Interspecific variation in plumage colour among birds: species recognition or light environment?

Abstract The traditional explanation for interspecific plumage colour variation in birds is that colour differences between species are adaptations to minimize the risk of hybridization. Under this explanation, colour differences between closely related species of birds represent reproductive character displacement. An alternative explanation is that interspecific variation in plumage colour is an adaptive response to variation in light environments across habitats. Under this explanation, differences in colour between closely related species are a product of selection on signal efficiency. We use a comparative approach to examine these two hypotheses, testing the effects of sympatry and habitat use, respectively, on divergence in male plumage colour. Contrary to the prediction of the Species Isolation Hypothesis, we find no evidence that sympatric pairs of species are consistently more divergent in coloration than are allopatric pairs of species. However, in agreement with the Light Environment Hypothesis, we find significant associations between plumage coloration and habitat use. All of these results remain qualitatively unchanged irrespective of the statistical methodology used to compare reflectance spectra, the body regions used in the analyses, or the exclusion of areas of plumage not used in sexual displays. Our results suggest that, in general, interspecific variation in plumage colour among birds is more strongly influenced by the signalling environment than by the risk of hybridization.     

Genetic divergences and intraspecific variation in corvids of the genus Corvus (Aves: Passeriformes: Corvidae) – a first survey based on museum specimens

The first comprehensive overview of intra‐ and interspecific variation within the genus Corvus as well as first insights into the phylogenetic relationships of its species is presented. DNA sequences of the mitochondrial control region were obtained from 34 of the 40 described species (including subspecies: 56 taxa). As the study was based mainly on museum material, several specimens did not yield the full length marker sequence. In these cases, only a short section of the control region could be analysed. Nevertheless, even these individuals could be assigned tentatively to clades established on the full length marker sequence. Inclusion of sequences of other corvid genera as available in GenBank clearly confirmed the monophyly of the genus Corvus. Within the Corvus clade several distinct subclades can be distinguished. Some represent lineages of single species or species pairs while other clades are composed of many species. In general, the composition of the clades reflects geographical contiguousness and confirms earlier assumptions of a Palearctic origin of the genus Corvus with several independent colonizations of the Nearctic and the Aethiopis. The Australasian radiation seems to be derived from a single lineage. The distribution of plumage colour in the phylogenetic tree indicates that the pale markings evolved several times independently. The white/grey plumage colour pattern – which is found also in other genera of the family Corvidae, for example, in Pica– occurs already in the species pair representing the first split within the genus Corvus (Corvus monedula, Corvus dauuricus). Thus, reversal to full black colour seems to have occurred as well. The use of colour traits as a phylogenetic marker within Corvus should be considered with severe caution.     

The mechanistic,genetic and evolutionary causes of bird eye colour variation

Birds display a rainbow of eye colours, but this trait has been little studied compared with plumage coloration. Avian eye colour variation occurs at all phylogenetic scales: it can be conserved throughout whole families or vary within one species, yet the evolutionary importance of this eye colour variation is under-studied. Here, we summarize knowledge of the causes of eye colour variation at three primary levels: mechanistic, genetic and evolutionary. Mechanistically, we show that avian iris pigments include melanin and carotenoids, which also play major roles in plumage colour, as well as purines and pteridines, which are often found as pigments in non-avian taxa. Genetically, we survey classical breeding studies and recent genomic work on domestic birds that have identified potential ‘eye colour genes’, including one associated with pteridine pigmentation in pigeons. Finally, from an evolutionary standpoint, we present and discuss several hypotheses explaining the adaptive significance of eye colour variation. Many of these hypotheses suggest that bird eye colour plays an important role in intraspecific signalling, particularly as an indicator of age or mate quality, although the importance of eye colour may differ between species and few evolutionary hypotheses have been directly tested. We suggest that future studies of avian eye colour should consider all three levels, including broad-scale iris pigment analyses across bird species, genome sequencing studies to identify loci associated with eye colour variation, and behavioural experiments and comparative phylogenetic analyses to test adaptive hypotheses. By examining these proximate and ultimate causes of eye colour variation in birds, we hope that our review will encourage future research to understand the ecological and evolutionary significance of this striking avian trait.     

