An unexpectedly long history of sexual selection in birds-of-paradise
© Irestedt et al; licensee BioMed Central Ltd. 2009
Received: 15 May 2009
Accepted: 16 September 2009
Published: 16 September 2009
The birds-of-paradise (Paradisaeidae) form one of the most prominent avian examples of sexual selection and show a complex biogeographical distribution. The family has accordingly been used as a case-study in several significant evolutionary and biogeographical syntheses. As a robust phylogeny of the birds-of-paradise has been lacking, these hypotheses have been tentative and difficult to assess. Here we present a well supported species phylogeny with divergence time estimates of the birds-of-paradise. We use this to assess if the rates of the evolution of sexually selected traits and speciation have been excessively high within the birds-of-paradise, as well as to re-interpret biogeographical patterns in the group.
The phylogenetic results confirm some traditionally recognized relationships but also suggest novel ones. Furthermore, we find that species pairs are geographically more closely linked than previously assumed. The divergence time estimates suggest that speciation within the birds-of-paradise mainly took place during the Miocene and the Pliocene, and that several polygynous and morphologically homogeneous genera are several million years old. Diversification rates further suggest that the speciation rate within birds-of-paradise is comparable to that of the enitre core Corvoidea.
The estimated ages of morphologically homogeneous and polygynous genera within the birds-of-paradise suggest that there is no need to postulate a particularly rapid evolution of sexually selected morphological traits. The calculated divergence rates further suggest that the speciation rate in birds-of-paradise has not been excessively high. Thus the idea that sexual selection could generate high speciation rates and rapid changes in sexual ornamentations is not supported by our birds-of-paradise data. Potentially, hybridization and long generation times in polygynous male birds-of-paradise have constrained morphological diversification and speciation, but external ecological factors on New Guinea may also have allowed the birds-of-paradise to develop and maintain magnificent male plumages. We further propose that the restricted but geographically complex distributions of birds-of-paradise species may be a consequence of the promiscuous breeding system.
Birds-of-paradise (Paradisaeidae) are renowned for their complex courtships and diverse male plumages with highly elongated and elaborate feathers. Arguably, the birds-of-paradise form one of the most extravagant clades of all bird families in terms of beauty and display behaviour. The degree of sexual dimorphism found in the majority of species of birds-of-paradise (cryptically coloured females while males have spectacular ornamented plumages and elaborate courtship displays) is one of the most prominent avian examples of sexual selection. The birds-of-paradise also show complex biogeographical patterns, where most species and subspecies are locally and disjunctly distributed, sometimes in seemingly uniform and interconnected landscapes (summarized in ). Consequently, the family has been used as one of the earliest case-studies in significant evolutionary and biogeographical syntheses (e.g., [2–4]). Despite the evolutionary interest in the family, no comprehensive robust phylogeny of the birds-of-paradise exists.
Several incongruent phylogenetic hypotheses have been proposed for the birds-of-paradise based on both morphology [5–8] and molecular distances [9–11]. The only molecular phylogenetic study  lacks several genera and is based only on a single mitochondrial marker. Recent molecular studies have demonstrated that some taxa, traditionally considered to belong to the birds-of-paradise, are more closely related to other passerine clades. Thus, Macgregor's bird-of-paradise (Macgregoria pulchra) is a giant honeyeater , while the cnemophiline birds-of-paradise form a distinct lineage well separated from the true birds-of-paradise clade [13–15]. The lesser melampitta (Melampitta lugubris) and the silktail (Lamprolia victoriae) have also been proposed to be related to the birds-of-paradise [10, 16, 17], but are now confidently placed outside this clade [14, 15, 18].
The Fisherian runaway model of sexual selection [19, 20] suggests that sexual selection could generate a rapid and continual change in sexual ornaments, as few males get most of the mating and are free from constraints imposed by parental behaviour. In lekking species, sexual selection and dimorphism are expected to be even stronger (e.g., [3, 21]. The power of sexual selection to drive changes in mate recognition traits is also potentially a potent force in speciation (e.g., [22–25]). However, some models suggest that strong sexual selection may act against speciation .
Here we present a robust phylogenetic hypothesis and divergence time estimates for the birds-of-paradise (stricto sensu), based on both nuclear and mitochondrial sequence data. We use this i) to asses if the speciation rate and the evolution of sexually selected traits have been excessively high in the polygynous core birds-of-paradise, and ii) to examine biogeographical patterns and analyze the geographical differentiation in relation to sexually selected traits.
