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Plumage Convergence in Picoides Woodpeckers Based on a Molecular Phylogeny, with Emphasis on Convergence in Downy and Hairy Woodpeckers Amy C

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Wayne State University Biological Sciences Faculty Research Publications Biological Sciences 11-1-2005 Plumage convergence in Picoides woodpeckers based on a molecular phylogeny, with emphasis on convergence in downy and hairy woodpeckers Amy C. Weibel Wayne State University, [email protected] William S. Moore Wayne State University, [email protected] Recommended Citation Weibel, A. C. and Moore, W. S. 2005. Plumage convergence in Picoides woodpeckers based on a molecular phylogeny, with emphasis on convergence in downy and hairy woodpeckers. Condor 107(4):797-809. http://dx.doi.org/10.1650/7858.1 Available at: http://digitalcommons.wayne.edu/biosci_frp/11 This Article is brought to you for free and open access by the Biological Sciences at DigitalCommons@WayneState. It has been accepted for inclusion in Biological Sciences Faculty Research Publications by an authorized administrator of DigitalCommons@WayneState. The Condor 107:797±809 q The Cooper Ornithological Society 2005 PLUMAGE CONVERGENCE IN PICOIDES WOODPECKERS BASED ON A MOLECULAR PHYLOGENY, WITH EMPHASIS ON CONVERGENCE IN DOWNY AND HAIRY WOODPECKERS AMY C. WEIBEL1 AND WILLIAM S. MOORE Department of Biological Sciences, Wayne State University, Detroit, MI 48202 Abstract. Adult and juvenile plumage characters were traced onto a well-resolved mo- lecular based phylogeny for Picoides woodpeckers, and a simple phylogenetic test of ho- mology, parallelism, and convergence of plumage characters was performed. Reconstruction of ancestral character states revealed multiple events of independent evolution of derived character states in most characters studied, and a concentrated changes test revealed that some plumage characters evolved in association with habitat type. For example, there was a statistically signi®cant association between loss of dorsal barring and use of densely veg- etated habitats among Picoides species. Two analyses indicated that convergence, as opposed to parallel evolution or shared ancestry, underlies the similarity in plumage patterns between the Downy (Picoides pubescens) and Hairy (P. villosus) Woodpeckers. Possible causal ex- planations for convergence in plumage patterns may include mimicry and interspeci®c ter- ritoriality. Key words: adaptation, character evolution, convergence, Picoides, plumage, wood- peckers. Convergencia en Plumaje en PaÂjaros Carpinteros del GeÂnero Picoides Basada en una Filogenia Molecular, con E nfasis en la ConvergeÂncia entre Picoides pubescens y P. villosus Resumen. Se reconstruyo la evolucioÂn de caracteres del plumaje de individuos adultos y juveniles con base en una ®logenia molecular bien resuelta de los paÂjaros carpinteros del geÂnero Picoides. El estudio provee una prueba ®logeneÂtica sencilla de homologõÂa, parale- lismo y convergencia para los caracteres de plumaje. Las reconstrucciones de estados de caracter ancestrales revelaron muÂltiples eventos de evolucioÂn independiente de estados de caracter derivados en casi todos los caracteres estudiados, y una prueba de cambios con- centrados revelo que algunos caracteres del plumaje evolucionaron en asociacioÂn con el tipo de haÂbitat. Por ejemplo, existe una asociacioÂn estadõÂsticamente signi®cativa entre la peÂrdida de barras dorsales y el uso de ambientes con vegetacioÂn densa en las especies de Picoides. Dos anaÂlisis indicaron que la similitud en los patrones de plumaje entre Picoides pubescens y P. villosus puede explicarse por convergencia, no por evolucioÂn paralela o por ancestrõÂa comuÂn. Se discuten posibles explicaciones causales para la convergencia, como la imitacioÂn y la territorialidad interespecõ®ca. INTRODUCTION forces in species that experience similar envi- The comparative method is a general and pow- ronments (Bell 1989, Harvey and Pagel 1991, erful approach for testing hypotheses of adap- Nee et al. 1996). Independent evolutionary tation (Ridley 1983) and identifying evolution- events can be identi®ed from a well-resolved ary trends (Ridley 1983, Harvey and Pagel phylogeny of the group of taxa under investi- 1991) across a range of taxonomic groups. Char- gation (Pagel and Harvey 1988, Losos 1990, acter states may be maintained in descendent Brooks and McLennan 1991, Omland 1999) and lineages and persist in extant sister species be- analyzed using the comparative method. cause of shared ancestry (Wilson 1975, Harvey Phenotypic resemblance among species may and Mace 1982, McKitrick 1993) or may evolve result from homology, parallel evolution, or con- independently in response to similar selective vergence. Homology of characters implies struc- tural resemblance due to shared ancestry (Boy- den 1973, Patterson 1982). In a review of his- Manuscript received 19 April 2005; accepted 10 Au- torical concepts and de®nitions of homology, gust 2005. 