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Moore2009chap65.Pdf Woodpeckers, toucans, barbets, and allies (Piciformes) William S. Moorea,* and Kathleen J. Migliab and divergence times of the Order Piciformes and its aDepartment of Biological Sciences, Wayne State University, Detroit, constituent clades to the level of families. MI 48202, USA; bDuke University Medical Center, Molecular As many as eight nominal families have been included Genetics & Microbiology, 210 Jones Building, Box 3020 Durham, in the Order Piciformes under various classiA cations: NC 27710, USA Picidae (wrynecks, piculets, and woodpeckers; ~28 gen- *To whom correspondence should be addressed (wmoore@biology. biosci.wayne.edu) era, 216 species), Indicatoridae (honeyguides; ~4 genera, 17 species), Megalaimidae (Asian barbets; ~3 genera, 26 species), Lybiidae (African barbets; ~7 genera, 42 spe- Abstract cies), Capitonidae (New World barbets; ~2 genera, 13 species), Ramphastidae (toucans; ~7 genera, 36 species, The avian Order Piciformes comprises two major lineages, the Pici and Galbulae, which diverged as early as 70 million years ago (Ma). The jacamars and puffbirds (Galbulae) also diverged relatively early, ~53 Ma. Later diversifi cation of the Pici gave rise to six additional families, beginning ~44–38 Ma. Molecular clock estimates for the origins of piciform clades, some estimated here, are consistent with the chron- ology of the sparse fossil record. With the exception of the woodpeckers, species of several piciform families were abundant on the northern continents during the Paleogene (66–23 Ma) but are now restricted to the tropics. 7 e Order Piciformes is a diverse assemblage of bird species that vary greatly in size, appearance, distri- bution, ecology, and life history. To the extent one can make descriptive generalizations, they tend to be stocky, brightly colored birds with disproportionately large bills—taken to an extreme in the toucans—and arbor- eal habits (Fig. 1). 7 eir distributions are restricted to the Asian, African, and New World tropics, with the excep- tion of the woodpeckers, which collectively have a more expansive distribution that includes the Old and New World temperate regions. Most species are insectivorous but many eat fruit at least occasionally and the barbets are primarily frugivorous. Cavity nesting is pervasive in the order, as is particularly well known for the woodpeckers, which have adaptations of the bill, skull, and associated musculature and enervation that renders them extra- ordinarily eB ective at excavating nest cavities in wood. 7 e honeyguides are nest parasites, but parasitize only Fig. 1 A Red-headed Woodpecker (Melanerpes erythrocephalus), cavity-nesting species. Here we review the relationships Family Picidae, from North America. Photo credit: R. Moul. W. S. Moore and K. J. Miglia. Woodpeckers, toucans, barbets, and allies (Piciformes). Pp. 445–450 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 444545 11/28/2009/28/2009 11:29:32:29:32 PPMM 446 THE TIMETREE OF LIFE Ramphastidae 7 6 Capitonidae 4 Lybiidae Megalaimidae Pici 3 Indicatoridae 5 1 Picidae Bucconidae 2 Galbulidae Galbulae Paleogene Neogene CENOZOIC 50 25 0 Million years ago Fig. 2 The timetree of woodpeckers, toucans, barbets, and allies (Piciformes). Divergence times are shown in Table 1. including two species of Semnornis), Galbulidae (jaca- were subsequently corroborated in a study by Lanyon mars; ~5 genera, 18 species), and Bucconidae (pu irds; and Zink (7) based on protein electromorph characters, ~12 genera, 35 species). Collectively, the species assigned although the latter study did not include a honeyguide to these families group into two clades that diverged rela- (Indicatoridae). 7 e tree hypothesized in these studies is tively early in the diversiA cation of Neoaves (1, 2). One ((((Indicatoridae, Picidae), (Ramphastidae, Capitonidae)), clade comprises the Galbulidae and Bucconidae and the (Bucconidae, Galbulidae)), Outgroup). Although these other comprises the Picidae, Indicatoridae, and barbets studies produced congruent results, some intraordinal and toucans, regardless of how the barbets and toucans details remained to be determined, and monophyly of are assigned to nominal families. 7 ese two ancient lin- the order as well as identiA cation of its closest relative eages are considered distinct orders, Galbuliformes and remained contentious. Piciformes, in some classiA cations, but suborders, Pici Olson (8), Burton (9), and Sibley and Ahlquist (4) and Galbulae, of Piciformes in others. Regardless of the argued that Piciformes is polyphyletic with the Galbulae nomenclature, the evidence is strong that the Pici and (Bucconidae and Galbulidae) related to the coraciiforms. Galbulae are both monophyletic. Until very recently, Lanyon and Zink (7) were not able to test the hypoth- however, it was less certain whether the Pici and Galbulae esis of monophyly of Piciformes directly, but they noted were closest relatives, but three recent studies based on that their distance data supported a closer relation- DNA sequence data from nuclear-encoded genes strongly ship of Galbulae to a coraciiform ( Momotus) than to support this hypothesis (1, 2, 10). 