair-shaft diameter in pocket gophers, and that there is also a positive relationship between body size and head-groove width in chewing lice. Finally, we show a positive relationship between gopher hair-shaft diameter and louse head-groove width. We postulate that changes in body size of chewing lice are driven by a mechanical relationship between the parasite's head-groove dimension and the diameter of the hairs of its host. Louse species living"on larger host species may be larger simply because their hosts have thicker hairs, which requires that the lice have a wider head groove. Our study of gopher hair-shaft diameter and louse head-groove dimensions suggest that there is a 'lock-and-key' relationship between these two anatomical features.     

Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model

Violation of the molecular clock has been amply documented, and is now routinely taken into account by molecular dating methods. Comparative analyses have revealed a systematic component in rate variation, relating it to the evolution of life-history traits, such as body size or generation time. Life-history evolution can be reconstructed using Brownian models. However, the resulting estimates are typically uncertain, and potentially sensitive to the underlying assumptions. As a way of obtaining more accurate ancestral trait and divergence time reconstructions, correlations between life-history traits and substitution rates could be used as an additional source of information. In this direction, a Bayesian framework for jointly reconstructing rates, traits, and dates was previously introduced. Here, we apply this model to a 17 protein-coding gene alignment for 73 placental taxa. Our analysis indicates that the coupling between molecules and life history can lead to a reevaluation of ancestral life-history profiles, in particular for groups displaying convergent evolution in body size. However, reconstructions are sensitive to fossil calibrations and to the Brownian assumption. Altogether, our analysis suggests that further integrating inference of rates and traits might be particularly useful for neontological macroevolutionary comparative studies.     

A shortening of the manus precedes the attenuation of other wing-bone elements in the evolution of flightlessness in birds

Nudds, R. L. and Slove Davidson, J. 2010. A shortening of the manus precedes the attenuation of other wing-bone elements in the evolution of flightlessness in birds. — Acta Zoologica (Stockholm) 91 : 115–122
This is the first study to present evidence for a general pattern of wing-bone attenuation during the early stages of the evolution of flightlessness. A comparative analysis using phylogenetic independent contrasts showed that in families that contain both flighted (volant) and flightless species, the volant species have shorter wings and total-arm (humerus + ulna + manus) lengths relative to their body masses than the species within their wholly volant sister families. A shortening of the manus may typify the early stages of the evolution of flightlessness, with the humerus and ulna attenuating later, perhaps because of their role in maintaining the position of the aerodynamically important alula. A shorter wing relative to body mass was not the result of the inverse (i.e. heavier body mass relative to wing length) because mean body masses of volant members of flightless families were similar to or lower than those of their wholly volant sister families. Despite finding a common trend in the wing morphologies of volant members of flightless families, it seems unlikely that a general model of selection pressures driving the evolution of flightlessness exists. At the very least, a dichotomy between those birds that have lost the ability to fly in order to gain the ability to swim and terrestrial forms, may persist.