JOURNAL OF AVIAN BIOLOGY 37: 260/272, 2006

Evolution of the - assemblage

(Aves: Furnariidae) / major shifts in nest architecture and adaptive radiation

Martin Irestedt, Jon Fjeldsa˚ and Per G. P. Ericson

Irestedt, M., Fjeldsa˚, J. and Ericson, P. G. P. 2006. Evolution of the ovenbird- woodcreeper assemblage (Aves: Furnariidae) / major shifts in nest architecture and adaptive radiation. / J. Avian Biol. 37: 260/272

The Neotropical ovenbirds (Furnariidae) form an extraordinary morphologically and ecologically diverse radiation, which includes many examples of that are superficially similar to other passerine as a resulting from their adaptations to similar lifestyles. The ovenbirds further exhibits a truly remarkable variation in nest types, arguably approaching that found in the entire passerine clade. Herein we present a -level phylogeny of ovenbirds based on both mitochondrial and nuclear DNA including a more complete taxon sampling than in previous molecular studies of the group. The phylogenetic results are in good agreement with earlier molecular studies of ovenbirds, and supports the suggestion that and form the sister clade to both core-ovenbirds and . Within the core-ovenbirds several relationships that are incongruent with traditional classifications are suggested. Among other things, the philydorine ovenbirds are found to be non-monophyletic. The mapping of principal nesting strategies onto the molecular phylogeny suggests cavity nesting to be plesiomorphic within the ovenbird/woodcreeper radiation. It is also suggested that the shift from cavity nesting to building vegetative nests is likely to have happened at least three times during the evolution of the group. We suggest that the shifts in nest architecture within the furnariine and synallaxine ovenbirds have served as an ecological release that has facilitated diversification into new habitats and new morphological specializations.

M. Irestedt (correspondence) and P. G. P. Ericson, Department of Vertebrate Zoology and Molecular Systematics Laboratory, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden. E-mail: [email protected]. J. Fjeldsa˚, Vertebrate Department, Zoological Museum, University of Copenhagen, Universitetsparken 15, DK/2100 Copenhagen Ø, Denmark.

The Neotropical ovenbirds (Furnariidae) exhibit a synallaxine genera resembling various Old World unique morphological and ecological variation among grass warblers (‘‘Sylviidae’’) or creepers (Certhiidae). passerine birds (Leisler 1977, Vaurie 1980, Remsen Also in their placement and structure of the nest the 2003). The group includes many examples of species ovenbirds exhibit an extraordinary diversity. In fact, that exhibit remarkable superficial morphological the variation in nest types in this family has been similarities with other passerine birds that only are suggested to approach that found in the entire passerine distantly related to ovenbirds, for instance the cinclodes clade (Sick 1993, Collias 1997, Zyskowski and Prum species (Cinclodes) resembling muscicapine thrushes 1999, Remsen 2003). Nevertheless, breeding in ‘‘closed’’ (Turdidae) or dippers (Cinclidae), miners (Geositta) nest chambers, whether placed inside a cavity or in resembling (Alaudidae), earthcreepers (Upucerthia) the vegetation, seems to unite all ovenbirds (and resembling thrashers (Toxostoma, Mimidae) and various woodcreepers).

# JOURNAL OF AVIAN BIOLOGY

260 JOURNAL OF AVIAN BIOLOGY 37:3 (2006) Clades of passerine birds differ greatly in their degree myoglobin intron 2 and G3PDH intron 11, and the of morphological divergence (Ricklefs 2003). Remark- mitochondrial cytochrome b gene. Based on these able radiations on small and species-poor landmasses, phylogenetic results we will reassess the evolution of such as islands, are often interpreted as a consequence of nest-building strategies of ovenbirds. competition for a limited range of food types (e.g., Grant 1986). The variation in the ovenbird clade may represent another model, given their vast distribution in South and Materials and methods Central America and the great diversity of other kinds of birds. ‘‘Key innovations’’ may represent another possible Taxon sampling, amplification and sequencing explanation for non-random variation in diversity among clades. The relative success of passerine birds The ingroup in this study includes 48 ovenbirds (repre- has for example been postulated to be promoted by the senting 40 out of 55 genera recognized by Remsen 2003) and 9 woodcreepers. The ovenbirds were chosen to complexity of the passerine foot (Raikow and Bledsoe represent all major subgroups previously suggested 2000) or by the ability to build nests from a wide variety (Vauri 1971, 1980, Feduccia 1973, Raikow 1994, Ridgely of materials (Olson 2001). The ability of ovenbirds to and Tudor 1994, Zimmer and Isler 2003). In addition, construct nests of a tremendous architectural diversity we included several species that have proven difficult to could thus be a possible explanation for their successful place in either of these subgroups. A selection of colonization of a wide range of habitats, along with a woodcreepers was also included, as recent molecular special modification of the kinetic properties of the bill, data have shown this group to be nested within oven- which allowed them to extract food that was otherwise birds (Irestedt et al. 2002, Chesser 2004, Fjeldsa˚ et al. hidden in complex vegetation structures (Fjeldsa˚ et al. 2005). As outgroups we used two representatives of the 2005). family Rhinocryptidae (Pteroptochos tarnii and Scyta- Monophyly of the ovenbirds and woodcreepers is lopus spillmanni) and one of the family Formicariidae inferred from their shared, unique syrinx morphology (Chamaeza meruloides), which form the sister clade to (Ames 1971), and has also been supported by molecular the Furnariidae (Irestedt et al. 2002, Chesser et al. 2004). data (Sibley and Ahlquist 1990, Irestedt et al. 2002, Sample identifications and GenBank accession numbers Chesser et al. 2004, Fjeldsa˚ et al. 2005). Mostly based on are given in Table 1. overall similarity ovenbirds have traditionally been The complete myoglobin intron 2, the complete divided into three major groups, Furnariinae, Synallax- glyceraldehydes-3-phosphodehydrogenase (G3PDH) in- inae and Philydorinae (i.e. Hellmayr 1925, Vaurie 1971, tron 11, and 999 bp from the cytochrome b gene have 1980; see Sibley and Ahlquist 1990 for a historical been sequenced (see Fjeldsa˚ et al. 2003, and Irestedt et review), with the woodcreepers as their closest relatives. al. 2002 for sequencing procedures). For each gene and However, Feduccia (1973) noted cranial similarities taxon, multiple sequence fragments were obtained by between certain woodcreepers and the philydorine oven- sequencing with different primers. These sequences were birds, and suggested that the woodcreepers had evolved assembled to complete sequences with SeqMan IITM from a philydorine ovenbird. Several recent DNA (DNASTAR Inc.). Positions where the nucleotide could analyses strongly support Feduccia?s hypothesis that not be determined with certainty were coded with the woodcreepers are nested within the ovenbirds, but reject appropriate IUPAC code. Due to the low number of a close affinity to the philydorines. Instead, it is insertions in the introns the combined sequences could suggested that the leaftossers (Sclerurus) and miners easily be aligned by eye. All gaps have been treated as (Geositta) are to both woodcreepers and core missing data in the analyses. No insertions, deletions, ovenbirds, and that these latter two groups are recipro- stop or nonsense codons were observed in any of the cally monophyletic (Irestedt et al. 2002, Chesser 2004, cytochrome b sequences. Fjeldsa˚ et al. 2005). The molecular studies also suggest Certhiaxis cinnamomea produced a partly unreadable other relationships at odds with traditional classifica- sequence for the G3PDH intron 11, and the PCR tions of ovenbirds: the placement of Pseudoseisura product from this taxon was cloned. The cloning, among the synallaxines and of Lochmias among the amplification and sequencing were done with the furnariines (as opposed to their traditional placement TOPO TA Cloning† Kit (Invitrogen Life Technologies), among philydorine ovenbirds), and in a basal using the manufacturer’s primers and protocol. In one of position in the woodcreeper radiation (instead of among the two clones studied, an autapomorphic insertion was philydorines) (Fjeldsa˚ et al. 2005). These studies ob- found at the positions where the sequences from the viously raise doubts about the monophyly of the uncloned PCR-products became unreadable. Thus, this ‘‘philydorine’’ ovenbirds. insertion likely explains the reading problems in the Herein, we present a molecular phylogenetic hypoth- latter. In the phylogenetic analysis of the G3PDH intron esis of ovenbird relationships based on an expanded 11 both clones were included, but as these two clones taxonomic sample and data from two nuclear introns, grouped together, the G3PDH partition in Certhiaxis

