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Tyrant ßycatchers coming out in the open: phylogeny and ecological radiation of Tyrannidae (Aves, Passeriformes) J AN O HLSON , J ON F JELDSÅ et al.Phylogeny and ecological radiation of Tyrannidae© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters¥Zoologica Scripta, , 3, May 2008, pp 315Ð335 and assemblages), were especiallyM. inornatus lacking. Mecocerculus calopterus and M. leucophrysTyranniscusAcrochordopus and Oreotriccus by Traylor (1977), but Lanyon(1988b) did not recover them as a monophyletic group. Toobtain an initial assessment of the relationships between these and Tyranniscusvirescens RamphotrigonTityra and Schiffornisspecimens, we found that NRM 976683 referred to as in Ericson with the QIAamp® Mini Kit (QIAGEN®, Valencia, CA),following the protocol provided by the manufacturer.glyceraldehyde-3-phosphate dehydrogenase intron 11 (G3PDH),Allen & Omland (2003), respectively. DNA was obtained from. (2006a). Primers used are listed in Table 1.plete sequences with SeqMan II’ (DNASTAR Inc., Madison,MegAlign’ (DNASTAR Inc.), using the Clustal V algorithmPhylogenetic trees were estimated using parsimony (Farris 1997).Primer nameUsePrimer sequence (5)ReferenceG3P-13bATCC ACC TTT GAT GCG GGT GCT GGC ATFjeldsŒ . (2003)G3P-14bA, SAAG TCC ACA ACA CGG TTG CTG TAFjeldsŒ . (2003)G3PintL1SGAA CGA CCA TTT TGT CAA GCT GGT TFjeldsŒ . (2003)Myo2A, SGCC ACC AAG CAC AAG ATC CCSlade . (1993)Myo3ACGG AAG AGC TCC AGG GCC TTHeslewood . (1998)Myo3FA, STTC AGC AAG GAC CTT GAT AAT GAC TTHeslewood . (1998)MyoIntCSAGC CCT GGA GGA TCC ATT GGIrestedt . (2002)MyoIntNCSCCA ATG GAT CCT CCA GGG CTIrestedt . (2002)Myo309LA, SCAT AAG ACC TGT CAG TGG CTG GAIrestedt . (2006a)MyoNso030LA, SATC TGG AGG TAT GGA AAA GGG CAIrestedt . (2006a)MyoSub149LA, SGTA CAG GCA GCA GGA GGC ACA GAThis studyMyoSub218HA, SGCA TGT GGT GTT TGG AAT GGG AAIrestedt . (2006a)MyoTyr345HA, SCCT CTA GGG CTT GCT CTA AAA TTG TAThis studyOD6A, SGAC TCC AAA GCA GTT TGT CGT CTC AGT GTAllen & Omland (2003)OD8RA, STCT TCA GAG CCA GGG AAG CCA CCA CCA ATAllen & Omland (2003)ODintFA, SATG CCC GCT GTG TGT TTGIrestedt . (2006a)ODintF2A, SCAC TTA AGA CTA GCA GGC TTC TTC TGG AIrestedt . (2006a)ODintR2SCTT ACT CCC ATA TCA AAC ACA CAThis studyODintR3A, SCAA ACA CAC AGC GGG CAT CAG AIrestedt . (2006a)ODintR4A, SCAT ATT GAA GCC AAG TTC AGC CTAIrestedt . (2006a) Table 1primers used in this study. A, ampli“cation; et al.Phylogeny and ecological radiation of Tyrannidae© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters¥Zoologica Scripta, , 3, May 2008, pp 315Ð335 and calculatedthe date for the split between the Furnariida and Tyrannidato 62.18 Mya. This age was used as a “xed calibration pointin our PATHd8 analysis of the combined Bayesian tree.PATHd8 is a nonparametric method, which smoothesproperty of the method is that zero or near-zero branchcertainties in the phylogeny (or both). However, PATHd8be used. With few calibration points available, as in thepresent study, deviating branch lengths can have a strongFrom data gathered from general sources (e.g. Ridgely & Tudor1994; Ridgely & Green“eld 2001; Hilty 2003; . 2004), we de“ned four broad habitat categories as data for the terminal taxa (Fig. 2): (i) humid forest interior,canopy (although adjacent edge zones are occasionally visited);and montane grassland and scrub. We made no distinctionHowever, some genera (e.g. programsame sources as the habitat data. With some minor modi“ca-of the sallying strategy. This strategy is characterized bysurroundings for prey, which are caught by an approach”ight, either to adjacent surfaces or to the air. This is differentand perch gleaning, where search time are much shorter.We also With a few exceptions detailed below, we obtained sequencesfor all taxa. Total alignment length, proportion of variablepatterns are given in Table 2. G3PDH sequences varied inlength between 318 bp (Terenotriccus erythrurus) and 345 bpSirystes sibilator and Rupicola peruvianuswas 646 bp long. For Alectrurus risora and were unable to get a good reading for the last 10 bp of G3PDH.For myoglobin, we were unable to sequence the “rst 31 bp of, and the last 30 bp for Anairetes alpinus and Satrapa icterophrys. With theexception of these, sequence length varied between 691 bpFurnarius cristatus) and 753 bp (Corythopis delalandeiranging between 712 and 727 bp. For and , 1885 bp; , 1296 bp, , 993 bp) or deletions (Furnarius cristatus, 558 bp;, 547 bp; Cnipodectes subbrunneus, 621 bfrom these outliers, sequence lengths ranged between 648 bpThamnophilus caerulescens) and 702 bp (both Schiffornis speciesPhylogenetic resultspartitions (Fig. 1) exhibited good resolution and generally Phylogeny and ecological radiation of Tyrannidae et al.Zoologica Scripta, , 3, May 2008, pp 315Ð335¥© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Lettersgroup to clade F-3 + F-4 instead of as part of clade F-1. In the and were placed outside clade(posterior probability = 0.95 vs. posterior probability = 0.66Corythopis and beingsister groups (posterior probability = 0.96 vs. unresolved inOxyruncus and clade B as thesister to Tyrannidae + was supported in ODC (posteriorprobability = 0.99), but the combined tree had a posteriorprobability = 0.93 for a clade consisting of clade B, TityridaeOxyruncusDeep lineages in Tyrannida.Fig. 1. We recovered three well-supported main clades inTyrannida: Cotingidae (Cotingas), Pipridae (Manakins) large clade consisting of Tityridae, Oxyruncus andall members of Tyrannidae (clade A). Tityridae was shown to beSchiffornis andTityra and Terenotriccushave been included in Tyrannidae, formed a strongly supportedclade (clade B) outside of Tyrannidae. In the combined tree,clade B, Tityridae and Oxyruncus formed a monophyletic came out together with strongsupport and were placed as the sister group to a well-traditionally assigned to Tyrannidae, as was found by Ericson. (2006). The Tyrannidae, in turn, was divided into twoTachuris and a large clade corresponding to anof Fitzpatrick .s (2004) Elaeniini, Fluvicolinae andTyranninae. This is in accordance with the subdivisionson smaller taxon samples (Johansson . 2006). However, several genera in Tyrannidaepreviously been suggested, these genera are underlined in Fig. 1. and . Within this clade, the tody-tyrantsTodirostrum and Myiornis as its and Tolmomyiasof three pairs of relatively “ne-billed genera ( and Corythopiselaeniines (Traylor 1977; Lanyon 1988b; Fitzpatrick and Tachuris, grouped together and were strongly supported as sister taxa.Relationships among true tyrant ”ycatchers.encompasses the majority of genera in Tyranninae and(see above). An unexpected outcome was that Pyrrhomyias, Hirundinea and three species traditionally placed and species formed and Hirundinea group of and assemblage. It further includes was unavailable to W. E. Lanyon, and and due to their aberrantsyrinx morphology. The elaeniine clade and its three subclades and P. griseiceps and OrnithionM. calopterus andP. uropygialis and P. virescens in an unresolved Phylogeny and ecological radiation of Tyrannidae et al.Zoologica Scripta, , 3, May 2008, pp 315Ð335¥© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters Phylogeny and ecological radiation of Tyrannidae et al.Zoologica Scripta, , 3, May 2008, pp 315Ð335¥© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Lettersrelated to Tityridae and Oxyruncus. Tello & Bates (2007) andTerenotriccus to group outside Tyrannidae, although the in Pipridae has long was not aP. pileatus to be the sister taxon to Tyrannidae, and this iscorroborated in this study, with P. chloris “rmly and (and of intrinsic syringeal muscu-for Tyrannidae in Ericson and in a number of genera in clade A (TerenotriccusTodirostrum ZimmeriusHirundinea and MachetornisTityridae, although these were hypothesized to be of anmentioned Tyrannidae genera was interpreted by Lanyonmusculature evolved in the ancestor of Tyrannidae, as suggestedTodirostrum ZimmeriusHirundineaMachetornisTody-tyrants, ”atbills and allies.than previously understood. Compared to Lanyons (1988c).s (see and Tachuris and, in accordance with Corythopis and ) thatgenera (Traylor 1977; Lanyon 1988a; Fitzpatrick 2004). A and is in accordance with LanyonLanyons (1988a) also considered Corythopis assemblage. T