Taxon sampling, amplification and sequencing
Specimen data and Genbank accession numbers for samples used in the study.
King of Saxony Bird-of-Paradise
Drepanornis (Epimachus) bruijnii
Diphyllodes (Cicinnurus) respublica
Short-tailed Batis/Fernando Po Batis
MNHN CG 1998-783/ZMUC 02953
Hooded Crow/Carrion Crow
NRM 986167/MNHN CG 1995-41*
Spangled Drongo/Hair-crested Drongo
Lovely Fairy-wren/Superb Fairy-wren
ZMCU S458/FMNH 345690*
Blue-fronted Amazon/Maroon-bellied Parakeet
Amazona aestiva/Pyrrhura frontalis (Psittacidae)
NRM 966989, uncat*
Primers designed for this study.
Primer sequence (5' - 3')
TCA CAC AAA TTA TCA CAG GCC T
TCC TCC TAA CCC TAA TAG CAA C
CCT ACA CGA AAC AGG ATC AAA CAA
CTC CCC ATA TCA AAC CAG AAT GAT A
TCC GAC GAA GGC TGT TGC TAT TA
GGG GGT TGT TTG ATC CTG TTT C
TCG GAG GAT GGC GTA TGC AAA TAG
AAT GGA TGT TCG ACT GGT TGG CT
AAT CCC ACT GTG GAG TGA GAT TGT
GAPDH intron 11
AGG AGG CAG CTA CAG TAA TTT CAG GT
GAPDH intron 11
CAG ACC CAG AGA CCT TTG TTC A
ODC intron 6 and 7
GTA GCT TAC TTT GAC CAG CTT GGC A
ODC intron 6 and 7
AGT TGC CAA TTT TAG TGC ATC AGT
ODC intron 6 and 7
AAA CAG AGG TAA CTC ATG TTC AAG T
ODC intron 6 and 7
Phylogenetic analyses and estimation of speciation rates
We used Bayesian inference (see e.g., ) to estimate phylogenetic relationships. The models for nucleotide substitution used in the analyses were selected for each gene individually by applying the Akaike Information Criterion (AIC, Akaike ) using the program MrModeltest 2.2  in conjunction with PAUP* . Due to a rather low number of insertions in the non-coding nuclear loci the sequences could easily be aligned by eye. All gaps were treated as missing data in the analyses.
Posterior probabilities of trees and parameters in the substitution models were approximated with MCMC and Metropolis coupling using the program MrBayes 3.1.1 . Analyses were performed for the cytochrome b gene, a concatenated data set of the nuclear loci (GAPDH and ODC), and a concatenated data set of all genes. In the analyses of the concatenated data sets the models selected for the individual gene partitions were used. We used an unconstrained, exponential branch length prior. All chains were run for 25 million generations, with trees sampled every 100 generations. The trees sampled during the burn-in (i.e., before the chain had reached its apparent target distribution) were discarded, and after checking for convergence, final inference was made from the concatenated output from the two runs.
Sexual selection has been considered a driving force behind speciation [22–25]. By comparing speciation rates between clades with and without sexual selection it could be possible to investigate if sexual selection promotes speciation (e.g., [34–36]). The temporal variation in diversification rates is reflected by the variation in branch lengths in a chronogram and can be used to estimate the overall speciation rates as well as relative contribution of extinction . However, this requires taxonomically almost complete chronograms which is still lacking for the core Corvoidea. However, by using the methods described by Magallon and Sanderson  it is possible to estimate the diversification rate and the corresponding 95% confidence interval for the entire core Corvoidea, and compare this with the diversification rate of the polygynous birds-of-paradise. As the confidence interval will depend on the relative extinction rate (which is unknown) we calculated confidence intervals for both a high (ε = 0.90), and a zero (ε = 0) relative extinction rate. By using previously published phylogenies and divergence time estimates [39–41] it is possible to roughly estimate the divergence rates for Dicruridae and Monarchidae, two bird families closely related to the birds-of-paradise within the core Corvoidea assemblage. As the available divergence time estimates for these groups are based on other calibration points that suggest slightly different ages on comparable nodes, or only show relative age estimates, these estimates have been rescaled to be consistent with our chronogram. The rescaling was done by calculating the relative age between the two families, respectively, and the Corvus node (a node present in all trees) and multiply this age with our age estimate of the corresponding split. We consequently used the method to calculate diversification rates for crown groups .
