An unexpectedly long history of sexual selection in birds-of-paradise

  • Martin Irestedt1Email author,

    Affiliated with

    • Knud A Jønsson2,

      Affiliated with

      • Jon Fjeldså2,

        Affiliated with

        • Les Christidis3, 4 and

          Affiliated with

          • Per GP Ericson1

            Affiliated with

            BMC Evolutionary Biology20099:235

            DOI: 10.1186/1471-2148-9-235

            Received: 15 May 2009

            Accepted: 16 September 2009

            Published: 16 September 2009

            Abstract

            Background

            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.

            Results

            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.

            Conclusion

            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.

            Background

            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 [1]). Consequently, the family has been used as one of the earliest case-studies in significant evolutionary and biogeographical syntheses (e.g., [24]). 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 [58] and molecular distances [911]. The only molecular phylogenetic study [12] 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 [13], while the cnemophiline birds-of-paradise form a distinct lineage well separated from the true birds-of-paradise clade [1315]. 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., [2225]). However, some models suggest that strong sexual selection may act against speciation [26].

            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.

            Methods

            Taxon sampling, amplification and sequencing

            We examined the phylogenetic relationship among birds-of-paradise by analyzing DNA sequence data from the mitochondrial cytochrome b gene and the two nuclear loci ornithine decarboxylase introns 6 to 7 (ODC), and glyceraldehyde-3-phosphodehydrogenase intron 11 (GAPDH). The taxon sampling includes all 40 species of birds-of-paradise recognized by Monroe and Sibley [27], omitting the genera Loboparadisea, Cnemophilus, Melampitta and Macgregoria, which have been shown to not be part of the birds-of-paradise clade [1315]. The taxon sampling also includes Corvus cornix and Monarcha melanopsis, two taxa representing lineages that have been suggested to be closely related to the birds-of-paradise [14]. Three additional but more distantly related representatives of core Corvoidea as well as representatives from other major passerine lineages were also included. A representative from Psittacidae, the sister group to passerine birds, was used to root the trees. See Table 1 for the taxon sampling and GenBank accession numbers.
            Table 1

            Specimen data and Genbank accession numbers for samples used in the study.

            Vernacular name

            Scientific name

            Sample id.

            G3P

            ODC

            Cyt b

            Paradise-crow

            Lycocorax pyrrhopterus

            NRM 569570

            GQ334294

            GQ334259

            GQ334221

            Glossy-mantled Manucode

            Manucodia ater

            NRM 566764

            EU726210

            EU726228

            GQ334222

            Jobi Manucode

            Manucodia jobiensis

            ZMUC100048

            GQ334295

            GQ334260

            GQ334223

            Curl-crested Manucode

            Manucodia comrii

            uncat.*

              