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 261 262

Table 1. Samples used in the study. Family and subfamily names follow the classification of Remsen (2003). Abbreviations: AHMN/American Museum of Natural History, New York; ANSP/Academy of Natural Sciences of Philadelphia; NRM/Swedish Museum of Natural History; ZMUC/Zoological Museum of the University of Copenhagen. References: (1) Irestedt et al. (2001), (2) Irestedt et al. (2004b), (3) Ericson et al. (2002), (4) Fjeldsa˚ et al. (2005), and Olson et al. (2005).

Species Subfamily/family Sample No. Cytochrome b Myoglobin G3PDH

Geositta rufipennis Furnariidae: Furnariinae ZMUC S290 AY590042 (ref. 4) AY590052 (ref. 4) AY590062 (ref. 4) Geositta tenuirostris Furnariidae: Furnariinae ZMUC S292 AY590043 (ref. 4) AY590053 (ref. 4) AY590063 (ref. 4) Upucerthia jelskii Furnariidae: Furnariinae ZMUC S439 AY065700 (ref. 1) AY065756 (ref. 1) AY590064 (ref. 4) Cinclodes fuscus Furnariidae: Furnariinae ZMUC S220 AY590044 (ref. 4) AY590054 (ref. 4) AY590065 (ref. 4) Furnarius leucopus Furnariidae: Furnariinae ZMUC 125590 AY996351 (ref. 5) AY996345 (ref. 5) AY996357 (ref. 5) Furnarius cristatus Furnariidae: Furnariinae NRM 966772 AY064279 (ref. 3) AY064255 (ref. 3) AY590066 (ref. 4) Limnornis curvirostris Furnariidae: Synallaxinae USNM B2735 AY996353 (ref. 5) AY996346 (ref. 5) AY996359 (ref. 5) Limnoctites rectirostris Furnariidae: Synallaxinae USNM B14895 AY996352 (ref. 5) AY996347 (ref. 5) AY996358 (ref. 5) Phleocryptes melanops Furnariidae: Synallaxinae USNM B2734 AY996354 (ref. 5) AY996348 (ref. 5) AY996360 (ref. 5) Aphrastura spinicauda Furnariidae: Synallaxinae ZMUC 134531 AY998188 AY998225 AY998206 Leptasthenura pileata Furnariidae: Synallaxinae ZMUC S338 AY590045 (ref. 4) AY590055 (ref. 4) AY590067 (ref. 4) Schizoeaca harterti Furnariidae: Synallaxinae ZMUC S2398 AY998189 AY998226 AY998207 Oreophylax moreirae Furnariidae: Synallaxinae ZMUC S128816 AY998190 AY998227 AY998208 Schoeniophylax phryganophilus Furnariidae: Synallaxinae NRM 947184 AY998191 AY998228 AY998209 ruficapilla Furnariidae: Synallaxinae NRM 956643 AY065707 (ref. 1) AY065763 (ref. 1) AY590068 (ref. 4) Synallaxis scutata Furnariidae: Synallaxinae ZMUC 125635 AY998192 AY998229 AY998210 Hellmayrea gularis Furnariidae: Synallaxinae ZMUC 124846 AY998193 AY998230 AY998211 sulphurifera Furnariidae: Synallaxinae USNM B17199 AY996350 (ref. 5) AY996344 (ref. 5) AY996356 (ref. 5) Cranioleuca pyrrhophia Furnariidae: Synallaxinae NRM 966821 AY065708 (ref. 1) AY065764 (ref. 1) AY590069 (ref. 4) Cranioleuca albicapilla Furnariidae: Synallaxinae ZMUC 124797 AY996349 (ref. 5) AY996343 (ref. 5) AY996355 (ref. 5) Certhiaxis cinnamomeus Furnariidae: Synallaxinae NRM 937358 AY998194 AY998231 AY998212, AY998213 Asthenes cactorum Furnariidae: Synallaxinae ZMUC S150 AY065705 (ref. 1) AY065761 (ref. 1) AY590070 (ref. 4) Asthenes urubambensis Furnariidae: Synallaxinae ZMUC S172 AY998195 AY998232 AY998214 Phacellodomus ruber Furnariidae: Synallaxinae NRM 947206 AY590046 (ref. 4) AY590056 (ref. 4) AY590071 (ref. 4) Anumbius annumbi Furnariidae: Synallaxinae NRM 966903 AY065709 (ref. 1) AY065765 (ref. 1) AY590072 (ref. 4) Coryphistera alaudina Furnariidae: Synallaxinae NRM 966910 AY065710 (ref. 1) AY065766 (ref. 1) AY590073 (ref. 4) Metopothrix aurantiaca Furnariidae: Synallaxinae NRM 569302 AY998224 Xenerpestes singularis Furnariidae: Synallaxinae ANSP 4370 AY998205 Premnornis guttuligera Furnariidae: Philydorinae ZMUC 128014 AY998196 AY998233 AY998215 Premnoplex brunnescens Furnariidae: Philydorinae ZMUC 124927 AY998197 AY998234 AY998216 Margarornis squamiger Furnariidae: Philydorinae ZMUC S1112 AY065703 (ref. 1) AY065759 (ref. 1) AY590074 (ref. 4) Pseudoseisura lophotes Furnariidae: Philydorinae NRM 976799 AY998199 AY998236 AY998218 ORA FAINBOOY3: (2006) 37:3 BIOLOGY AVIAN OF JOURNAL Pseudocolaptes boissonneautii Furnariidae: Philydorinae ZMUC 124935 AY998198 AY998235 AY998217 Berlepschia rikeri Furnariidae: Philydorinae ZMUC S1214 AY590047 (ref. 4) AY590057 (ref. 4) AY590075 (ref. 4) Anabacerthia striaticollis Furnariidae: Philydorinae ZMUC 124673 AY998200 AY998237 AY998219 rufosuperciliata Furnariidae: Philydorinae ZMUC124972 AY998201 AY998238 AY998220 Philydor atricapillus Furnariidae: Philydorinae NRM 937334 AY065702 (ref. 1) AY065758 (ref. 1) AY590076 (ref. 4) Thripadectes flammulatus Furnariidae: Philydorinae ZMUC S428 AY065701 (ref. 1) AY065757 (ref. 1) AY590077 (ref. 4) leucophthalmus Furnariidae: Philydorinae NRM 937251 AY590048 (ref. 4) AY590058 (ref. 4) AY590078 (ref. 4) Hylocryptus erythrocephalus Furnariidae: Philydorinae ZMUC 124862 AY998202 AY998239 AY998221 Sclerurus mexicanus Furnariidae: Philydorinae ZMUC S1443 AY590049 (ref. 4) AY590059 (ref. 4) AY590079 (ref. 4) Sclerurus scansor Furnariidae: Philydorinae NRM 937258 AY065715 (ref. 1) AY065772 (ref. 1) AY590080 (ref. 4) Lochmias nematura Furnariidae: Philydorinae ZMUC S2577 AY065699 (ref. 1) AY065755 (ref. 1) AY590081 (ref. 4) Heliobletus contaminatus Furnariidae: Philydorinae ZMUC 127191 AY998203 AY998240 AY998222 Xenops minutus Furnariidae: Philydorinae ZMUC S451 AY590050 (ref. 4) AY590060 (ref. 4) AY590082 (ref. 4) Xenops rutilans Furnariidae: Philydorinae ZMUC S452 AY590051 (ref. 4) AY590061 (ref. 4) AY590083 (ref. 4) Megaxenops parnaguae Furnariidae: Philydorinae ZMUC 125605 AY998204 AY998241 AY998223 Pygarrhichas albogularis Furnariidae: Philydorinae AMNH PRS1128 AY065704 (ref. 1) AY065760 (ref. 1) AY590084 (ref. 4) cinnamomea in the combined analysis is represented by the consensus sequence from both clones.