or found a close relationship between Corythopis and and also found some support for a relationship between and genera being the sister group to the Tody-tyrants. Mostfacial pattern Within the pipromorphines, there was strong support for a and TolmomyiasTodirostrum andMyiornis). This is in accordance with the results of Tello &to be re-evaluated. However, these cannot be clari“ed withoutis less clear, however. Lanyon (1988c) placed in an unresolvedposition in the Flatbill and Tody-tyrant assemblage, where it and Tolmomyias by Tellosister taxon to the Tody-tyrants.. (2006), Tello & Bates (2007) andinternode. One of the most unexpected “ndings in our study, consistently comes out as the sister was traditionally placed in group in the assemblage of LanyonTerenotriccusHirundinea and some species. We found these to any of them. Tosequenced G3PDH for a second specimen of possesses the complete, ossi“ed bronchial A elements group in assemblage (Mobley & Prum 1995). However, Phylogeny and ecological radiation of Tyrannidae et al.Zoologica Scripta, , 3, May 2008, pp 315Ð335¥© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters assemblage and is reminiscent in general appearance and they were suggestedto be close relatives by W. E. Lanyon (1982, 1985). wasassociated with the myiarchines and tyrannines by W. E. is placedtyrannines. Our result supports the suggestion of W. E. RamphotrigonHowever, the results of Tello & Bates (2007) and Rheindt belongs with the myiarchinesfeatures of the syrinx, nesting behaviour, and in the case ofthese two genera must be explored further. Besides that, theMachetornis Machetornis, based on general morphology and behaviour,with earlier classi“cations (Traylor 1977; Fitzpatrick 2004), but assemblage ofclear-cut group, none of W. E. Lanyons groups is embeddedamong the ”uvicolines, although its exact position is unclear. group of his assemblage, a group that is demonstrated here to bewas not particularly strong (posterior probability of 0.93).the only ”uvicoline taxa con“ned to humid forest interior. species to has not been suggested previously. The three andM. inornatus and the sister and Tumbezia indicates that as currently delimited may notTumbezia in and proposed the genus for (including the purported relative by Lanyon (1986); he found a close relationship betweenArundinicola and Alectrurus although he placed and Gubernetes outside theThe monophyly of W. E. Lanyons group is is their sister group, together formingstudies (Lanyon & Lanyon 1986; and group had theiras a possible ancestral habitat. This is supported by the fact thathabitats. However, this suggestion must be substantiated byhigh Andean regions (e.g. Agriornis andMyiotheretes) have generally been assumed to be close relatives.sister group to clade F-4. In fact, the relationships depicted inthe Adams consensus tree in Birdsley (2002, “g. 6), obtainedsimilar to our results, including a basal position of Phylogeny and ecological radiation of Tyrannidae et al.Zoologica Scripta, , 3, May 2008, pp 315Ð335¥© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Lettersforaging strategy, upward striking, is remarkably stereotyped,Tolmomyias and Todirostrum that have colonized canopy andrelatives: (aerial sallier in canopy), Oxyruncus (prober/Tachuris (perch-gleaner in marshes) and (ground gleaner in desert scrub). Long branchesTachuris and some species in theTolmomyias and TodirostrumTityra and several species of in Tityridae.However, it apparently resulted in a large-scale diversi“cationHirundinea and which chie”yNorth America). However, a humid forest interior origin for optimization. To clarify this, better resolution is and is coded as such, this is alsofavoured as the ancestral habitat for both of them. However, is excluded, that is, if its character state is treatedas an uninformative autapomorphy, or assumed to haveinterior, mesic woodland and open habitat.Both the elaeniines and clade D are ecologically verysuccessful in terms of generic and species-level diversity.Interestingly, they show very consistent differences inprincipal foraging behaviour. Like the pipromorphines andallies, the