Dynamic colonization exchanges between continents and islands drive diversification in paradise‐flycatchers (Terpsiphone,Monarchidae)

Aim We use parametric biogeographical reconstruction based on an extensive DNA sequence dataset to characterize the spatio‐temporal pattern of colonization of the Old World monarch flycatchers (Monarchidae). We then use this framework to examine the role of dispersal and colonization in their evolutionary diversification and to compare plumages between island and continental Terpsiphone species. Location Africa, Asia and the Indian Ocean. Methods We generate a DNA sequence dataset of 2300 bp comprising one nuclear and three mitochondrial markers for 89% (17/19) of the Old World Monarchidae species and 70% of the Terpsiphone subspecies. By applying maximum likelihood and Bayesian phylogenetic methods and implementing a Bayesian molecular clock to provide a temporal framework, we reveal the evolutionary history of the group. Furthermore, we employ both Lagrange and Bayes‐ Lagrange analyses to assess ancestral areas at each node of the phylogeny. By combining the ancestral area reconstruction with information on plumage traits we are able to compare patterns of plumage evolution on islands and continents. Results We provide the first comprehensive molecular phylogenetic reconstruction for the Old World Monarchidae. Our phylogenetic results reveal a relatively recent diversification associated with several dispersal events within this group. Moreover, ancestral area analyses reveal an Asian origin of the Indian Ocean and African clades. Ancestral state reconstruction analyses of plumage characters provide an interpretation of the plumage differentiation on islands and continents. Ancestral plumage traits are inferred to be close to those of the Asian paradise‐flycatcher (Terpsiphone paradisi), and island species display a high degree of plumage autapomorphy compared with continental species. Main conclusions Terpsiphone paradisi is polyphyletic and comprises populations that have retained the ancestral plumage of the widespread Terpsiphone genus. The genus appears to have colonized south‐west Asia, the Indian Ocean and Africa from eastern Asia. The phylogeny and divergence time estimates indicate multiple simultaneous colonizations of the western Old World by Terpsiphone. These results reinforce a hypothesis of range expansions of a Terpsiphone paradisi‐like ancestor into eastern Asia and the western Old World.     

Molecular phylogenetics and diversification of the genus Sporophila (Aves: Passeriformes)

The evolutionary affinities within and among many groups of nine-primaried oscines remain unresolved. One such group is Sporophila, a large genus of New World tanager-finches. Our study focused particularly on clarifying the relationship between this genus and a closely related one, Oryzoborus, and on examining the phylogenetic affinities of the "capuchinos," a group of 11 Sporophila species that share a similar male plumage coloration pattern. Our phylogenetic analyses, based on 498 bp of mitochondrial DNA sequence, indicated that: (1) Oryzoborus is embedded within a well-supported clade containing all Sporophila species, which strongly suggests that both genera should be merged, (2) the species of capuchinos comprise a monophyletic group, implying that the plumage patterns common to all probably arose only once, and (3) the capuchinos clade is comprised of two sub-clades, one including two species that are distributed in northern South America and the other one containing eight species that are present south of the Amazon River. Mean sequence divergence among the southern capuchinos species was extremely low, suggesting a rapid radiation within the last half-million years that may be related to the high level of sexual selection present in the genus and might have been promoted by marine ingressions and egressions that occurred in some southern coastal regions of South America in the Late Pleistocene.     