Phylogenetic inference and model selection Bayesian inference and Markov chain Monte Carlo (MCMC) were used for estimating phylogenetic hypoth- esis from our DNA data (see recent reviews by Huel- senbeck et al. 2001, Holder and Lewis 2003). The models for nucleotide substitutions used in the analyses were selected for each gene individually by using Akaike Information Criterion (AIC, Akaike, 1973) and the program MrModeltest (Nylander 2002) in conjunction

Myoglobin G3PDH with PAUP* (Swofford 1998). The posterior probabilities of trees and parameters in the substitution models were approximated with MCMC and Metropolis coupling using the program MrBayes (Ronquist and Huelsenbeck 2003). Analyses were per- formed for both the individual gene partitions and the

b combined data set. In the analysis of the combined data set the models selected for the individual gene partition were used, but the topology was constrained to be the same. One cold and three incrementally heated chains were run for 2.5 million generations, with a random starting tree. Trees were sampled every 100th genera- tions, and the trees sampled during the burn-in phase (i.e., before the chain had reached its apparent target distribution) were discarded. Two runs, starting from different, randomly chosen trees, were made to ensure that the individual runs had converged on the same target distribution (Huelsenbeck et al. 2002). After checking for convergence, final inference was made from the concatenated output from the two runs.

Results Variation in the molecular data set The sequences obtained ranged from 667 bp (Helioble- tus) to 716bp (Chamaeza) in the myoglobin intron 2, and from 287 bp (Chamaeza) to 410 bp (Margarornis)in the G3PDH intron 11. Most indels observed in the two introns were autapomorphic and mainly found in DendrocolaptidaeDendrocolaptidaeDendrocolaptidaeDendrocolaptidaeDendrocolaptidaeDendrocolaptidaeDendrocolaptidae NRMDendrocolaptidae 947183 ZMUCDendrocolaptidae S1249 NRMFormicariidae 976662 NRMRhinocryptidae 966930 ZMUCRhinocryptidae S1521 ZMUC S1831 NRM 967031 NRM AY442987 966847 (ref. 2) ZMUC AY442989 (ref. S1616 2) AY065713 (ref. 2) AY065711 (ref. ZMUC 1) S2053 AMNH AY442992 (ref. RTC467 2) ZMUC AY442995 (ref. S540 2) AY442961 (ref. AY065714 2) (ref. AY442963 1) (ref. 2) AY065712 (ref. 1) AY065770 AY442997 (ref. (ref. 2) 2) AY065768 (ref. 1)particularly AY442966 AY065717 (ref. (ref. 2) 1) AY590085 AY442969 AY065718 (ref. (ref. (ref. 4) 2) 1) AY590086 (ref. AY065771 4) (ref. 1) AY590087 AY065716 (ref. (ref. AY065769 4) (ref. 1) 1) AY590088 AY442971 (ref. (ref. 4) 2) AY590089 (ref. 4) AY590091 AY065774 (ref. (ref.variable 1) 4) AY065776 (ref. AY590092 (ref. 1) 4) AY590093 (ref. 4) AY065773 AY590094 (ref. (ref. 1) 4) and AY590096 (ref. 4) AY590095 (ref. 4) repetitive AY590097 (ref. 4) regions. However, some synapomorphic indels were observed when map- ping the data onto the tree topologies obtained from the Bayesian analyses of the combined data set. In the myoglobin intron 2, all ovenbirds and woodcreepers lack

) 28 bp present in the outgroup (Scytalopus also lack 12 of these bp but shares the remaining 16 bp with the other outgroup taxon); the woodcreeper representatives share

Continued a deletion of 12 bp; Pteroptochos tarnii and Scytalopus spillmanni share a deletion of 13 bp and an insertion of 10 bp; Sclerurus mexicanus and Sclerurus scansor share Deconychura longicauda tyrannina Drymornis bridgesii Glyphorynchus spirurus Nasica longirostris Sittasomus griseicapillus major erythropygius Chamaeza meruloides Pteroptochos tarnii Scytalopus spillmanni trochilirostris Table 1 ( Species Subfamily/family Sample No.a deletion Cytochrome of 4 bp; and Philydor atricapillus and

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 263 Heliobletus contaminatus share a deletion of 14 bp. In These models were used in the Bayesian analyses of the relatively more indel-rich G3PDH intron 11 indels the individual genes as well as in the combined analysis. with different lengths sometimes overlap. However, if After discarding the burn-in phase the inference for these are treated as independent events the following the cytochrome b gene was based on a total of 48,400 synapomorphic indels are found; Geositta rufipennis and samples from the posterior, while the inference tenuirostris share a deletion of 23 bp; Deconychura, for myoglobin and G3PDH introns were based on Dendrocincla and Sittasomus share two deletions of 34 47,800 samples and 47,500 samples for the combined and 1 bp, respectively; Furnarius cristatus and leucopus data set. For the phylogenetic inference, the mode of share a deletion of 19 bp; Xenops minutus and rutilans the posterior distribution of topologies was presented share a deletion of 1 bp; Pteroptochos tarnii and as a majority-rule consensus tree from each analysis Scytalopus spillmanni share a deletion of 3 bp; (Figs. 1 and 2). all ovenbirds and woodcreepers share an extra basepair The trees obtained from the Bayesian analyses of lacking in the outgroup and in the representatives the individual gene partitions (Fig. 1) shows a similar Geositta Sclerurus Anabacerthia of the genera and ; , degree of resolution (although the tree obtained from Automolus, Heliobletus, Hylocryptus, Megaxenops, the cytochrome b partition is slightly more resolved). Philydor and Syndactyla share an insertion of 1 bp The gene trees are also overall topologically similar (Thripadectes has an autapomorphic deletion in and the non-congruent relationships are mostly at short that region); and Heliobletus and Philydor share an nodes with rather modest posterior probabilities. Phylo- insertion of 9 bp. genetic relationships congruently supported by all A few indels were also found to be incongruent with the phylogenetic tree obtained from the analysis three genes includes a strong support for a sister of the combined data set. These were generally found relationship between the genera Geositta and Sclerurus; in the most variable regions and some of the single a clade consisting of the Cranioleuca representatives basepair insertions actually consist of different bases. and Limnoctites rectirostris; a core foliage-gleaners However, one of these indels in myoglobin consists of clade (Anabacerthia, Syndactyla, Megaxenops, Helioble- a 4 bp deletion shared between Certhiaxis cinnamomea tus, Philydor, Automolus, Hylocryptus, and Thripa- and Schoeniophylax phryganophila. The remaining, dectes); and a clade consisting of traditional phylogenetically incongruent indels were found to in Furnariinae ovenbirds (Furnarius, Cinclodes and Upu- the G3PDH intron 11 and includes a 1 bp insertion in ) plus the genera Lochmias, Phleocryptes and Cinclodes, Deconychura and Premnoplex; a 1 bp inser- Limnornis. tion in Asthenes cactorum and Furnarius cristatus;a1bp A few conflicting topologies between the individual deletion in Automolus and Thripadectes; a 1 bp deletion gene trees are supported by rather solid posterior in Pteroptochos and Glyphorynchus; a 10 bp deletion probabilities, but there is no indication that one gene in Drymornis and Xiphorhynchus; and a 3 bp insertion in tree should be more different than the others. Examples Glyphorynchus, Campylorhamphus, Drymornis, Nasica, of strong topological conflicts include the relative Xiphocolaptes and Xiphorhynchus. position of Limnoctites rectirostris. While the G3PDH The observed, pairwise distances (p-distances) range tree gives a strong support placing Limnoctites recitros- between 0.3% (Limnoctites rectirostris and Cranioleuca tris with Cranioleuca albicapilla, both the myoglobin sulphurifera, Synallaxis scutata and Synallaxis rufica- and cytochrome b trees placed it with C. sulphurifera. pilla, Cranioleuca pyrrhophia and Cranioleuca albica- Another example is in the relative positions of Certhiaxis pilla) and 8.8% (Scytalopus spillmanni and Synallaxis cinnamomea and Synallaxis scutata, where the topology scutata) in myoglobin, 0.0% (Xenops minutus and of the G3PDH tree differs from those in the myoglobin rutilans) and 13.2% (Berlepschia rikeri and Scytalopus and cytochrome b trees. There are also examples where spillmanni, Berlepschia rikeri and Chamaeza meruloides) the cytochrome b tree or the myoglobin tree supports in G3PDH, and between 2.4% (Lochmias nematura and relationships different from what suggested by the Upucerthia jelskii) and 20.3% (Chamaeza meruloides and G3PDH tree. For example, the cytochrome b tree Synallaxis ruficapilla, Pteroptochos tarnii and Nasica supports a basal position of Xenops minutus and Xenops longirostris) in cytochrome b. rutilans relative to all other ovenbirds except the genera Geositta and Sclerurus, while both the G3PDH and myoglobin trees suggest that Xenops instead is basal within the woodcreeper clade. The analysis of the Model selection and phylogenetic relationships combined data set results in a tree (Fig. 2) that is better The priori selection of substitution models supported resolved than the individual gene trees, although topo- that the GTR/I/G model had the best fit for the logically overall similar to them. Overall the combined cytochrome b, and the myoglobin partitions, while the tree tends to support relationships that are supported by