elaeniines are remarkably homogenous in bothuse. With few exceptions, members of the elaeniines inhabitperch-gleaning and upward hover-gleaning, are taken together. Several species in clade F-1 inhabit shadyPy. rubinus and Sayornis in clade F-3 and and (and likely also and Tyrannus et al.Phylogeny and ecological radiation of Tyrannidae© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters¥Zoologica Scripta, , 3, May 2008, pp 315Ð335TyrannidaeZMUC 125 434Imbabura, EcuadorEU231685EU231783EU231886TyrannidaeZMUC 127 231Caazapa, ParaguayEU231686EU231784EU231887TyrannidaeZMUC 126 247Chuquisaca, BoliviaEU231659EU231757EU231859TyrannidaeNRM 976 752Presidente Hayes, ParaguayEU231707EU231805EU231908TyrannidaeNRM 976 724Concepci—n, ParaguayDQ435473DQ435525DQ435497TyrannidaeZMUC 125 976Napo, EcuadorEU231666EU231764EU231866TyrannidaeZMUC 84-04-18Morona-Santiago, EcuadorEU231660EU231758EU231860TyrannidaeZMUC 125 448Apur’mac, PeruEU231741EU231839EU231942TyrannidaeZMUC 127 227Cordilera, ParaguayEU231679EU231777EU231880TyrannidaeZMUC 125 459Cotopaxi, EcuadorEU231681EU231779EU231882TyrannidaeZMUC 89-06-08Hu‡nuco, PeruEU231661EU231759EU231861TyrannidaeNRM 965 730Alto Paraguay, ParaguayEU231720EU231818EU231921TyrannidaeZMUC 125 477Loja, EcuadorEU231693EU231791EU231894TyrannidaeZMUC 127 218Alto Paran‡, ParaguayEU231700EU231798EU231901TyrannidaeZMUC 125 895Mato Grosso, BrazilEU231701EU231799EU231902TyrannidaeZMUC 127 832Morona-Santiago, EcuadorEU231664EU231762EU231864TyrannidaeZMUC 125 482Sucumbios, EcuadorEU231704EU231802EU231905TyrannidaeNRM 996 681Alto Paraguay, ParaguayEU231734EU231832EU231935TyrannidaeZMUC 125 483Zamora-Chinchipe, EcuadorEU231728EU231826EU231929TyrannidaeNRM 947 171Alto Paraguay, ParaguayEU231682EU231780EU231883TyrannidaeNRM 956 578Itapua, ParaguayEU231702EU231800EU231903TyrannidaeNRM 966 804Boquer—n, ParaguayDQ435476DQ435528DQ435503TyrannidaeNRM 996 668Alto Paraguay, ParaguayEU231723EU231821EU231924TyrannidaeNRM 976 762Presidente Hayes, ParaguayEU231671EU231769EU231872TyrannidaeZMUC 135 914Jun’n, PeruEU231657EU231755EU231857TyrannidaeZMUC 126 692Napo, EcuadorEU231655EU231753EU231855TyrannidaeNRM 947 036Alto Paraguay, ParaguayAY336575AY338740DQ435506TyrannidaeZMUC 125 587Bahia, BrazilEU231665EU231763EU231865TyrannidaeZMUC 125 508Lambayeque/Piura, PeruEU231718EU231816EU231919TyrannidaeNRM 976 722Concepci—n, ParaguayAY336579AY165826DQ435507TyrannidaeNRM 947 038Alto Paraguay, ParaguayEU231740EU231838EU231941TyrannidaeZMUC 125 511Zamora-Chinchipe, EcuadorEU231683EU231781EU231884TityridaeZMUC 125 762Napo, EcuadorDQ435467DQ435519DQ435485TityridaeZMUC 127 782Morona-Santiago, EcuadorEU231649EU231747EU231848TityridaeZMUC 125 879Mato Grosso, BrazilDQ470527DQ470554EU231849TityridaeNRM 976 715Concepci—n, ParaguayEU231652EU231750EU231852TityridaeNRM 967 032Concepci—n, ParaguayAY336573AY338747DQ435493TityridaeNRM 947 250Amambay, ParaguayEU231651EU231749EU231851TityridaeUSNM B05097Essequibo, GuyanaEU231648EU231746EU231847TityridaeNRM 937 315Caazapa, ParaguayAY336574AY338741DQ435501TityridaeNRM 956 584Itapua, ParaguayAY336580AY338742DQ435505TityridaeNRM 967 083Amambay, ParaguayEU231650EU231748EU231850OxyruncidaeNRM 967 078Amambay, ParaguayAY336572AY338745DQ435492PipridaeNRM 956 620Caazapa, ParaguayDQ435462DQ435516DQ435477PipridaeZMUC 126 073Napo, EcuadorEU231647EU231745EU231846PipridaeZMUC 125 609Bahia, BrazilEU231646EU231744EU231845PipridaeNRM 947 271Amambay, ParaguayAY336583AY065787DQ435495PipridaeZMUC 126 866Pastaza, EcuadorEU231645EU231743EU231844CotingidaeZMUC 127 031Guayas, EcuadorDQ470516DQ470543EU231841CotingidaeNRM 967 030Concepci—n, ParaguayAY336582AY065786DQ435498CotingidaeZMUC 126 003Zamora-Chinchipe, EcuadorDQ435474DQ435526DQ435500CotingidaeZMUC 128 821Southeast BrazilDQ470540DQ470567EU231843CotingidaeZMUC 125 021Lima, PeruDQ470542DQ470569EU231842Incerta sedisZMUC 127 972Morona-Santiago, EcuadorEU231656EU231754EU231856Incerta sedisZMUC 128 817Southeast BrazilDQ435472DQ435524DQ435496FurnariidaeNRM 966 772Boquer—n, ParaguayAY590066AY064255DQ435482ThamnophilidaeNRM 967 007Concepci—n, ParaguayAY336587AY065783DQ435504TaxonFamilySample IDProvenanceG3PMyoglobinODC Appendix 1Continued.