Molecular Data Reveal Some Major Adaptational Shifts in the Early Evolution of the Most Diverse Avian Family, the Furnariidae
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J Ornithol (2005) 146: 1–13 DOI 10.1007/s10336-004-0054-5 ORIGINAL ARTICLE Jon Fjeldsa˚Æ Martin Irestedt Æ Per G. P. Ericson Molecular data reveal some major adaptational shifts in the early evolution of the most diverse avian family, the Furnariidae Received: 15 March 2004 / Revised: 19 May 2004 / Accepted: 20 May 2004 / Published online: 14 September 2004 Ó Dt. Ornithologen-Gesellschaft e.V. 2004 Abstract A robust phylogeny estimate for the family clusters and debris suspended in the vegetation, and in Furnariidae (sensu lato) was obtained using sequences of epiphyte masses. Adaptations to live in open terrain are two nuclear introns and one mitochondrial gene (cyt b). secondary. Contrary to the widely accepted sister-group relationship of ovenbirds (Furnariinae) and woodcreepers (Dendro- Keywords Adaptative shifts Æ Bayesian analysis Æ colaptinae), a basal clade is suggested for Sclerurus and Dendrocolaptinae Æ Furnariinae Æ Nuclear introns Geositta, while Xenops, hitherto considered an aberrant ovenbird, was found to occupy a basal position on the woodcreeper lineage. The morphological variation is re- Introduction interpreted in view of this revised phylogenetic hypothe- sis. Presumably, the remarkable adaptive radiation in this The South American ovenbirds, Furnariinae, exhibit a family started as primitive, Sclerurus-likes forms, which morphological heterogeneity that is unparalleled among used the tail as a prop during terrestrial feeding, lured up avian groups on that taxonomic level (Leisler 1977; to seek food on tree-trunks. The two basal woodcreeper Vaurie 1980; Remsen 2003). Inhabiting all habitats from genera, Xenops and then Glyphorynchus, show strong tropical rainforest to deserts, and all strata, the currently cranial specializations for hammering in wood, thus pre- recognized 236 species vary greatly in size and devel- senting a remarkable parallelism with the family Picidae, opment of peculiar tail-shapes. This is in strong contrast Xenops resembling a piculet, Glyphorynchus, a diminutive to their presumed sister group (Sibley and Ahlquist woodpecker. However, this specialization was lost in 1990), the woodcreepers (Dendrocolaptinae), all 69 other woodcreepers, which show a more normal passerine species of which nest in cavities and are scansorial with skull, adapted for probing and prying in tree-trunk cre- specialized tail-tips providing support as they climb on vices and sallying for escaping insects. The ovenbirds tree-trunks, like woodpeckers (Marantz et al. 2003). developed a more flexible (rhynchokinetic) bill, well suited The ovenbirds are traditionally divided into three for probing and retrieving hidden prey in dead-leaf broad groups (Hellmayr 1925; Vaurie 1971, 1980; Sibley and Ahlquist 1990, for historical review): the ground-liv- ing Furnarini, which resemble thrashers and slender-bil- Electronic Supplementary Material Supplementary material is led larks; the ‘‘spinetails’’ Synallaxini, which are small and available in the online version of this article at http://dx.doi.org/ acrobatic, with long and in many cases peculiarly shaped 10.1007/s10336-004-0054-5 tails; and the Philydorini, which are more heavily built Communicated by A.J. Helbig forest ovenbirds. Sclerurus leaftossers and the monotypic genus Lochmias have been regarded as a separate sub- J. Fjeldsa˚ (&) family, Sclerurinae (Sclater 1890), but are placed near the Zoological Museum, University of Copenhagen, end, or near the beginning, respectively, of the Philydorini Universitetsparken 15, 2100 Copenhagen, Denmark E-mail: [email protected] sequence. However, characters have not been specified that clearly define the three groups, and aberrant forms M. Irestedt have been embedded or placed at the ends of the taxo- Department of Zoology, University of Stockholm, 106 91 Stockholm, Sweden nomic sequence of these groups, often with no other evi- dence than a superficial plumage similarity with some core P. G. P. Ericson Department of Vertebrate Zoology and Molecular Systematics members of that group. This is, for instance, the case with Laboratory, Swedish Museum of Natural History, some ovenbirds with similar stiff tail-spines as the wood- P.O. Box 50007, 104 05 Stockholm, Sweden creepers, namely Aphrastura, which are usually placed at 2 the beginning of the synallaxine group, Margarornis, the Electronic Supplementary Material). These represent which is placed at beginning of the philydorine group, and the major subgroups that previously have been sug- Pygarrhicas, which is appended at the end of that group. gested for ovenbirds (Hellmayr 1925; Vaurie 1971, 1980; The peculiar Xenops species, tiny canopy birds with re- Ridgely and Tudor, 1994) and