GTR/G model was selected for the G3PDH intron 11. a majority of the gene partitions.

264 JOURNAL OF AVIAN BIOLOGY 37:3 (2006) Fig. 1. The 50% majority rule Cranioleuca sulphurifera A) 0.99 Limnoctites rectirostris consensus trees obtained from the 1.00 Cranioleuca albicapilla Bayesian analyses of the individual 1.00 Cranioleuca pyrrhophia genes. A) the tree obtained from the 0.72 Metopothrix aurantiaca analyses of G3PDH (glyceraldehydes- Synallaxis ruficapilla 3-phosphodehydrogenase) intron 11 0.99 Schoeniophylax phryganophilus 1.00 Certhiaxis cinnamomeus cl 1 data set, B) the tree obtained from the 1.00 Certhiaxis cinnamomeus cl 2 analyses of the myoglobin intron 2 data Asthenes cactorum 0.52 set, and C) tree obtained from the 0.63 Pseudoseisura lophotes Bayesian analyses of the cytochrome b Synallaxis scutata 0.50 Oreophylax moreirae data set. Posterior probability values 1.00 0.90 Schizoeaca harterti are indicated to the right of the nodes. Asthenes urubambensis Anumbius annumbi 0.79 0.96 Coryphistera alaudina Hellmayrea gularis 0.95 Phacellodomus ruber Leptasthenura pileata 0.69 Aphrastura spinicauda Premnoplex brunnescens Limnornis curvirostris 0.70 Phleocryptes melanops 0.77 0.78 Lochmias nematura 0.96 Cinclodes fuscus 1.00 0.96 Upucerthia jelskii Furnarius cristatus 1.00 0.98 Furnarius leucopus Premnornis guttuligera 0.97 Pseudocolaptes boissonneautii Margarornis squamiger Pygarrhichas albogularis 1.00 Anabacerthia striaticollis 1.00 Syndactyla rufosuperciliata 0.98 Megaxenops parnaguae Heliobletus contaminatus 1.00 Philydor atricapillus 1.00 Automolus leucophthalmus 0.99 Hylocryptus erythrocephalus Thripadectes flammulatus Berlepschia rikeri Xiphorhynchus erythropygius Campylorhamphus trochilirostris 1.00 0.86 0.99 Drymornis bridgesii 0.78 0.66 Nasica longirostris 1.00 Xiphocolaptes major 0.59 Glyphorynchus spirurus Deconychura longicauda 0.74 Sittasomus griseicapillus 0.72 0.79 Dendrocincla tyrannina 1.00 Xenops minutus Xenops rutilans Sclerurus mexicanus 1.00 Sclerurus scansor 0.98 Geositta tenuirostris 0.78 Geositta rufipennis Pteroptochos tarnii 1.00 Scytalopus spillmanni Chamaeza meruloides

Discussion estimates that are at odd with both nuclear data and the relationships that could be expected based on biogeo- Phylogenetic resolution graphy or morphological data (Degnan 1993, Alstro¨m ¨ The overall topological similarity between the individual and Odeen 2002). Furthermore, even though the ob- served topological conflicts could be genuine, i.e., that gene trees (Fig. 1) support that the tree obtained in the the different genomic partitions used herein have differ- analysis of the combined data set (Fig. 2) is an overall ent phylogenies (reviewed in e.g., Moore 1995, Maddison good estimate of the generic relationships among oven- 1997, Mindell 1997), the conflicts might also be due to birds. Nevertheless, the topological disagreements that inaccuracies of the substitution models, or in the do exist between the gene trees might cause some methods used to infer the trees. Without further evidence concern about the accuracy of certain parts of the from, for example, DNA sequence data obtained from combined tree. other linkage groups, morphological or behavioral It has been postulated that trees based on the characters, it seems virtually impossible to discriminate mitochondrial genome has a better chance to correctly between individual gene trees. As the combined tree is estimate avian phylogenies than single nuclear genes based on all gene partitions it tends to exhibit relation- (Moore 1995, Moore and DeFilippis 1997), but exam- ships supported by a majority of these. Consequently, we ples exist where mitochondrial trees yield phylogenetic believe that the combined tree overall is a better