Estimation of birds-of-paradise divergence times
We used a relaxed clock model implemented in Beast 1.4.7 [42–44] to estimate divergence times between phylogenetic lineages based on the concatenated dataset of all genes. To calibrate the tree we used the geological split between New Zealand and Antarctica, as it has been associated with the basal separation of the Acanthisitta-lineage from all other passerines [45, 46]. The dating of this split has often been assumed to be around 85-82 Mya [47, 48], but more recently the timing of this split has been suggested to be more uncertain, 85-65 Mya [49, 50]. In order to account for this uncertainty we used a normal distributed tree prior with a median at 76 Mya and a standard deviation of 8 (quintiles 2.5% = 60.3 Mya, 5% = 62.8 Mya, 95% = 89,2 Mya, 97.5% = 91.7 Mya). As for other priors, we used all default settings, except for the Tree Prior category that was set to Yule Process and an uncorrelated lognormal distribution for the molecular clock model. We used a GTR+Γ model and ran MCMC chains for 25 million generations.
Variation in the molecular data set, model selection
For all taxa 841 bp of the cytochrome b gene was sequenced. As we used partially overlapping primers the region covers a 868 bp region (ending 125 bp from the 3' end in the cytochrome b gene). Taking into account that for some taxa a few short fragments are missing, the alignments of the non-coding intron regions are 387 bp for GAPDH (the individual sequences ranged between 247-269 bp), and 685 bp for ODC (ranging between 577-619 bp for all taxa, except Corvus that, due to a large deletion, is only 429 bp). Some indels in more variable regions were found to be autapomorphic, while most other indels are congruent with the phylogenetic tree obtained from the analysis of the combined data set. The only exceptions are a 4 bp deletion shared between all Paradisaea and Monarcha and a 1 bp insertion shared by the Parotia-Pteridophora clade and some outgroup taxa in the GAPDH locus.
The trees obtained from the analyses of cytochrome b and the nuclear data sets receive less support than the tree obtained from the analysis of the concatenated data set. Nevertheless, several clades are recognized in all analyses, and conflicts exclusively concern weakly supported nodes (posterior probabilities < 0.95). Most deviant in relation to the combined tree is the sister relationship between Epimachus and Drepanornis (pp = 0.83) suggested only by the cytochrome b tree. In the cytochrome b tree Monarcha is also nested between the Manucodia, Phonygammus and Lycocorax clade and core birds-of-paradise (pp = 0.90).
Most nodes in our combined phylogeny receive strong support (pp > 0.95) and are often recovered by both the nuclear and the mitochondrial genes. Thus, we consider our combined phylogeny a reliable estimate of the evolutionary relationships among the birds-of-paradise.
Five main clades are recognized in our phylogeny (A-E in Figure 1). The first clade (A) consists of manucodes (Manucodia and Phonygammus) and the paradise crow (Lycocorax pyrrhopterus). This clade is supported as the sister group to the core birds-of-paradise (remaining genera). The king of Saxony bird-of-paradise (Pteridophora alberti) and parotias (Parotia) form the second clade (B). Within this clade P. carolae is highly divergent and warrants separate generic treatment.
The third clade (C) consists of the twelve-wired bird-of-paradise (Seleucidis melanoleuca), Drepanornis sicklebills, the standardwing bird-of-paradise (Semioptera wallacii), riflebirds (Ptiloris), and the superb bird-of-paradise (Lophorina superba). However, support for more basal nodes within this clade is low, and the affinity of the twelve-wired bird-of-paradise, Drepanornis sicklebills, and the standardwing bird-of-paradise should be regarded as provisional. Although support values are low, New Guinean Ptiloris and Lophorina form a clade separate from the Australian Ptiloris. This apparent relationship is worth investigating further as it suggests a significant phylogenetic break between Australia and New Guinea.
The fourth clade (D) includes sicklebills (Epimachus), paradigallas (Paradigalla) and astrapias (Astrapia). The fifth clade (E), consists of Paradisaea birds-of-paradise, Wilson's bird-of-paradise (Diphyllodes respublica), magnificent bird-of-paradise (Diphyllodes magnificus), and king bird-of-paradise (Cicinnurus regius). Within this clade the genera Diphyllodes and Cicinnurus are sister lineages, while the blue bird-of-paradise (Paradisaea rudolphi) is sister to other Paradisaea birds-of-paradise.
Divergence time estimates and speciation rates
Rates of diversification.