            U15207

            Crinkle-collared Manucode

            Manucodia chalybatus

            NRM 566755

            GQ334296

            GQ334261

            GQ334224

            Trumpet Manucode

            Phonygammus (Manucodia) keraudrenii

            NRM 566775

            GQ334297

            GQ334262

            GQ334225

            Long-tailed Paradigalla

            Paradigalla carunculata

            ZMUC100049

            GQ334298

            GQ334263

            GQ334226

            Short-tailed Paradigalla

            Paradigalla brevicauda

            NRM 566736

            GQ334299

            GQ334264

            GQ334227

            Arfak Astrapia

            Astrapia nigra

            NRM 551602

            GQ334300

            GQ334265

            GQ334228

            Splendid Astrapia

            Astrapia splendidissima

            NRM 569961

            GQ334301

            GQ334266

            GQ334229

            Stephanie's Astrapia

            Astrapia stephaniae

            NRM 551677

            GQ334302

            GQ334267

            GQ334230

            Ribbon-tailed Astrapia

            Astrapia mayeri

            AM O.45772

            GQ334303

            GQ334268

            GQ334231

            Huon Astrapia

            Astrapia rothschildi

            ZMUC 100463

            GQ334304

            GQ334269

            GQ334232

            Western Parotia

            Parotia sefilata

            NRM 561818

            GQ334305

            GQ334270

            GQ334233

            Carola's Parotia

            Parotia carolae

            NRM 566752

            GQ334306

            GQ334271

            GQ334234

            Lawes' Parotia

            Parotia lawesii

            NRM 569963

            GQ334307

            GQ334272

            GQ334235

            Eastern Parotia

            Parotia helenae

            ZMUC100047

            GQ334308

            GQ334273

            GQ334236

            Wahnes's Parotia

            Parotia wahnesi

            ZMUC 100462

            GQ334309

            GQ334274

            GQ334237

            King of Saxony Bird-of-Paradise

            Pteridophora alberti

            NRM 566740

            GQ334310

            GQ334275

            GQ334238

            Superb Bird-of-Paradise

            Lophorina superba

            NRM 566745

            GQ334311

            GQ334276

            GQ334239

            Paradise Riflebird

            Ptiloris paradiseus

            ZMUC 100062

            GQ334312

            GQ334277

            GQ334240

            Victoria's Riflebird

            Ptiloris victoriae

            ZMUC100043

            GQ334313

            GQ334278

            GQ334241

            Magnificent Riflebird

            Ptiloris magnificus

            NRM 569616

            EU726211

            EU726229

            GQ334242

            Growling Riflebird

            Ptiloris intercedens

            ZMUC100040

            GQ334314

            GQ334279

            GQ334243

            Black Sicklebill

            Epimachus fastuosus

            NRM 551601

            GQ334315

            GQ334280

            GQ334244

            Brown Sicklebill

            Epimachus meyeri

            NRM 569995

            GQ334316

            GQ334281

            GQ334245

            Buff-bailed Sicklebill

            Drepanornis (Epimachus) albertisi

            MV C148

            EU380475

            EU380436

            U15205

            Pale-billed Sicklebill

            Drepanornis (Epimachus) bruijnii

            ZMUC100045

            GQ334317

            GQ334282

            GQ334246

            Magnificent Bird-of-Paradise

            Diphyllodes (Cicinnurus) magnificus

            NRM 569677

            GQ334318

            GQ334283

            GQ334247

            Wilson's Bird-of-Paradise

            Diphyllodes (Cicinnurus) respublica

            NRM 566767

            GQ334319

            GQ334284

            GQ334248

            King Bird-of-Paradise

            Cicinnurus regius

            NRM 569661

            GQ334320

            GQ334285

            GQ334249

            Standardwing Bird-of-Paradise

            Semioptera wallacii

            ZMUC100061

            GQ334321

            GQ334286

            GQ334250

            Twelve-wired Bird-of-Paradise

            Seleucidis melanoleucus

            NRM 552057

            GQ334322

            GQ334287

            GQ334251

            Greater Bird-of-Paradise

            Paradisaea apoda

            ZMUC64493

            GQ334323

            GQ334288

            GQ334252

            Raggiana Bird-of-Paradise

            Paradisaea raggiana

            ZMUC100039

            GQ334324

            GQ334289

            GQ334253

            Lesser Bird-of-Paradise

            Paradisaea minor

            NRM 700230

            GQ334325

            GQ334290

            GQ334254

            Red Bird-of-Paradise

            Paradisaea rubra

            NRM 700233

            GQ334326

            GQ334291

            GQ334255

            Goldie's Bird-of-Paradise

            Paradisaea decora

            AM A.14473

              

            GQ334256

            Emperor Bird-of-Paradise

            Paradisaea guilielmi

            ZMUC100041

            GQ334327

            GQ334292

            GQ334257

            Blue Bird-of-Paradise

            Paradisaea rudolphi

            ZMUC100060

            GQ334328

            GQ334293

            GQ334258

            Short-tailed Batis/Fernando Po Batis

            Batis mixta/poensis

            MNHN CG 1998-783/ZMUC 02953

            DQ406665

            EU272120

            DQ011862

            Hooded Crow/Carrion Crow

            Corvus cornix/corone

            NRM 986167/MNHN CG 1995-41*

            DQ406663

            EU272116

            AY228087

            Spangled Drongo/Hair-crested Drongo

            Dicrurus bracteatus/hottentottus

            UBMW 68045/uncat.*

            EF052813

            EU272113

            EF113121

            Australian magpie

            Gymnorhina tibicen

            MV AC78/uncat.*

            DQ406669

            EU27119

            AF197867

            Black-faced Monarch

            Monarcha melanopsis

            MV B541

            EU272089

            EU272114

            FJ821128

            Tree Sparrow

            Passer montanus

            NRM 976359

            AY336586

            DQ785937

            AY228073

            Lovely Fairy-wren/Superb Fairy-wren

            Malurus amabalis/cyaneus

            MV C803/uncat.*

            EF441219

            EF441241

            AF197845

            Superb Lyrebird

            Menura novaehollandiae

            MV F722

            EF441220

            EF441242

            AY064276

            Yellow-bellied Elaenia

            Elaenia flavogaster

            NRM 966970

            DQ435464

            DQ435480

            AF453807

            Variable Antshrike

            Thamnophilus caerulescens

            NRM 967007

            AY336587

            DQ435504

            AY078176

            Velvet Asity

            Philepitta castanea

            ZMCU S458/FMNH 345690*

            AY336591

            DQ785938

            AY065726

            Rifleman

            Acanthisitta chloris

            NRM 569989

            EU726202

            EU726220

            AY325307

            Blue-fronted Amazon/Maroon-bellied Parakeet

            Amazona aestiva/Pyrrhura frontalis (Psittacidae)

            NRM 966989, uncat*

            AY194432

            DQ881775

            AY751643

            Acronyms: NRM = Swedish Museum of Natural History, Stockholm; ZMUC = Zoological Museum of the University of Copenhagen. All samples excect those marked with an asterisk are from vouchered specimens.