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 265 Cranioleuca sulphurifera Fig. 1 (Continued ) B) 1.00 1.00 Limnoctites rectirostris Cranioleuca albicapilla Cranioleuca pyrrhophia Synallaxis ruficapilla 0.73 1.00 0.59 0.94 Synallaxis scutata Schoeniophylax phryganophilus Certhiaxis cinnamomeus Pseudoseisura lophotes 0.56 Oreophylax moreirae 1.00 0.78 Schizoeaca harterti Asthenes urubambensis Anumbius annumbi Premnornis guttuligera Hellmayrea gularis Asthenes cactorum 0.76 Phacellodomus ruber Leptasthenura pileata 0.86 Coryphistera alaudina 0.68 Aphrastura spinicauda 1.00 Limnornis curvirostris Phleocryptes melanops Lochmias nematura 1.00 Cinclodes fuscus 0.99 Upucerthia jelskii Furnarius cristatus 1.00 Furnarius leucopus Pseudocolaptes boissonneautii 1.00 Margarornis squamiger 0.96 0.78 Premnoplex brunnescens Pygarrhichas albogularis Anabacerthia striaticollis 0.95 Syndactyla rufosuperciliata 0.89 Megaxenops parnaguae Heliobletus contaminatus 1.00 1.00 Philydor atricapillus Automolus leucophthalmus 0.90 1.00 Hylocryptus erythrocephalus Thripadectes flammulatus Berlepschia rikeri Deconychura longicauda 0.93 1.00 Sittasomus griseicapillus Dendrocincla tyrannina Nasica longirostris 1.00 0.99 Xiphocolaptes major 1.00 Glyphorynchus spirurus 1.00 Campylorhamphus trochilirostris 1.00 Drymornis bridgesii 0.83 0.73 Xiphorhynchus erythropygius Xenops minutus 1.00 Xenops rutilans Sclerurus mexicanus 0.99 Sclerurus scansor 0.90 Geositta tenuirostris 1.00 Geositta rufipennis Pteroptochos tarnii 1.00 Scytalopus spillmanni Chamaeza meruloides phylogenetic estimate than any of the individual gene strong indication that our combined phylogeny is a good trees. In fact, we found relationships based on the estimate of the generic relationships of ovenbirds. individual genes to be in conflict with those of the The finding that Geositta and Sclerurus are basal combined tree mainly where nodes are short and poster- positioned to both the woodcreepers and remaining ior probabilities modest (B/0.95). ovenbirds are, for example, also conclusively supported The combined phylogeny is in many respects incon- by the b-fibrinogen intron 7 (Chesser 2004). In addition, gruent with the traditional division of ovenbirds into recently revealed morphological characters also support three major groups, Furnariinae, Synallaxinae and several of these novel molecular hypotheses. Fjeldsa˚ Philydorinae (i.e. Hellmayr 1925, Vaurie 1971, 1980). et al. (2005) demonstrate that Geositta and Sclerurus Many recent molecular studies of other passerine share similar skull morphologies with the so called groups (i.e. Madagascan songbirds, see Cibois et al. ‘‘transitory woodcreepers’’ (Feduccia 1973), and differ 2001; , see Irestedt et al. 2004a) have shown that from the skull morphologies found in other ovenbirds. traditional classifications, based on overall similarities, An even more unexpected example, exposed by Fjeldsa˚ often overlooked natural relationships, and the present et al. (2005), is that Xenops shares with Glyphorhynchus result is therefore no great surprise. The overall good a unique functional system for hammering in wood. Also phylogenetic agreement between the results presented a different interpretation of Clench’s (1995) study of the herein and other studies of ovenbirds based on DNA- pterylosis patterns of woodcreepers and ovenbirds sup- sequences partly obtained from other genes (Irestedt port this relationship, as Xenops and woodcreepers et al. 2002, Chesser 2004) are, on the other hand, a shares a lower number of in the pars dorsalis

266 JOURNAL OF AVIAN BIOLOGY 37:3 (2006) Fig. 1 (Continued ) Cranioleuca sulphurifera C) 1.00 Limnoctites rectirostris 1.00 Cranioleuca albicapilla 0.62 0.64 1.00 Cranioleuca pyrrhophia Xenerpestes singularis Asthenes cactorum 0.64 Synallaxis ruficapilla 0.97 Synallaxis scutata Schoeniophylax phryganophilus 1.00 1.00 Certhiaxis cinnamomeus Pseudoseisura lophotes 1.00 Oreophylax moreirae 1.00 1.00 Schizoeaca harterti Asthenes urubambensis 0.93 Anumbius annumbi 0.99 0.96 0.64 Coryphistera alaudina Hellmayrea gularis 0.61 Phacellodomus ruber Leptasthenura pileata Premnornis guttuligera 0.78 Pseudocolaptes boissonneautii Aphrastura spinicauda Cinclodes fuscus 1.00 Upucerthia jelskii 0.80 1.00 Limnornis curvirostris 0.64 Phleocryptes melanops 0.83 Lochmias nematura 0.56 Furnarius cristatus 0.94 1.00 Furnarius leucopus Berlepschia rikeri Margarornis squamiger 0.62 Premnoplex brunnescens 0.90 Pygarrhichas albogularis Anabacerthia striaticollis 0.69 Syndactyla rufosuperciliata 0.53 0.95 Megaxenops parnaguae Heliobletus contaminatus Philydor atricapillus 1.00 Hylocryptus erythrocephalus 1.00 Automolus leucophthalmus 0.74 Thripadectes flammulatus Xenops minutus 1.00 0.84 Xenops rutilans Campylorhamphus trochilirostris 0.66 Drymornis bridgesii 0.59 Xiphorhynchus erythropygius 0.80 Nasica longirostris 1.00 Xiphocolaptes major 1.00 1.00 Deconychura longicauda 0.64 Sittasomus griseicapillus 0.96 1.00 Dendrocincla tyrannina Glyphorynchus spirurus Sclerurus mexicanus 1.00 Sclerurus scansor 1.00 Geositta rufipennis 0.76 Geositta tenuirostris Pteroptochos tarnii 1.00 Scytalopus spillmanni Chamaeza meruloides than found in ovenbirds. Nevertheless, other morpholo- corroborated by molecular data, while other groups gical characters are sometimes in conflict with the results could be rejected or modified. While the Furnariinae presented herein. Thus, the ‘‘Margarornis assemblage’’, and Synallaxinae in large parts remains intact, although as defined from characters from the hindlimb muscu- with somewhat different generic compositions, the lature (Rudge and Raikow 1992), is suggested to be non- philydorine ovenbirds are unlikely to be monophyletic monophyletic by our molecular data. However, Irestedt (see also Fjeldsa˚ et al. 2005): four ‘‘philydorine’’ clades et al. (2004b) and McCracken et al. (1999) have found could be recognized; (1) a core foliage-gleaners clade similar conflicts between molecular data and morpho- (Anabacerthia, Syndactyla, Megaxenops, Heliobletus, logical characters from the hindlimb, suggesting that Philydor, Automolus, Hylocryptus, and Thripadectes), hindlimb characters may often be under adaptive selec- (2) a clade with Margarornis, Premnoplex and Pygar- tion and less useful in phylogenetic reconstructions. This rhichas, (3) a clade with Premnornis and Pseudocolaptes, might also be case for several other morphological and (4) a clade for the aberrant Berlepschia. Except for characters (that have been used to infer relationships the Premnornis and Pseudocolaptes clade, these foliage- among ovenbirds and woodcreepers) that are in conflict gleaner clades are positioned basal to traditional furnar- with the present molecular phylogeny. iines and synallaxines, but the combined phylogeny As a consequence of our much denser taxon sampling suggests that they are separated by fairly long inter- than in previous DNA-based phylogenies of ovenbirds, nodes. Most noticeable is the position of Premnornis and several taxa with contested affinity can now be placed, Pseudocolaptes, which strongly suggests that the Phily- some traditional groupings can for the fist time be dorinae is an unnatural group.