Nummer of species
Diversification rates (ε = 0)
Diversification rates (ε = 0.90)
Expected number of species (ε = 0)
Expected number of species (ε = 0.90)
Evolution of sexual dimorphism
Christidis and Schodde  postulated that the evolution of spectacular variation in male plumages in birds-of-paradise could be explained by female sexual selection for novel partners (but see [52, 53]). This model was proposed to explain the apparent rapid radiation of the birds-of-paradise. However, in the present study we find no evidence that sexual selection has promoted a particularly rapid morphological diversification [19, 20] or an exceptionally high rate of speciation [22–25] in birds-of-paradise.
Among passerine birds there is probably no other family with so many reported cases of interspecific and intergeneric hybrids in the wild as in the birds-of-paradise . For some genera where several species tend to have interconnected distributions, such as Paradisaea, gene flow through hybridization may have constrained speciation and phenotypic diversification. However, in most genera within core birds-of-paradise, species and subspecies are geographically well separated (i.e. Astrapia and Parotia), and modest speciation and phenotypic differentiation rates are thus difficult to explain by hybridization. Although little is known about the age when birds-of-paradise breed for the fist time, it is assumed that males of polygynous species do not reproduce until they have obtained full adult plumages, which happens several years later than in females . A longer generation time in polygynous male birds-of-paradise, compared to other passerine birds, may thus influence the inheritance rate of phenotypic characters in polygynous species of birds-of-paradise. Ecological factors, such as abundant food sources in New Guinea, may also explain that male birds-of-paradise have been able to develop and maintain promiscuous breeding, magnificent plumages and elaborate courtship displays.
Birds-of-paradise are among the few bird groups that have developed a social system based on promiscuous mating and arenas or leks . It is therefore notable that our phylogeny suggests that the degree of lekking behaviour (from large communal lekking to solitary display) varies considerably within the polygynous core birds-of-paradise, showing no clear phylogenetic structure (Figure 1). It is also notable that the strong sexual dimorphism within core birds-of-paradise has been lost in the genus Paradigalla.
Sexual behaviour and dispersal ability
Groups closely related to the birds-of-paradise, such as Monarchidae, Rhipiduridae and Dicruridae [41, 55–57] have all dispersed to other continents and remote oceanic islands. The birds-of-paradise on the other hand have only colonized islands within the New Guinea orogen, except two species (Lycocorax pyrrhopterus and Semioptera wallacii) inhabiting Halmahera and surrounding islands of the North Moluccas. The present distributions can largely be explained by vicariance, considering the fluctuating sea levels in the Late Miocene and Pliocene . This raises the question if the development of the special reproductive behaviour of birds-of-paradise may have constrained the capacity to disperse.
In four genera of birds-of-paradise the sexes are morphologically similar: Manucodia, Phonygammus, Paradigalla and Lycocorax. These species are monogamous and form pair bonds, which is quite unlike the promiscuous behaviour of the rest of the family. This less "spectacular" life strategy probably enabled these birds to have a higher dispersal capacity and could explain the present day occurrence of Manucodia and Phonygammus on several islands off the New Guinea coast and on Australia's Cape York Peninsula, and of Lycocorax on the North Moluccas. Paradigalla on the other hand is a genus restricted to the central New Guinean mountain range, which renders it less likely to disperse. The present day distribution of Semioptera wallacii in the North Moluccas is more difficult to explain. However, molecular clock estimates (Figure 2) suggest that it diverged from other birds-of-paradise in the late Miocene at a time when these islands, which are of oceanic origin, drifted close by the Vogelkop peninsula [59, 60].
We propose that the main reason why the core birds-of-paradise, unlike other corvoid bird families, have only diversified within New Guinea and islands in the immediate vicinity is linked with their promiscuous breeding system. It is likely that the costs not only involve handicaps associated with ornamental plumes and intensive displaying, but also involve a strong attachment to display sites . Furthermore, the fact that males and females live separately, except during mating time, means that successful long-distance dispersal and establishment of new breeding populations are less likely.
A similar sedentary life strategy, with limited dispersal outside mainland areas (and islands which have been connected with these areas) is evident in several other families with elaborate plumages, such as Phasianidae , Pipridae and the polygynous species within Cotingidae .
