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Evolution of the Ovenbird-Woodcreeper Assemblage (Aves: Furnariidae) Б/ Major Shifts in Nest Architecture and Adaptive Radiatio

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Evolution of the Ovenbird-Woodcreeper Assemblage (Aves: Furnariidae) Б/ Major Shifts in Nest Architecture and Adaptive Radiatio JOURNAL OF AVIAN BIOLOGY 37: 260Á/272, 2006 Evolution of the ovenbird-woodcreeper assemblage (Aves: Furnariidae) / major shifts in nest architecture and adaptive radiation Á 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) Á/ major shifts in nest architecture and adaptive radiation. Á/ J. Avian Biol. 37: 260Á/272 The Neotropical ovenbirds (Furnariidae) form an extraordinary morphologically and ecologically diverse passerine radiation, which includes many examples of species that are superficially similar to other passerine birds 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 genus-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 Geositta and Sclerurus form the sister clade to both core-ovenbirds and woodcreepers. 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 ovenbirdÁ/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, DKÁ/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 larks (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 basal 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 Xenops 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
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