woodcreepers (Feduccia curved and laterally flattened bills, are also placed near the 1973; Raikow 1994; Marantz et al. 2003; Irestedt et al. end of the philydorine sequence. Geositta is placed first in 2004a; the two latter papers based on molecular data). the entire ovenbird group, because of a primitive syringial As the first phylogenetic analyses yielded unexpected character shared with the woodcreepers, and it is then placements of the genera Geositta, Sclerurus and Xenops followed by furnarines of similar body shape. These (see below), one additional representative of each of placements simply reflect the agony of choice when no these genera was added to verify the authenticity of the clear character analysis was used to determine a sequence samples. Two representatives from the family Rhino- of phylogenetic branches. Without a clear phylogenetic cryptidae and one from the Formicariidae were used as hypothesis it is difficult to exclude the possibility that some outgroup taxa, as these families have been suggested as of these aberrant genera could be ancestral forms, which forming the sister clade to Furnariidae (Irestedt et al. would most logically be placed in the beginning of the 2002). classification. The following genetic markers were sequenced: the Modern molecular systematics has provided numer- complete myoglobin intron 2 (along with 13 bp and ous examples of taxonomic neglect caused by the past 10 bp of the flanking exons 2 and 3, respectively), cor- tendency to ‘‘bury’’ aberrant species and genera into responding to position 303 (exon 2) through 400 (exon larger and well-known groups based on overall similar- 3) in humans (GenBank accession number XM009949), ity (e.g.,‘‘Yuhina’’ zantholeuca, see Cibois et al. 2002; the complete glyceraldehydes-3-phosphodehydrogenase Sapayoa, see Fjeldsa˚ et al. 2003; Pseudopodoces, see (G3PDH) intron 11 (along with 36 bp and 18 bp of James et al. 2003). A preliminary molecular analysis of exons 11 and 12, respectively) corresponding to the re- the tracheophone suboscine birds of South America gion 3,915 to 4,327 in Gallus gallus (GenBank accession (Irestedt et al. 2002) revealed some cases of neglected number M11213) and 999 bp of the cytochrome b gene, ‘‘ancestral’’ types, e.g., the ‘‘tapaculo’’ genus Melano- corresponding to positions 15,037 to 16,035 in the pareia was found to represent an ancestral lineage from chicken mitochondrial genome sequence (Desjardins near the base of the entire tracheophone radiation, and and Morais 1990) (for primer sequences see Table 2, and Sclerurus was found to be a sister taxon to other oven- see also Supplementary Table 2 in the Electronic Sup- birds and woodcreepers (see also Chesser 2004). We now plementary Material; for laboratory procedures see Er- follow this up with more thorough studies of individual icson et al. 2002; Irestedt et al. 2002; Fjeldsa˚ et al. 2003). tracheophone families (see Irestedt et al. 2004a, 2004b). Positions where the nucleotide could not be determined Here, we aim to define the deep branching pattern of the with certainty were coded with the appropriate IUPAC ovenbird-woodcreeper radiation. (ambiguity) code. Due to the low number of insertions in Since little is gained by just presenting new patterns of the introns, the combined sequences could easily be grouping that may be more high-tech and objective than aligned by eye (Appendices 1 and 2 in the Electronic traditional, morphology-based grouping (see Lipscomb Supplementary Material). All gaps in the myoglobin and et al. 2003), we will supplement the phylogenetic analysis the G3PDH sequences were treated as missing data in by examining how some morphological characters vary the analyses. No insertions, deletions, stop or nonsense among the deeper branches. By contrasting phylogenetic codons were observed in any of the cytochrome b se- and morphological information we hope to provide evi- quences. dence about the early adaptive shifts, and identify what adaptive changes may have spurred the spectacular adaptive radiation of the ovenbird-woodcreeper assem- Phylogenetic inference and model selection blage. By doing this we hope to provide a better basis for interpreting the many specializations that took place We used Bayesian inference for estimating phylogenetic during the further diversification. However, the finer hypothesis from our DNA data (see recent reviews by branching pattern of the ovenbird radiation, the alloca- Huelsenbeck et al. 2002; Holder and Lewis 2003). Prior tion of genera to subgroups, and a suggested new classi- to the analyses, the models for nucleotide substitutions fication, will be presented in another publication. were selected for each gene individually by using Akaike Information Criterion (AIC; Akaike 1973) and the program MrModeltest (Nylander 2002) in conjunction Materials and methods with PAUP* (Swofford