Patterns of speciation and diversification
Within several lineages of birds-of-paradise (Astrapia, Ptiloris and Paradigalla) there are distinct allopatric clades distributed in the east and the west of New Guinea, which separated about 3 - 6 million years ago (Figure 2). Allopatric speciation also appears to be the major mode of diversification within Paradisaea, which is a mainland lowland species complex that originated in the Pleistocene, while island species (P. rubra and P. decora) are slightly older. However, the divergences involving the mountain species (P. guilielmi and the highly divergent P. rudolphi) are much older. Within Ptiloris, the time separation of New Guinean and Australian taxa corresponds to broad land connections in the upper Miocene and marine transgression in the Pliocene .
Heads [63–65] has argued that present day distributions of birds-of-paradise in New Guinea are difficult to explain simply by Pleistocene refugia processes, and rather that biogeographical patterns should be seen in light of historic terrane movements over a longer time span. As support for this hypothesis he used three birds-of-paradise genera (Astrapia, Parotia, and Paradisaea) for which assumed sister relationships suggest a strong biogeographical connection between the Vogelkop and the Huon Peninsula in western and eastern New Guinea, respectively. Our phylogeny does not provide support for this biogeographical scenario. A sister relationship between Parotia sefilata in the Vogelkop and Parotia wahnesi on the Huon Peninsula is only weakly supported (PP = 0.59), and within the genus Astrapia our phylogeny strongly suggests sister relationships between species that occur in closely connected geographical areas (between Huon Peninsula and the Central Highlands, and between the Vogelkop and the Star Mountains). Within the genus Paradisaea, P. guiliemi from the Huon Peninsula is sister to all other Paradisaea species (except P. rudolphi, a morphologically rather divergent montane species) occupying almost all lowland areas in New Guinea.
The two species of Drepanornis as well as the two species of Epimachus separated about 10 and 7 million years ago, respectively. While the two species of Drepanornis occupy different elevations in low- and mid-montane forests, the two species of Epimachus are altitudinal replacements in mountain forests. Consequently, these two cases could represent old cases of altitudinal speciation. Parotia lawesii and Parotia helenae have similar patchy distributions as Epimachus across the mountains of New Guinea, and may represent a recent altitudinal speciation event. Examples of presumed altitudinal speciation in New Guinea have also been reported in Meliphagidae honeyeaters .
The phylogenetic results suggest that the birds-of-paradise could be subdivided into five main clades (A-E in Figure 1). Some of these clades confirm traditionally recognized relationships while others are novel hypotheses. The divergence time estimates further suggest that birds-of-paradise constitute an older clade than previously suggested. It appears that diversification within several genera of birds-of-paradise has been a continuous process through the Tertiary and that younger divergences are geographically rather closely linked. In addition to allopatric speciation, there appear to be some examples of altitudinal speciation. Particularly interesting is the observation that sexually dimorphic polygynous genera are morphologically homogeneous although divergences between species are suggested to be several million years old, and that calculations of diversification rates indicate that the speciation rate is not excessively high. Thus, sexual selection in birds-of-paradise appears not to have generated a particularly rapid change in sexual ornamentations or a markedly high speciation rate. Although the explanation remains uncertain, a long generation time in polygynous male birds-of-paradise and extensive hybridization may have constrained morphological diversifications and speciation. External ecological factors, such as abundant food sources in New Guinea, may also explain why male birds of paradise have been able to develop and maintain promiscuous breeding systems, magnificent plumages and elaborate courtship displays.
Foot pad samples were obtained from the Zoological Museum of Copenhagen (Jan Bolding Kristensen), the Swedish Museum of Natural History (Göran Frisk), and Australian Museum (Walter Boles). Jan Ohlson, Dario Zuccon, Love Dalén and three anonymous reviewers are thanked for comments on the manuscript. We also want to thank the staff at the Molecular Systematics Laboratory, Swedish Museum of Naturalhistory, for practical support. The laboratory work was funded by a grant to MI from Riksmusei vänner.