Genetic divergence in the superspecies Manacus

The bearded manakins in the genus Manacus are lekking, neotropical passerines. Male plumage colour varies with geographical location and classification is based solely on these plumage patterns. It has recently been suggested that in this group of birds, plumage patterns may be a misleading taxonomic character. In this study we used microsatellite variation in a collection of museum samples to establish the amount of genetic divergence between the previously described bearded manakin species/subspecies. We found substantial genetic substructuring between species/subspecies and that plumage patterns indeed may be a misleading taxonomic character because the presence of yellow in male nuptial plumage is found in most divergent forms. We did not detect a significant isolation by distance relationship although the P -value was close to significance. Physical barriers such as rivers and mountains may affect gene flow and play a role in shaping genetic structure of the genus Manacus . Accordingly, boundaries between species/subspecies often coincide with large rivers, mountains and seas.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 439–447.     

Using colour spectral data in studies of geographic variation and taxonomy of birds: examples with two hummingbird genera, Anthracothorax and Eulampis

I propose a methodology to obtain and compare integral information on bird plumage coloration, using colour spectral data to conduct studies on geographic variation and taxonomy of different bird groups. I used principal component analysis and discriminant function analysis to compare groups of individuals by plumage coloration. As examples of the application of the methodology, I compared populations within the genus Eulampis and Anthracothorax. The results indicate possible taxonomic inadequacies and reveal situations that deserve further analysis, demonstrating the potential of the methodology in this area.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Phylogenetic relationships, biogeography and speciation in the avian genus Saxicola

The avian genus Saxicola is distributed throughout Africa, Asia, Europe and various islands across Oceania. Despite the fact that the group has great potential as a model to test evolutionary hypotheses due to the extensive variability in life history patterns recorded between and within species, the phylogenetic relationships among species and subspecies of this genus are poorly understood. We undertook a systematic investigation of the relationships within this genus with three main objectives in mind, (1) to test the monophyly of the genus; (2) to ascertain geographical origin and dispersal sequence; and (3) to test for monophyly within the most morphologically diverse species, S. torquata and S. caprata. We studied sequence data from the mitochondrial cytochrome b gene from 11 of the 12 recognized species and 15 of the 45 described subspecies. Four clades, two exclusively Asian, one Eurasian, and the fourth encompassing Eurasia and Africa, were identified. Based on our analyses, monophyly of the genus Saxicola is not supported and an Asian origin for the genus can be inferred. Results from DIVA analyses, tree topology and nodal age estimates suggest independent colonisation events from Asia to Africa and from Asia to the Western Palearctic, with the Sahara desert acting as a natural barrier for S. torquata. Subspecies and populations of S. torquata are not monophyletic due to S. tectes, S. dacotiae and S. leucura grouping within this complex. Subspecies and populations of S. caprata are monophyletic. Importantly, within S. torquata and S. caprata, slight morphological traits and plumage colour pattern differences used to recognize subspecies are indicative of the greater cryptic diversification that has occurred within this genus.     

Sillem's Mountain Finch Leucosticte sillemi is a valid species of rosefinch (Carpodacus,Fringillidae)

Sillem's Mountain Finch Leucosticte sillemi was described in 1992 on the basis of an adult and an immature specimen collected in western Tibet in September 1929, but its taxonomic validity and phylogenetic position have been unclear. Based on phylogenetic analysis of mitochondrial DNA from the holotype, we show that L. sillemi is not a colour morph of Brandt's Mountain Finch Leucosticte brandti but represents a valid, previously overlooked species of rosefinch (Carpodacus) that has secondarily acquired a pale plumage convergent on that of Leucosticte. Sillem's Mountain Finch is one of the least known species of bird and represents the only known species of rosefinch in which males have no reddish plumage coloration. This species and its sister taxon, the Tibetan Rosefinch Carpodacus roborowskii, are likely to be the world's highest‐altitude sister‐species pair of birds.     