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 267 Cranioleuca sulphurifera 1.00 Fig. 2. The 50% majority rule Limnoctites rectirostris 1.00 consensus tree obtained from the Cranioleuca albicapilla Cranioleuca pyrrhophia analyses of the combined data set 1.00 0.98 Synallaxis ruficapilla (G3PDH intron 11, the myoglobin 1.00 0.97 Synallaxis scutata intron 2 and the cytochrome b data Schoeniophylax phryganophilus 1.00 sets). Posterior probability values are 1.00 Certhiaxis cinnamomeus Asthenes cactorum indicated to the right of the nodes. 0.93 Pseudoseisura lophotes 0.99 Oreophylax moreirae 1.00 1.00 Schizoeaca harterti 1.00 Asthenes urubambensis 0.89 Anumbius annumbi 1.00 Coryphistera alaudina 0.70 Hellmayrea gularis Phacellodomus ruber 0.98 Leptasthenura pileata 0.96 Aphrastura spinicauda Limnornis curvirostris 1.00 Phleocryptes melanops 0.99 1.00 Lochmias nematura 0.68 Cinclodes fuscus 1.00 Upucerthia jelskii 0.74 1.00 Furnarius cristatus 1.00 0.90 Furnarius leucopus Premnornis guttuligera 1.00 Pseudocolaptes boissonneautii Margarornis squamiger 0.69 Premnoplex brunnescens 0.99 Pygarrhichas albogularis Anabacerthia striaticollis 0.98 1.00 Syndactyla rufosuperciliata 1.00 Megaxenops parnaguae 1.00 Heliobletus contaminatus 1.00 1.00 Philydor atricapillus Automolus leucophthalmus 0.97 Hylocryptus erythrocephalus 1.00 Thripadectes flammulatus Berlepschia rikeri 1.00 Campylorhamphus trochilirostris 0.95 Drymornis bridgesii 1.00 1.00 Xiphorhynchus erythropygius Nasica longirostris 1.00 1.00 Xiphocolaptes major Deconychura longicauda 0.95 Sittasomus griseicapillus 1.00 1.00 1.00 Dendrocincla tyrannina 1.00 Glyphorynchus spirurus Xenops minutus 1.00 Xenops rutilans Sclerurus mexicanus 1.00 Sclerurus scansor 1.00 Geositta rufipennis 1.00 Geositta tenuirostris Pteroptochos tarnii 1.00 Scytalopus spillmanni Chamaeza meruloides

Ecological shifts and morphology ovenbirds (generally adapted to more xeric life zones and more opened landscapes) would represent more The new phylogenetic groupings might seem surprising drastic shifts of environment. in view of the general similarities in external morphology Although the Furnariinae and Synallaxinae clades between ‘‘philydorine’’ ovenbirds (even though certain remain largely intact in the combined molecular tree, genera such as Margarornis and Pygarrhichas are quite some of the suggested relationships are novel. Most divergent from the typical philydorines). However, based noticeable is the placement of reedhaunters, with Lim- on our combined phylogeny (Fig. 2), it is obvious that nornis forming a clade with Phleocryptes, close to deeper branches (except for Geositta) comprise forest Lochmias, within the Furnariinae ovenbirds, and Lim- birds of a fairly uniform appearance. noctites being placed among the Synallaxinae ovenbirds. The most parsimonious solution of the ovenbird The relationships of all these have been obscure, but the radiation is thus an early forest diversification, leading suggested relationship between Phleocryptes and Lim- to divergence of woodcreepers, a large radiation of nornis is supported by their similar nest architecture foliage-gleaners, most of which obtained their food by (Zyskowski and Prum 1999). These relationships are probing and prying in internodes and among masses of discussed in further detail by Olson et al. (2005). dead leaves and debris suspended among vines and Other forest taxa that have been difficult to place are branches (Fjeldsa˚ et al. 2005), and lineages that specia- Megaxenops and Heliobletus, which now can be placed, lized to search food in epiphyte-clad cloud-forest and with high confidence, among the philydorine foliage- shrubbery of the rising Andean mountains. Thus the gleaners. Cytochrome b and G3PDH data, respectively, terminal radiations of Furnariinae and Synallaxinae also provide good evidence for placing Xenerpestes and

268 JOURNAL OF AVIAN BIOLOGY 37:3 (2006) Metopothrix among the synallaxines, near the Cranio- and also serve as dormitories for family groups (Zys- leuca group, and it is therefore likely that Siptornis and kowski and Prum 1999, Remsen 2003). Mapping of the the odd, new-described Acrobatornis (Pacheco et al. general nesting strategies (as coded by Zyskowski and 1996) also belong here. Prum 1999) onto the combined phylogeny indicates that It is finally interesting to see that the large genus cavity nesting is plesiomorphic within ovenbirds (Fig. 3), Asthenes, which is mainly associated with open montane a hypothesis that accords with the frequent use of cavity- habitats, may not be a natural taxon. Further studies are nesting among the closest relatives of Furnariidae needed to see how many Asthenes species (and Thripo- (Ridgely and Tudor 1994, Krabbe and Schulenberg phaga softtails) that fall outside the main group 2003) and with the phylogenetic results by Zyskowski (represented here by A. cactorum). and Prum (1999). The woodcreepers often use cavities Environmental factors clearly put morphological rather low in the trees, or even subterranean (as constraints on birds. Certain morphologies are repeat- Sclerurinae), and have simple nest-cups, and we suggest edly observed in obviously unrelated passerine species that this was the ancestral condition in the Furnariidae. that occupy forested habitats, while other morphologies The shift from cavity nesting to building vegetative are shared by species living in open habitats. Not nests is a rather rare evolutionary event in birds, but our surprisingly, the large and ecologically diverse data suggest that it has happened at least three times in ovenbird/woodcreeper radiation includes many exam- the Furnariidae: One time early in the evolution of the ples of morphological parallels to distantly related synallaxine clade, another time in the ancestor of some passerine birds with similar adaptations (Remsen genera within the enlarged furnariine clade, and a

2003). Given two independent cases of cavity nesters third time within the ‘‘philydorine’’ Pygarrhichas / colonizing open habitats in the ovenbird/woodcreeper Premnoplex /Margarornis clade (Fig. 3). However, note radiation (Geositta and the Furnariinae clade) and that that the synallaxine, furnariine, and Pygarrhichas /Pre- shifts from cavity nesting to building vegetative nests mnoplex /Margarornis clades are rather terminal have independently happened at least three times within lineages that share a common ancestor in our phylogeny. the ovenbird/woodcreeper radiation (see below), it is An alternative explanation might thus be that this not surprising to also find several examples of parallel common ancestor sometimes placed a reduced vegetative morphological evolution within this radiation. However, nest in cavities and built a more advanced vegetative nest other instances of similar-looking taxa, for example the placed in the open at other times, as do Premnoplex and ‘‘philydorine’’ Premnoplex and Premnornis, may not be Leptasthenura. The pre-disposed ability to vary nest explained by convergent evolution. Instead, the phylo- architecture may then have been the major source for the geny suggests that the deep nodes in the ovenbird/ nest patterns we find within these clades today. Note also woodcreeper radiation mainly consisted of forest birds that our phylogeny lacks Eremobius, a genus close to that nested in cavities and that often resemble each other Upucerthia based on morphology that builds a stick-nest in size, plumage and shape. The superficial similarities placed in the open. between various ‘‘philydorine’’ lineages may thus be due It is noticeable that species that built enclosed to their shared retention of a plesiomorphic, ‘‘philydor- vegetative nests within cavities are basal in all the ine’’ appearance. lineages where this major shift in nests architecture took places, suggesting that the shift from cavity nesting to building enclosed vegetative nests is a gradual process. Shifts in nest architecture as innovations in the Lochmias, which is positioned basally in the phylogeny Limnornis Phleocryptes diversification of ovenbirds to the vegetative nesters and within the furnariine clade, builds a domed vegetative As mentioned, ovenbirds exhibit an extraordinary di- nest within a cavity. Within the ‘‘philydorine’’ versity in nest placement and structure, including the Pygarrhichas /Premnoplex /Margarornis clade, Premno- construction of various types of nests in cavities and plex often places its domed moss nest in a cavity, and crevices, massive ‘‘houses’’ in clay, and vegetative that of Margarornis is often placed under a limb or a structure, which in some cases attain gigantic dimensions rock. Aphrastura, which constitutes the most basal