- Frith CB, Beehler BM: The Birds of Paradise. 1998, Oxford: Oxford University PressGoogle Scholar
- Wallace AR: The Malay archipelago: the land of the orang-utan and the birds of paradise. 1962, New York: Dover, Google Scholar
- Darwin C: The descent of man, and selection in relation to sex. 1871, London: MurrayGoogle Scholar
- Mayr E: Systematics and the origin of species. 1964, New York: DoverGoogle Scholar
- Stonor CR: Some features of the variation of the birds of paradise. Proc Zool Soc London. 1938, 107: 425-490.Google Scholar
- Mayr E: Birds of paradise. Nat Hist. 1945, 54: 264-276.Google Scholar
- Gilliard ET: Birds of Paradise and bower birds. 1969, London: Weidenfeld and NicolsonGoogle Scholar
- Diamond JM: Avifauna of the Eastern Highlands of New Guinea. 1972, Massachusetts: Nuttall Ornithological ClubGoogle Scholar
- Schodde R: Evolution in the birds-of-paradise and bowerbirds: A resynthesis. Proceedings of the 16th International Ornithological Congress: Canberra. Edited by: Frith HJ, Calaby JH. 1976, Canberra: Australian Academy of Science, 137-149.Google Scholar
- Sibley CG, Ahlquist JE: The phylogeny and classification of the Australo-Papuan passerine birds. Emu. 1985, 85: 1-14.View ArticleGoogle Scholar
- Christidis L, Schodde R: Relationships among the birds-of-paradise (Paradisaeidae) and bowerbirds (Ptilonorhynchidae): Protein evidence. Aust J Zool. 1992, 40: 343-353. 10.1071/ZO9920343.View ArticleGoogle Scholar
- Nunn GB, Cracraft J: Phylogenetic relationships among the major lineages of the Birds-of-Paradise (Paradisaeidae) using mitochondrial DNA gene sequences. Mol Phyl Evol. 1996, 5: 445-459. 10.1006/mpev.1996.0041.View ArticleGoogle Scholar
- Cracraft J, Feinstein J: What is not a bird of paradise? Molecular and morphological evidence places Macgregoria in the Meliphagidae and the Cnemophilinae near the base of the corvoid tree. Proc R Soc B. 2000, 267: 233-241. 10.1098/rspb.2000.0992.PubMed CentralView ArticlePubMedGoogle Scholar
- Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J: Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA. 2004, 101: 11040-11045. 10.1073/pnas.0401892101.PubMed CentralView ArticlePubMedGoogle Scholar
- Irestedt M, Ohlson JI: The division of the major songbird radiation into Passerida and "core Corvoidea" (Aves: Passeriformes) - the species tree versus gene trees. Zool Scr. 2008, 37: 305-313. 10.1111/j.1463-6409.2007.00321.x.View ArticleGoogle Scholar
- Cottrell GW: A problem species: Lamprolia victoriae. Emu. 1966, 66: 253-266.View ArticleGoogle Scholar
- Heather BD: The Vanua Levu Lamprolia (Lamprolia victoriae kleinschmidti): a preliminary look at its status and habits. Notornis. 1977, 24: 94-128.Google Scholar
- Irestedt M, Fuchs J, Jønsson KA, Ohlson JI, Pasquet E, Ericson PGP: Passeriformes) - an example of avian dispersal between New Guinea and Fiji over Miocene intermittent land bridges?. Mol Phyl Evol. 2008, 48: 1218-1222. 10.1016/j.ympev.2008.05.038.View ArticleGoogle Scholar
- Fisher RA: The evolution of sexual preference. Eugenics Review. 1915, 7: 184-192.PubMed CentralPubMedGoogle Scholar
- Fisher RA: The Genetical Theory of Natural Selection. 1930, Oxford: Clarendon PressView ArticleGoogle Scholar
- Payne RB: Sexual selection, lek and arena behavior and sexual size dimorphism in birds. Ornithol monogr. 1984, 33: 1-53.Google Scholar
- West-Eberhard M: Sexual selection, social competition, and speciation. Q Rev Biol. 1983, 58: 155-183. 10.1086/413215.View ArticleGoogle Scholar
- Coyne JA: Genetics and speciation. Nature. 1992, 355: 511-515. 10.1038/355511a0.View ArticlePubMedGoogle Scholar
- Panhuis TM, Butlin R, Zuk M, Tregenza T: Sexual selection and speciation. TREE. 2001, 16: 364-371.PubMedGoogle Scholar
- Seddon N, Merrill RM, Tobias JA: Sexually selected traits predicts patterns of species richness in a diverse clade of suboscine birds. Am Nat. 2008, 171: 620-631. 10.1086/587071.View ArticlePubMedGoogle Scholar