Phylogeny of Laniarius: molecular data reveal L. liberatus synonymous with L. erlangeri and "plumage coloration" as unreliable morphological characters for defining species and species groups

Laniarius is one of the larger genera within the avian bush-shrike radiation, the family Malaconotidae. Fairly homogenous by size and shape but highly variable by colours, these have been classified mainly on basis of plumage colours. In the present study, which is the first taxon-dense analysis of the genus Laniarius based on molecular sequence data (nuclear BRM15 intron-15, and mitochondrial ND2 and ATPase6 genes), we investigate interrelationships between 16 species and 34 subspecies of Laniarius. Altogether 2094 bp were aligned and subjected to maximum likelihood and Bayesian inference analyses. Results strongly support the monophyly of Laniarius, and place it close to Chlorophoneus, but without outlining a precise sister-group. In a generally well-resolved phylogeny of Laniarius, L. leucorhynchus and L. atrococcineus constitute deep branches and the remaining species form five clades which are not concordant with previously defined superspecies. The black and white boubous belong to two different clades. L. aethiopicus appears polyphyletic and our results support the resurrection of Laniarius major, Laniarius erlangeri and Laniarius sublacteus. We also find that L. liberatus, described in 1991 based on the only known live individual, is identified as an unusual colour morph from L. erlangeri. The black boubous are not monophyletic; L. funebris and L. leucorhynchus appear as isolated species whereas L. poensis and L. fuelleborni are sister-taxa. We recovered the polyphyly of crimson boubous and new hypotheses on their relationships have been generated. Overall, the variation in pigments and patterns does not follow phylogenetic lineages. The plumage coloration could be thoroughly subject to modification and it could not reflect exactly colour plumages of the parents. From then on, the plumage coloration appears as an unreliable morphological character for defining species and species groups.     

Systematics of the parasitic wasp genus Yelicones Cameron (Hymenoptera: Braconidae: Rogadinae) and revision of the genus from the New World

Species of the braconid wasp genus Yelicones Cameron from North, Central and South America are revised and the first phylogenetic analysis of the world Yelicones fauna is presented. The results are considered from a biogeographical perspective and the effect of including and excluding colour characters is investigated. One hundred and twenty‐four species from throughout the world are recognised. Eighty‐five species are from the New World, 63 of which are new. A fully illustrated key to New World species is provided. A total of 116 characters were scored, of which 86 were morphological and 30 were based on the wasps’ colour pattern. All analyses show a near perfect diversion between New and Old World species. However, analyses excluding and including colour produced completely opposite results in terms of whether New or Old World species were basal. We found that in our data matrix colour characters performed at least as well as morphological characters in terms of their ensemble retention index, making it difficult to decide which phylogenetic hypotheses is correct. However, consideration of venom apparatus features leads us to prefer the hypotheses placing the New World taxa basally.     

Widespread polychromatism in female sunangel hummingbirds (Heliangelus: Trochilidae)

In hummingbirds, a showy gorget of iridescent throat feathers is a characteristic male ornament in many sexually dichromatic species. Given that polygynous breeding systems are the only ones observed in hummingbirds, and that polygyny is often associated with dramatic male ornamentation and sexual dimorphism, it is not surprising that gorgets are usually interpreted as sexual display characters. This proposition is challenged by exceptional 'polychromatic' species in which adult females diner in their development of a male-like gorget. This analysis focuses on determining the prevalence of polychromatic variation in the Andean genus Heliangelus. In eight of nine species, females' gorgets range from a dull plumage characteristic of most female hummingbirds (female-like), to a bright iridescent plumage that matches that of the males (male-like). Analysis of museum study-skins reveals that individual variation in gorget colour is limited to females, and that it is independent of month and year of collection. Only H. exortis and H. amethysticollis exhibit significant geographic variation in the frequencies of different colour forms, though most male-like female H. amethysticollis occur in southern Ecuador-northern Peru. Some species-specific features of the male-like females' gorget appear to be linked to qualities of the male gorget (presence/absence, colour and maximum size). However, non-adaptive hypotheses, including genetic correlation between the sexes, hybridization and neutral variation, cannot account for the plumage variation among females. The absence of any association between female gorget colour and breeding condition suggests that gorget colour has a non-sexual function. I propose that gorgets can evolve solely as a non-sexual signal associated with different foraging behaviours.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Genomic evidence for convergent evolution of a key trait underlying divergence in island birds