            For extractions, amplifications, and sequencing procedures from study skin samples we followed the procedures described in Irestedt et al. [28]. Several new primers were also designed (Table 2).
            Table 2

            Primers designed for this study.

            Primer name

            Primer sequence (5' - 3')

            Region

            Cytb-BopF1

            TCA CAC AAA TTA TCA CAG GCC T

            Cytochrome b

            Cytb-BopF2

            TCC TCC TAA CCC TAA TAG CAA C

            Cytochrome b

            Cytb-BopF3

            CCT ACA CGA AAC AGG ATC AAA CAA

            Cytochrome b

            Cytb-BopF4

            CTC CCC ATA TCA AAC CAG AAT GAT A

            Cytochrome b

            Cytb-BopR1

            TCC GAC GAA GGC TGT TGC TAT TA

            Cytochrome b

            Cytb-BopR2

            GGG GGT TGT TTG ATC CTG TTT C

            Cytochrome b

            Cytb-BopR3

            TCG GAG GAT GGC GTA TGC AAA TAG

            Cytochrome b

            Cytb-BopR4

            AAT GGA TGT TCG ACT GGT TGG CT

            Cytochrome b

            G3P-BopintF1

            AAT CCC ACT GTG GAG TGA GAT TGT

            GAPDH intron 11

            G3P-BopintR1

            AGG AGG CAG CTA CAG TAA TTT CAG GT

            GAPDH intron 11

            ODC-Bop-F2

            CAG ACC CAG AGA CCT TTG TTC A

            ODC intron 6 and 7

            ODC-Bop-F3

            GTA GCT TAC TTT GAC CAG CTT GGC A

            ODC intron 6 and 7

            ODC-Bop-R1

            AGT TGC CAA TTT TAG TGC ATC AGT

            ODC intron 6 and 7

            ODC-Bop-R3

            AAA CAG AGG TAA CTC ATG TTC AAG T

            ODC intron 6 and 7

            The primers have been designed to amplify short regions (~200-300 bp) from degraded DNA obtained from museum study skin samples.

            Phylogenetic analyses and estimation of speciation rates

            We used Bayesian inference (see e.g., [29]) 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 [30]) using the program MrModeltest 2.2 [31] in conjunction with PAUP* [32]. 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 [33]. 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 [2225]. By comparing speciation rates between clades with and without sexual selection it could be possible to investigate if sexual selection promotes speciation (e.g., [3436]). 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 [37]. 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 [38] 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 [3941] 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 [38].

            Estimation of birds-of-paradise divergence times

            We used a relaxed clock model implemented in Beast 1.4.7 [4244] 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.

            Results

            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 prior selection of substitution models supported the GTR+I+Γ model for cytochrome b, the HKY+ Γ for GAPDH, and GTR+Γ for ODC. After discarding the burn-in phase the final inference was based on a total of 200 000-225 000 samples from the posterior for all conducted Bayesian analyses. For the phylogenetic inference of the concatenated data set of all genes, the mode of the posterior distribution of topologies is presented as a 50% majority-rule consensus tree (Figure 1).
            http://static-content.springer.com/image/art%3A10.1186%2F1471-2148-9-235/MediaObjects/12862_2009_Article_1149_Fig1_HTML.jpg
            Figure 1

            Phylogenetic relationships of the birds-of-paradise. The 50% majority rule consensus tree obtained from the analyses of the combined data set (cytochrome b, ornithine decarboxylase introns 6 and 7, and glyceraldehyde-3-phosphate dehydrogenase intron 11). Posterior probability values are indicated above the nodes, posterior probability values of 1.00 are indicated with an asterisk. Male display strategies in core birds-of-paradise according to (Frith and Behler 1998) are indicated by boxes to the right of the taxon names (red = lek, blue = exploded lek, black = solitary). Question marks to the right of the boxes indicate that display strategy is not fully established.

            Phylogenetic relationships

            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

            All nodes supported by posterior probabilities above 0.95 in the tree obtained from the Bayesian analyses of the concatenated data set of all genes (Figure 1) are recognized in the chronogram. The chronogram and divergence time estimates are shown in Figure 2. The split between the Manucodia/Lycocorax clade and core birds-of-paradise clade is estimated to have occurred around 24 million years ago, while the basal divergence of the polygynous core birds-of-paradise is suggested to be around 15 million years old. The age estimates further suggest that generic separations occurred between 6 and14 million years ago, while speciation within genera mostly occurred between 0.5 and 10 million years ago.
            http://static-content.springer.com/image/art%3A10.1186%2F1471-2148-9-235/MediaObjects/12862_2009_Article_1149_Fig2_HTML.jpg
            Figure 2

            Chronogram with divergence times estimates of the birds-of-paradise. The divergence times and confidence intervals (grey bars) were estimated under a relaxed clock model implemented in Beast 1.4.7 [33]. For the calibration of the chronogram the postulated separation of Acanthisitta from all other passerines in the phylogeny was used.