- Ritchie MG: Sexual selection and speciation. Annu Rev Ecol Evol Syst. 2007, 38: 79-102. 10.1146/annurev.ecolsys.38.091206.095733.View ArticleGoogle Scholar
- Monroe BL, Sibley CG: A World Checklist of Birds. 1993, New Haven and London: Yale University PressGoogle Scholar
- Irestedt M, Ohlson JI, Zuccon D, Källersjö M, Ericson PGP: Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World suboscines (Aves, Passeriformes). Zool Scr. 2006, 35: 567-580. 10.1111/j.1463-6409.2006.00249.x.View ArticleGoogle Scholar
- Holder M, Lewis PO: Phylogeny estimation: Traditional and Bayesian approaches. Nat Genet. 3003, 4: 275-284.View ArticleGoogle Scholar
- Akaike H: Information theory as an extension of the maximum likelihood principle. Second International Symposium on Information Theory. Edited by: Petrov BN, Csaki F. 1973, Budapest: Akademiai Kiado, 267-281.Google Scholar
- Nylander JAA: MrModeltest v.2. 3. Program distributed by the author. 2008, Evolutionary Biology Centre, Uppsala University, UppsalaGoogle Scholar
- Swofford DL: PAUP*. Phylogenetic analysis using parsimony (*and other methods). version 4. 1988, Sunderland, Massachusetts: Sinauer AssociatesGoogle Scholar
- Ronquist F, Huelsenbeck JP: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.View ArticlePubMedGoogle Scholar
- Barraclough TG, Harvey PH, Nee S: Sexual selection and taxonomic diversity in passerine birds. Proc R Soc London B Biol Sci. 1995, 259: 211-215. 10.1098/rspb.1995.0031.View ArticleGoogle Scholar
- Mitra S, Landel H, Pruett-Jones S: Species richness covaries with mating system in birds. Auk. 1996, 113: 544-551.View ArticleGoogle Scholar
- Hodges SA, Arnold ML: Spurring plant diversification: are floral nectar spurs a key innovation?. Proc R Soc London B Biol Sci. 1995, 262: 343-348. 10.1098/rspb.1995.0215.View ArticleGoogle Scholar
- Rabosky DL, Lovette IJ: Explosive evolutionary radiations: decreasing speciation or increasing extinction through time?. Evolution. 2008, 62: 1866-1875. 10.1111/j.1558-5646.2008.00409.x.View ArticlePubMedGoogle Scholar
- Magallón S, Sanderson MJ: Absolute diversification rates in angiosperm clades. Evolution. 2001, 55: 1762-1780.View ArticlePubMedGoogle Scholar
- Filardi CE, Moyle RG: Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature. 2005, 438: 216-219. 10.1038/nature04057.View ArticlePubMedGoogle Scholar
- Fuchs J, Cruaud C, Couloux A, Pasquet E: Complex biogeographic history of the cuckoo-shrikes and allies (Passeriformes: Campephagidae) revealed by mitochondrial and nuclear sequence data. Mol Phyl Evol. 2007, 44: 138-153. 10.1016/j.ympev.2006.10.014.View ArticleGoogle Scholar
- Pasquet E, Pons J-M, Fuchs J, Cruaud C, Bretagnolle V: Evolutionary history and biogeography of the drongos (Dicruridae), a tropical Old World clade of corvoid passerines. Mol Phyl Evol. 2007, 45: 158-167. 10.1016/j.ympev.2007.03.010.View ArticleGoogle Scholar
- Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W: Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics. 2002, 161: 1307-1320.PubMed CentralPubMedGoogle Scholar
- Drummond AJ, Ho SYW, Phillips MJ, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biology. 2006, 4: e88-10.1371/journal.pbio.0040088.PubMed CentralView ArticlePubMedGoogle Scholar
- Rambaut A, Drummond AJ: Tracer v1.4. 2007, [http://tree.bio.ed.ac.uk/software/tracer/]Google Scholar
- Barker KF, Barrowclough GF, Groth JG: A phylogenetic analysis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc R Soc Lond B. 2002, 269: 295-305. 10.1098/rspb.2001.1883.View ArticleGoogle Scholar
- Ericson PGP, Christidis L, Cooper A, Irestedt M, Jackson J, Johansson US, Norman JA: A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc R Soc Lond B. 2002, 269: 235-241. 10.1098/rspb.2001.1877.View ArticleGoogle Scholar