Fig. 3. Distribution of nest habits within the ovenbird-woodcreeper radiation. Principal nest strategies (nest in cavity and/or domed vegetative structure) have been mapped on the tree obtained from the analysis of the combined molecular data set. Data on nest habits are mainly from Zyskowski and Prum (1999), and for a few taxa from Remsen (2003). Black branches indicate cavity nesting, blue branches represent the habit of building enclosed vegetative nests placed in the open, and green branches indicate that enclosed vegetative nests are placed within cavities. Note also that the black branches to the representatives of Furnarius have been marked with blue stripes as it is difficult to tell whether the complex, domed Furnarius nest, built of clay and dung with admixed hairs and plant fibres, should be regarded as a case of cave-nesting (as coded by Zyskowski and Prum 1999) or as homologous with a domed vegetative nest. The asterisk after the names Premnoplex brunnescens and Leptasthenura pileata indicates that these taxa sometimes place their vegetative nests in cavities and sometimes in the open. Two asterisks mark taxa for which the nest habits are insufficiently known. Note that Xenerpestes singularis and Metopothrix aurantiaca have tentatively been added to the tree based on their relative position in the cytochrome b and G3PDH trees, respectively.

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 269 Cranioleuca sulphurifera Limnoctites rectirostris Cranioleuca albicapilla Cranioleuca pyrrhophia Xenerpestes / Metopothrix Synallaxis ruficapilla Synallaxis scutata Schoeniophylax phryganophilus Certhiaxis cinnamomeus Asthenes cactorum Pseudoseisura lophotes Oreophylax moreirae Schizoeaca harterti Asthenes urubambensis Anumbius annumbi Coryphistera alaudina Hellmayrea gularis** Phacellodomus ruber Leptasthenura pileata* Aphrastura spinicauda Limnornis curvirostris Phleocryptes melanops Lochmias nematura Cinclodes fuscus Upucerthia jelskii Furnarius cristatus Furnarius leucopus Premnornis guttuligera** Pseudocolaptes boissonneautii Margarornis squamiger Premnoplex brunnescens* Pygarrhichas albogularis Anabacerthia striaticollis Syndactyla rufosuperciliata Megaxenops parnaguae** Heliobletus contaminatus** Philydor atricapillus Automolus leucophthalmus Hylocryptus erythrocephalus Thripadectes flammulatus Berlepschia rikeri** Campylorhamphus trochilirostris Drymornis bridgesii Xiphorhynchus erythropygius Nasica longirostris Xiphocolaptes major Deconychura longicauda Sittasomus griseicapillus Dendrocincla tyrannina Glyphorynchus spirurus Xenops minutus Xenops rutilans Sclerurus mexicanus Sclerurus scansor Geositta rufipennis Geosittatenuirostris Pteroptochos tarnii Scytalopus spillmanni Chamaeza meruloides

Fig. 3 (Continued )

270 JOURNAL OF AVIAN BIOLOGY 37:3 (2006) branch in the synallaxine clade, builds a cup-shaped nest denser taxon sampling, as well as a more information that partially covers the wall of the cavity. Leptasthe- about nest architecture in critical groups, is needed to get nura, the next branch in the synallaxine clade, builds a a full understanding of the evolution of nesting strategies domed vegetative nest that often is placed within a cavity in ovenbirds. (Zyskowski and Prum 1999). Building a closed nest structure inside a cavity would Acknowledgements / Tissue and blood samples were mainly obtained from the Zoological Museum of Copenhagen (with immediately seem to represent unnecessary extra labour, data collecting supported by the Danish Research Councils) and but may have served a function of securing less humid the Swedish Museum of Natural History (collected in conditions inside the nest. It is noteworthy that the collaboration with the Museo Nacional de Historia Natural del Paraguay, San Lorenzo). Important samples have also been change in nest construction happened in lineages in- obtained from the American Museum of Natural History, New habiting montane environments, and it is worth noting in York, Academy of Natural Sciences of Philadelphia, and the this respect that also Andean tapaculos (Scytalopus) National Museum of Natural History, Smithsonian Institution. often build a closed nest of moss inside cavities. It is Mari Ka¨llersjo¨ provided logistic support and advice for the work at the Molecular Systematics Laboratory at the Swedish unfortunate, for this interpretation, that the nest of Museum of Natural History, and Pia Eldena¨s and Dario Hellmayrea, which inhabits humid Andean forest, is still Zuccon is thanked for practical support at the laboratory. undescribed. Lochmias breeds near streams in montane Bernd Leisler and an anonymous reviewer are thanked for valuable comments on the manuscript. The Swedish Research forests, thus in a humid environment, and Leptasthenura Council (grant no. 621/2004/2913 to P.E.) funded the spp. inhabit a broad habitat spectrum from humid tree- laboratory work. lines to semiarid highlands. However, other taxa repre- senting deeper synallaxine branches, Phacellodomus, Coryphistera and Anumbius, mainly inhabit drier scrub and savanna, where they assemble enormous masses of References interwoven thorny twigs, containing a system of tunnels, Akaike, H. 1973. Information theory as an extension of the and a nest chamber. It is therefore not fully clear under maximum likelihood principle. / In: Petrov, B. N., Csaki, F. what environmental conditions the shifts in nest-con- (eds). Second International Symposium on Information Theory. Akademiai Kiado, Budapest, pp. 267/281. struction happened. Ames, P. L. 1971. The morphology of the syrinx in passerine The fact that the terminal synallaxine and furnariine birds. / Bull. Peabody Mus. Nat. Hist. 37: 1/194. radiations comprise no less than 115 species and 38 Alstro¨m, P. and O¨ deen, A. 2002. Incongruence between mitochondrial DNA, nuclear DNA and non-molecular species, respectively, compared with 119 species in all the data in the avian genus Motacilla: implications for estimates remaining lineages of Furnariidae (incl. Dendrocolapti- of species phylogenies. / In: Alstro¨m, P. Species limits and nae), suggests that the shift in nest architecture may have Systematics in Some Passerine Birds. Ph. D.-thesis, Uppsala University. served as an innovation spurring further diversification. Chesser, R. T. 2004. Molecular systematics of New World This includes adaptations to new environments. Natural Suboscine birds. / Mol. Phyl. Evol. 32: 11/24. cavities or ground patches suitable for excavating tunnels Cibois, A., Slikas, B., Schulenberg, T. S. and Pasquet, E. 2001. are often in limited supply in open landscapes (Remsen An endemic radiation of Malagasy songbirds is revealed by mitochondrial DNA sequence data. / Evolution 55: 1198/ 2003), and the ability to build own vegetative nest 1206. obviously gives a competitive advantage in such environ- Clench, H. M. 1995. Body pterylosis of woodcreepers and ments. In case of marsh habitats, home of Phleocryptes, ovenbirds (Dendrocolaptidae and Furnariidae). / Auk 112: 800/804. Limnornis and Limnoctites, there is no possibility to find Collias, N. E. 1997. On the origin and evolution of nest building a cavity or excavate a tunnel. In the Andean cloud- by passerine bird. / Condor 99: 253/270. forests a small closed nest structure can easily be hidden Degnan, S. M. 1993. The perils of single gene trees / mitochondrial versus single-copy nuclear DNA variation in in the enormous masses of epiphytes that are often white-eyes (Aves: Zosteropidae). / Mol. Ecol. 2: 219/225. found, which may have played a role among the Ericson, P. G. P., Christidis, L., Irestedt, M. and Norman, J. A. synallaxines, and could also explain why Margarornis 2002. Systematic affinities of the lyrebirds (Passeriformes: Menura), with a novel classification of the major groups of and Premnoplex build domed moss nests. passerine birds. / Mol. Phyl. Evol. 25: 53/62. It is noticeable that several of the nest characteristics Feduccia, A. 1973. Evolutionary trends in the Neotropical of ovenbirds, as coded by Zyskowski and Prum (1999), ovenbirds and woodhewers. / Ornithol. Monogr. 13: 1/69. become synapomorphies for subclades of taxa when Fjeldsa˚, J., Zuccon, D., Irestedt, M., Johansson, U. S. and Ericson, P. G. P. 2003. Sapayoa aenigma: a New World mapped onto our combined phylogeny. Examples are the representative of ‘Old World suboscines’. / Proc. R. Soc. Sphagnum nests of Schizoeaca and Oreophylax, the Lond. B. (Suppl.) 270: 238/241. thatch placed over the camber in Certhiaxis, Schoenio- Fjeldsa˚, J., Irestedt, M. and Ericson, P. G. P. 2005. Molecular data reveal some major adaptational shifts in the early phylax and Synallaxis, the roof adornments in Anum- evolution of the most diverse avian family, the Furnariidae. bius and Coryphistera, and the pensile nest-type of / J. Ornithol. 146: 1/13. Cranioleuca and possibly Xenerpestes (Remsen 2003, p. Grant, P. R. 1986. Ecology and evolution of Darwin’d finches. / Princeton Univ. Press, Princeton N.J. 319). Other nest characteristics exhibit a large degree of Hellmayr, C. E. 1925. Catalogue of birds of the Americas. convergent evolution. However, a phylogeny based on a / Field Mus. Nat. Hist., Zool. Ser., vol. 13.