            The calculated diversification rates and the 95% confidence intervals based on the mean diversification rate for the core Corvoidea at a relative extinction rates of ε = 0 and ε = 0.90 are shown in Table 3 (expressed as expected number of species). The results suggest that the speciation rates within the entire birds-of-paradise clade as well as within the restricted polygynous core birds-of-paradise fall within the 95% confidence intervals for the core Corvoidea at both low (ε = 0) and high (ε = 0.90) relative extinction rates.
            Table 3

            Rates of diversification.

            Clade

            Nummer of species

            Age

            Diversification rates (ε = 0)

            Diversification rates (ε = 0.90)

            Expected number of species (ε = 0)

            Expected number of species (ε = 0.90)

            Birds-of-paradise

            40

            23.8

            0,13

            0,06

            2-131

            4-455

            core birds-of-paradise

            34

            15.1

            0,19

            0,09

            1-35

            2-156

            Monarchidae

            ~130

            ~10.6

            ~0,39

            ~0,24

            ~1-17

            ~1-83

            Dicuridae

            ~24

            ~20.0

            ~0,12

            ~0,06

            ~2-74

            ~3-290

            core Corvoidae

            755

            39.5

            0,15

            0,11

            11-1402

            19-2658

            Absolute rate of diversification for the entire birds-of-paradise clade, core (polygynous) birds-of-paradise, some closely related families, and core Corvoidea, estimated in absence of extinction (ε = 0) and comparatively high (ε = 0.90) relative extinction rate. The 95% confidence intervals at relative extinction rates of ε = 0 and ε = 0.90 are expressed as expected number of species for each clade. The 95% confidence intervals have been calculated as described by Magallon and Sanderson [Magallon and Sanderson 2001] and is based mean diversification rate for the core Corvoidea (at a relative extinction rates of ε = 0 and ε = 0.90) and the age of the clades.

            Discussion

            Evolution of sexual dimorphism

            Our divergence time estimates suggest that the birds-of-paradise originated approximately 24 million years ago, which renders the family older than previously suggested by DNA-DNA hybridization data [10] and allozyme data [9, 11]. Particularly noticeable is the old age (ca 15 My) of the sexually dimorphic and polygynous core birds-of-paradise. Although the variation in male plumage ornamentations is astonishing within the core birds-of-paradise (Figure 3), most of this variation is found between genera that diverged around 10 million years ago. More interesting is that morphologically homogeneous genera seem to be quite old. One of the most prominent examples is the genus Paradisaea. In this genus all lekking species are morphologically very homogeneous although the age of the genus is found to be more than 6 million years old (the split between P. guilielmi and other lekking Paradisaea species). Similarly, the morphological variation is modest within the genus Parotia, for which the exploded lekking system is estimated to be around 10 million years old. Other sexually dimorphic and polygynous genera such as Ptiloris and Astrapia also show little morphological diversification between species. The calculated diversification rates (Table 3) further indicate that the speciation rate in core birds-of-paradise is not excessively high. In fact the speciation rate seems to be more similar to the speciation rate found for the sexually monomorphic drongos (Dicruridae) than to the speciation rate found for the sexually dimorphic monarch flycatchers (Monarchidae).
            http://static-content.springer.com/image/art%3A10.1186%2F1471-2148-9-235/MediaObjects/12862_2009_Article_1149_Fig3_HTML.jpg
            Figure 3

            Examples of plumage diversity and sexual dimorphism in birds-of-paradise. Lower left male and female of the monogamous Manucodia keraudrenii, lower right male and two females of Parotia carolae, center left male and female Pteridophora alberti, top left male and female Paradisaea rubra, and top right male and female Diphyllodes magnificus.

            Christidis and Schodde [51] 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 [2225] 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 [1]. 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 [1]. 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 [54]. 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, 5557] 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 [58]. 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 [1]. 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 [61], Pipridae and the polygynous species within Cotingidae [62].

            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 [59].

            Heads [6365] 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 [66].

            Conclusion

            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.

            Declarations

            Acknowledgements

            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.

            Authors’ Affiliations

            (1)
            Molecular Systematics Laboratory, Swedish Museum of Natural History
            (2)
            Vertebrate Department, Zoological Museum, University of Copenhagen
            (3)
            Division of Research and Collections, Australian Museum
            (4)
            Department of Genetics, University of Melbourne

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            Copyright

            © Irestedt et al. 2009

            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.

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