- Lawver LA, Royer JY, Sandwell DT, Scotese CR: Evolution of the Antarctic continental margins. Geological Evolution of Antarctica. Edited by: Thomson MRA, Crame JA, Thomson JW. 1991, Cambridge: Cambridge University Press, 533-539.Google Scholar
- Cooper RA, Millener P: The New Zealand biota: historical background and new research. Trends Ecol Evol. 1993, 8: 429-433. 10.1016/0169-5347(93)90004-9.View ArticlePubMedGoogle Scholar
- McLoughlin S: The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Aust J Bot. 2001, 49: 271-300. 10.1071/BT00023.View ArticleGoogle Scholar
- Ladiges PY, Cantrill D: New Caledonia-Australian connection: biogeographic patterns and geology. Aust Syst Bot. 2007, 20: 383-389. 10.1071/SB07018.View ArticleGoogle Scholar
- Christidis L, Schodde R: Sexual selection for novel partners: a mechanism for accelerated morphological evolution in the birds-of-paradise (Paradisaeidae). Bull Br Ornithol Club. 1993, 113: 169-172.Google Scholar
- LeCroy M, Kulupi A, Peckover WS: Goldie's bird of paradise: Display, natural history, and traditional relationships to people to the bird. Wilson Bull. 1980, 92: 289-301.Google Scholar
- LeCroy M: The genus Paradisaea - display and evolution. Am Mus Novit. 1981, 2714: 1-52.Google Scholar
- Lack D: Ecological adaptations for breeding in birds. 1968, London: MethuenGoogle Scholar
- Jønsson KA, Irestedt M, Fuchs J, Ericson PGP, Christidis L, Bowie RCK, Norman JA, Pasquet E, Fjeldså J: Explosive Avian Radiations and Multi-directional Dispersal across Wallacea: Evidence from the Campephagidae and other Crown Corvida (Aves). Mol Phyl Evol. 2008, 47: 221-236. 10.1016/j.ympev.2008.01.017.View ArticleGoogle Scholar
- Norman JA, Ericson PGP, Jønsson KA, Fjeldså J, Christidis L: A multi-gene phylogeny reveals novel relationships for aberrant genera of Australo-Papuan core Corvoidea and polyphyly of the Pachycephalidae and Psophodidae (Aves: Passeriformes). Mol Phyl Evol. 2009, 52: 488-497. 10.1016/j.ympev.2009.03.019.View ArticleGoogle Scholar
- Nyari AS, Benz BW, Jønsson KA, Fjeldså J, Moyle RG: Phylogenetic relationships of fantails (Aves: Rhipiduridae). Zool Scr.
- Chappell JMA: Late Quaternary sea-level changes in the Australian region. Sea-level changes. Edited by: Tooley MJ, Shennan I. 1987, Oxford: Institute of British Geographers Special Publication 20, Basil Blackwell, 296-331.Google Scholar
- Hall R: The plate tectonics of the Cenozoic SE Asia and the distribution of land and sea. Biogeography and geological Evolution of SE Asia. Edited by: Hall R, Holloway JD. 1998, Leiden: Backhuys Publishers, 133-163.Google Scholar
- Hall R: Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J Asian Earth Sci. 2002, 20: 353-431. 10.1016/S1367-9120(01)00069-4.View ArticleGoogle Scholar
- McGowan PJK: Family Phasianidae (Pheasants and partridges). Handbook of the Birds of the World. New World Vultures to Guineafowl. Edited by: del Hoyo J, Elliott A, Sargatal J. 1994, Barcelona: Lynx Edicions, 2: 434-553.Google Scholar
- del Hoyo J, Elliot A, Christie DA: Handbook of the Birds of the World. Cotingas to Pipits and Wagtails. 2004, Barcelona: Lynx Ediciones, 9:Google Scholar
- Heads M: Birds of paradise, biogeography and ecology in New Guinea: a review. J Biogeogr. 2001, 28: 893-927. 10.1046/j.1365-2699.2001.00600.x.View ArticleGoogle Scholar
- Heads M: Birds of paradise and bowerbirds: regional levels of biodiversity and terrance tectonics in New Guinea. J Zool. 2001, 255: 331-339. 10.1017/S0952836901001431.View ArticleGoogle Scholar
- Heads M: Birds of paradise, vicariance biogeography and terrane tectonics in New Guinea. J Biogeogr. 2002, 29: 261-283. 10.1046/j.1365-2699.2002.00667.x.View ArticleGoogle Scholar
- Norman JA, Rheindt FE, Rowe DL, Christidis L: Speciation dynamics in the Australo-Papuan Meliphaga honeyeaters. Mol Phyl Evol. 2007, 42: 80-91. 10.1016/j.ympev.2006.05.032.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.