Reproductive isolation can be initiated by changes in one or a few key traits that prevent random mating among individuals in a population. During the early stages of speciation, when isolation is often incomplete, there will be a heterogeneous pattern of differentiation across regions of the genome between diverging populations, with loci controlling these key traits appearing the most distinct as a result of strong diversifying selection. In this study, we used Illumina‐sequenced ddRAD tags to identify genomewide patterns of differentiation in three recently diverged island populations of the Monarcha castaneiventris flycatcher of the Solomon Islands. Populations of this species have diverged in plumage colour, and these differences in plumage colour, in turn, are used in conspecific recognition and likely important in reproductive isolation. Previous candidate gene sequencing identified point mutations in MC1R and ASIP, both known pigmentation genes, to be associated with the difference in plumage colour between islands. Here, we show that background levels of genomic differentiation based on over 70,000 SNPs are extremely low between populations of distinct plumage colour, with no loci reaching the level of differentiation found in either candidate gene. Further, we found that a phylogenetic analysis based on these SNPs produced a taxonomy wherein the two melanic populations appear to have evolved convergently, rather than from a single common ancestor, in contrast to their original classification as a single subspecies. Finally, we found evidence that the pattern of low genomic differentiation is the result of both incomplete lineage sorting and gene flow between populations.     

Cryptic plumage signaling in Aphelocoma Scrub-Jays

Recent studies of avian vision and plumage coloration have revealed a surprising degree of cryptic sexual dimorphism, with many examples of male–female differences in UV reflectance that are invisible to humans. We examined the potential for male–female and adult–subadult differences in plumage coloration in the genus Aphelocoma. This group of jays comprises 10 phylogenetic species, which are found across southern and central North America and include cooperatively breeding species, as well as species that form socially monogamous pair-bonds typical of most species of birds. Our goal was to determine whether male–female and adult–subadult differences in plumage coloration were more common in species with complex social systems (i.e., cooperative breeders). We collected a series of reflectance measurements from hundreds of museum specimens and analyzed the results using a model of an avian visual system. We found that age- and sex-related differences were not more frequent in species that practice cooperative breeding. Hence, plumage signaling relating sex and age may not be strongly associated with complex social systems. Rather, the relative lack of a stable and familiar social environment, as well as other selective pressures and constraints (e.g., habitat use and plumage complexity), may have favored a greater degree of age- and sex-related differences in plumage coloration in jays that practice simple biparental care.     

Plumage-based phylogenetic analyses of the Merops bee-eaters

I review previous systematic work on the family Meropidae and present phylogenetic hypotheses derived from my analyses of colour, pattern and shape variation in 30 plumage regions among species and subspecies in this family. Consistent patterns are seen across shallow portions of the trees. Uncertainty remains concerning the placement of several deep branches within this group's phylogeny. In particular, the phylogenetic placement of Meropogon forsteni and Merops breweri , M. ornatus , M. hirundineus and M. boehmi remains uncertain. The biogeographical patterns in the resultant trees are similar with either a Southeast Asian or African origin for the family, with most of the early diversification occurring in Africa, and with multiple independent subsequent invasions of non-African areas.     