1 Present address: Academic Affairs, Grand Canyon Patterson (1982) noted that true homologies are University, Phoenix, AZ 85017. E-mail: acweibel@ synapomorphies, and thus the test for homology msn.com of similar character states is also a test of con- [797] 798 AMY C. WEIBEL AND WILLIAM S. MOORE gruence within a monophyletic group. Similar METHODS character states resulting from parallel or con- The phylogeny that served as the comparative vergent evolution are homoplasies and, collec- framework for this study was estimated from tively, are distinguished from homologies by in- pooled DNA sequences of two mitochondrial congruence with other character states that de- protein-coding genes, cytochrome oxidase I ®ne a monophyletic group. Parallel and conver- (COI) and cytochrome b (cyt b), and a nuclear gent evolution are more dif®cult to distinguish gene intron, b-®brinogen intron 7 (b-®bint7) from each other. Parallel evolution implies struc- (Weibel and Moore 2002b). The phylogeny is tural resemblance in derived character states the maximum likelihood topology for the data among closely related species in which devel- set based on a general time-reversible nucleotide opmental pathways were similarly yet indepen- rate variation model that included the proportion dently modi®ed after separation of evolutionary of invariable sites and the gamma distribution lineages from a common ancestor, whereas con- shape parameter (GTR 1 I 1G). The portion of vergence in phenotypes results from modi®ca- the Weibel and Moore (2002b) tree relevant to tion of different antecedent characters or differ- this study is presented in Figure 2 and 3. ent developmental pathways in distantly related Adult plumage data were collected from study species (Futuyma 1998). Thus, the subtle dis- skins housed at the University of Michigan Mu- tinction between parallel and convergent evolu- seum of Natural History. Male and female adult tion is linked to development as well as phylog- plumages were evaluated using characters and eny, and inferences that distinguish the two can methods following Short (1971). Because of be made by studying developmental pathways substantial geographic variation in most Picoi- that transform juvenile to adult character states des species, we selected for study subspecies in a phylogenetic context. that were used by Winkler et al. (1995) for spe- In this study we used MacClade (Maddison cies descriptions. Juvenile plumage character and Maddison 1992) to examine plumage char- data were extracted primarily from Short (1971, acter data of Picoides woodpeckers in the con- 1982), Ehrlich et al. (1988), and Winkler et al. text of a well-resolved, DNA-sequence-based (1995). Data were arranged into two matrices phylogeny. Characters are traced or mapped (adult plumage and juvenile plumage). Charac- onto a phylogeny using the criterion of maxi- ters were individually traced onto the 3-gene mum parsimony; character state transformations species tree using the criterion of simple parsi- are polarized and ancestral character states are mony (unordered parsimony) in MacClade, ver- sion 3.0 (Maddison and Maddison 1992), in inferred. Thus, patterns of character evolution which gains and losses are given equal proba- are detected that allow hypotheses regarding the bilities and ancestral states are reconstructed direction of evolution, adaptation, and develop- based on character states of extant lineages. The mental programs to be tested. phylogeny is rooted (Weibel and Moore 2002a, A particularly intriguing example of apparent 2002b), thus character states are polarized al- convergence in plumage characteristics occurs lowing inference of ancestral versus derived in the Hairy (Picoides villosus) and Downy (P. states in the Picoides clade. pubescens) Woodpeckers. These two broadly Levels of similarity in plumage patterns sympatric species are so similar in plumage that among species pairs were evaluated, and the to- they can be dif®cult to distinguish in the ®eld tal number of character states (ancestral 1 de- without side-by-side comparison, yet they are rived) held in common for all pairwise species not closely related (Weibel and Moore 2002a, comparisons in each of the two plumage matri- 2002b). Although each species belongs to a dis- ces were tabulated. The empirical distributions tinct clade, they more closely resemble each oth- of total character states held in common between er than other members of their respective clades pairs of species were represented in histograms (Fig. 1). Here we test the hypothesis of conver- for adult and juvenile plumage data using NCSS gence in plumage characters in Picoides wood- 2000 statistical software (Hintze 1999). Pairs of peckers and discuss potential adaptive causes
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