7 us, it is reasonable to other piciforms, which suggests paraphyly. However, recognize the Order Piciformes comprising two major recent DNA sequence-based studies consistently sup- lineages, the Pici and Galbulae, totaling ~403 species. port monophyly of Piciformes at statistically signiA cant Using Peters (3) classiA cation as a reference list for levels (1, 2, 10). Johansson and Ericson’s (1) study, based species usually included in an order called Piciformes, on exon segments from the nuclear RAG1 and c-myc the history of systematic groupings of those species genes and intron II from the myoglobin gene totaling into families, superfamilies, and suborders is a kaleido- 3400 nucleotides, was speciA cally designed to test the scope through the nineteenth and much of the twen- close relationship of Pici and Galbulae and thus mono- tieth centuries. 7 e early systematic history has been phyly of Piciformes. Combining all sequences from the thoroughly reviewed (1,4–6). Considerable stability of three genes, monophyly was supported by maximum inferred relationships was established with the cladistic parsimony (90% bootstrap) and Bayesian (100% poster- studies of Swierczewski and Raikow ( 5), and Simpson ior probability) analyses. 7 e maximum likelihood ana- and CracraJ (6) based on myological and osteological lysis based on the “Early Bird” data set also inferred a characters. 7 ese studies reached identical conclusions monophyletic Piciformes with 100% BS support (2). 7 e regarding relationships among piciform families, which “Early Bird” data set is more comprehensive and includes HHedges.indbedges.indb 444646 11/28/2009/28/2009 11:29:35:29:35 PPMM Eukaryota; Metazoa; Vertebrata; Aves; Piciformes 447 Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among woodpeckers, toucans, barbets, and allies (Piciformes). Timetree Estimates Node Time Ref. (10) Ref. (17) Ref. (22) Time Time CI Time CI 161.85370.589–5793.6107–80 255.05356.974–4473.692–53 340.943.638.151–2873.289–59 431.532.530.542–21– – 529.930.928.840–20– – 6 24.6 24.6 24.6 – 50.9 65–36 7 13.4 13.4 13.4 – 48 63–34 Note: Node times in the timetree represent the mean of time estimates from two studies (10, 17). PATHd8 analysis of DNA sequences from fi ve nuclear genes was conducted in ref. (10). Ref. (17) presents a reanalysis of the same data using the Bayesian program Multidivtime. Some divergence times were estimated here, which is detailed in the text. ~32,000 nucleotides from 19 nuclear gene regions and likelihood and Bayesian) and a dense taxon sample ena- 169 species. 7 us the inferred descent of species, listed bled him to resolve nearly complete relationships among by Peters, from a common ancestor is probably true; that species comprising the traditional Capitonidae and is, Piciformes is monophyletic and, thus, a valid taxon. Ramphastidae, including enigmatic basal lineages and/or With regard to relationships within and among fam- convergent lineages such as Gymnobucco, Calorhamphus, ilies, the greatest uncertainty has involved the barbets Semnornis, and Trachyphonus. and toucans. Traditionally the barbets, which occur in Moyle’s analyses strongly support the existence of three the African, Asian, and New World tropics, were con- geographically deA ned clades: Asian barbets, African sidered a single family, the Capitonidae, and the tou- barbets, and New World barbets, the last one including cans, which are restricted to the New World, were put the toucans. 7 is is consistent with the earlier A nding of in a separate family, the Ramphastidae (3). A series of Sibley and Ahlquist (4), and their recognition of three recent studies, however, have been consistent in show- families is warranted: Lybiidae (African), Megalaimidae ing that the traditional Capitonidae is paraphyletic with (Asian), and Capitonidae (New World). Recognition of a close relationship between the New World barbets and the Family Ramphastidae also seems warranted, but toucans and that the Asian and African barbets, each a the placement of the toucan-barbet, Semnornis ram- distinct clade, are more distantly related. 7 ese recent phastinus, then becomes an issue. 7 is species, which studies are based on anatomical (9, 11) as well as molecu- appears very much like what one might imagine as the lar characters (4, 12–14). common ancestor of
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