Morphological and plumage colour variation in the Réunion grey white‐eye (Aves: Zosterops borbonicus): assessing the role of selection

The Réunion grey white‐eye (Zosterops borbonicus), a small passerine endemic to the island of Réunion (Mascarene archipelago), constitutes an extraordinary case of phenotypic variation within a bird species, with conspicuous plumage colour differentiation at a microgeographical scale. To understand whether natural selection could explain such variability, we compared patterns of variation in morphological and plumage colour traits within and among populations. To quantify morphological variation, we used measurements obtained by Frank Gill in the 1960s from 239 individuals collected in 60 localities distributed over the entire island of Réunion. To quantify colour variation, we measured the reflectance spectra of plumage patches of 50 males from a subset of Gill's specimens belonging to the five recognized plumage colour variants and used a visual model to project these colours in an avian‐appropriate, tetrachromatic, colour space. We found that variants occupy different regions of the avian colour space and that between‐variant differences for most plumage patches could be discriminated by the birds. Differences in morphology were also detected, but these were, in general, smaller than colour differences. Overall, we found that variation in both plumage colour and morphology among variants is greater than would be expected if genetic drift alone was responsible for phenotypic divergence. As the plumage colour variants correspond to four geographical forms, our results suggest that phenotypic evolution in the Réunion grey white‐eye is at least partly explained by divergent selection in different habitats or regions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 459–473.     

Plumage coloration can be perceived as a multiple condition‐dependent signal by Great Tits Parus major

The evolution of multiple signals can be explained because they enhance the perception of a general message by recipients. Plumage coloration frequently acts as a condition‐dependent signal, so that species displaying different colour patches have the potential to transmit information on condition through a multiple signalling system. The Great Tit Parus major exhibits plumage colour patches generated by the main types of colour production, some of which, particularly those based on melanins and carotenoids, are known to be related to body condition. However, the colour expressions of all of the different colour types have never been investigated simultaneously to determine whether they function as multiple signals of condition. In addition, visual perception models have never been applied to a multiple signalling system in a wild population of birds. Here I present information that links body condition with the colour expression of almost all of the different plumage patches of male Great Tits captured during the winter. Birds in better condition had greater reflectance values at short wavelengths in all plumage patches, and this was especially so in the white (i.e. structural) colour of the cheeks. Plumage colour characteristics were calculated by means of avian visual models, suggesting that Great Tits have the capacity to perceive information contained in the plumage coloration of conspecifics. These results show that short‐wavelength reflectance has great potential to transmit biologically significant information on the body condition of birds, even in achromatic plumage patches.     

Phylogenetic relationships, diversification and biogeography in Neotropical Brotogeris parakeets

Aim We present a molecular phylogenetic analysis of Brotogeris (Psittacidae) using several distinct and complementary approaches: we test the monophyly of the genus, delineate the basal taxa within it, uncover their phylogenetic relationships, and finally, based on these results, we perform temporal and spatial comparative analyses to help elucidate the historical biogeography of the Neotropical region. Location Neotropical lowlands, including dry and humid forests. Methods Phylogenetic relationships within Brotogeris were investigated using the complete sequences of the mitochondrial genes cyt b and ND2, and partial sequences of the nuclear intron 7 of the gene for Beta Fibrinogen for all eight species and 12 of the 17 taxa recognized within the genus (total of 63 individuals). In order to delinetae the basal taxa within the genus we used both molecular and plumage variation, the latter being based on the examination of 597 skin specimens. Dates of divergence and confidence intervals were estimated using penalized likelihood. Spatial and temporal comparative analyses were performed including several closely related parrot genera. Results Brotogeris was found to be a monophyletic genus, sister to Myiopsitta. The phylogenetic analyses recovered eight well‐supported clades representing the recognized biological species. Although some described subspecies are diagnosably distinct based on morphology, there was generally little intraspecific mtDNA variation. The Amazonian species had different phylogenetic affinities and did not group in a monophyletic clade. Brotogeris diversification took place during the last 6 Myr, the same time‐frame as previously found for Pionus and Pyrilia. Main conclusions The biogeographical history of Brotogeris implies a dynamic history for South American biomes since the Pliocene. It corroborates the idea that the geological evolution of Amazonia has been important in shaping its biodiversity, argues against the idea that the region has been environmentally stable during the Quaternary, and suggests dynamic interactions between wet and dry forest habitats in South America, with representatives of the Amazonian biota having several independent close relationships with taxa endemic to other biomes.