JOURNAL OF AVIAN BIOLOGY 37:3 (2006) 271 Holder, M. and Lewis, P. O. 2003. Phylogeny estimation: Olson, S. R., Irestedt, M., Ericson, P. G. P and Fjeldsa˚, J. 2005. Traditional and Bayesian approaches. / Nature Genetics Independent evolution of two Darwinian marsh-dwelling 4: 275/284. ovenbirds (Furnariidae: Limnornis, Limnoctites). / Orn. Huelsenbeck, J. P., Larget, B., Miller, R. E. and Ronquist, F. Neotropical 16: 347/359. 2002. Potential applications and pitfalls of Bayesian infer- Pacheco, J. F., Whitney, B. M. and Gonzaga, L. P. 1996. A new ence of phylogeny. / Syst. Biol. 51: 673/688. genus and species of furnariid (Aves: Furnariidae) from the Huelsenbeck, J. P., Ronquist, F., Nielsen, R. and Bollback, J. P. cocoa-growing southeastern Bahia, Brazil. / Wilson Bull. 2001. Reverend Bayes meets Darwin: Bayesian inference of 108: 397/606. phylogeny and its impact on evolutionary biology. / Science Raikow, R. J. 1994. A phylogeny of the woodcreepers (Den- 288: 2349/2350. drocolaptinae). / Auk 111: 104/114. Irestedt, M., Fjeldsa˚, J., Johansson, U. S. and Ericson, P. G. P. Raikow, R. J. and Bledsoe, A. H. 2000. Phylogeny and evolution 2002. Systematic relationships and biogeography of the of the Passerine birds. / BioScience 50: 487/499. tracheophone suboscines (Aves: Passeriformes). / Mol. Remsen, J. V. 2003. Family Furnariidae (Ovenbirds). / In: del Phyl. Evol. 23: 499/512. Hoyo, J., Elliot, A. and Christie, D. (eds). Handbook of the Irestedt, M., Fjeldsa˚, J., Nylander, J. A. A. and Ericson, P. G. P. Birds of the World. Broadbills to Tapaculos. BirdLife 2004a. Phylogenetic relationships of typical antbirds (Tham- International and Lynx Edicions; Cambridge U.K. / and nophilidae) and test of incongruence based on Bayes Barcelona 8: 162/357. factors. / BMC Evolutionary Biology 4: 23. Ricklefs, R. E. 2003. Global diversification rates of passerine Irestedt, M., Fjeldsa˚, J. and Ericson, P. G. P. 2004b. Phyloge- birds. / Proc. R. Soc. B 270: 2285/2291. netic relationships of woodcreepers (Aves: Dendrocolapti- Ridgely, R.S. and Tudor, G. 1994. The birds of South America. nae)-incongruence between molecular and morphological / University of Texas Press, Austin, vol. II. data. / J. Avian Biol. 35: 280/288. Ronquist, F. and Huelsenbeck, J. P. 2003. MRBAYES 3: Krabbe, N. K. and Schulenberg, T. S. 2003. Family Formicar- Bayesian phylogenetic inference under mixed models. iidae (Ground-antbirds). / In: del Hoyo, J., Elliot, A. and / Bioinformatics 19: 1572/1574. Christie, D. (eds). Handbook of the Birds of the World. Rudge, D. W. and Raikow, R. J. 1992. The phylogenetic Broadbills to Tapaculos. BirdLife International and Lynx relationship of the Margarornis assemblage (Furnariidae). Edicions; Cambridge U.K. / and Barcelona 8: 682/731. / Condor 94: 760/766. Leisler, B. 1977. komorphologische Aspekte von Speziation und Sibley, C. G. and Ahlquist, J. E. 1990. Phylogeny and adaptiver Radiation bei Vo¨geln. / Vogelwarte 29: 136/153. classification of the birds of the World. / Yale University Maddison, W. P. 1997. Gene trees in species trees. / Syst. Press, New Haven, CT. / Biol. 46: 523/536. Sick, H. 1993. Birds in Brazil. A natural history. / Princeton McCracken, K. G., Harshman, J., McClellan, D. A. and Afton, University Press, Princeton, New Jersey. A. D. 1999. Data set incongruence and correlated character Swofford, D. L. 1998. Paup*. Phylogenetic analysis using evolution: An Example of functional convergence in the parsimony (* and other methods), v.4. / Sinauer, Sunder- hind-limbs of stifftail diving ducks. / Syst. Biol. 48: 683/ land. 714. Vaurie, C. 1971. Classification of the ovenbirds (Furnariidae). Mindell D.P. 1997. Avian molecular evolution and systematics. / London. / Academic press, San Diego, California. Vaurie, C. 1980. and geographical distribution of the Moore, W. S. 1995. Inferring phylogenies from mtDNA varia- Furnariidae (Aves, Passeriformes). / Bull. Am. Mus. Nat. tion: Mitochondrial-gene trees versus nuclear-gene trees. Hist. 166: 1/357. / Evolution 49: 718/726. Zimmer, K.J. and Isler. K.J. 2003. Family Thamnophilidae Moore W. S. and DeFillips V. R. 1997. The window of (typical antbirds). / In: del Hoyo, J., Elliot, H. and Christie, taxonomic resolution for phylogenies based on mitochon- D. (eds). Handbook of the birds of the World, vol. 8, drial cytochrome b. / In: Mindell, D. P. (ed.). Avian broadbills to tapaculos, Lynx Ed., Barcelona, pp. 448/681. Molecular Evolution and Systematics. San Diego and Zyskowski, K. and Prum, R. O. 1999. Phylogenetic analysis of London: Academic press, pp. 83/119. the nest architecture of neotropical ovenbirds (Furnariidae). Nylander, J. A. A. 2002. MrModeltest v.1.0. Program distrib- / Auk 116: 891/911. uted by the author. / Department of Systematic Zoology, Uppsala University, Uppsala. Olson, S. R. 2001. Why so many kinds of passerine birds? / (Received 3 January 2005, revised 8 April 2005, accepted BioScience 51: 268/269. 9 April 2005.)

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