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On the Origin of the Galápagos Hawk: an Examination of Phenotypic Differentiation and Mitochondrial Paraphyly

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On the Origin of the Galápagos Hawk: an Examination of Phenotypic Differentiation and Mitochondrial Paraphyly Biological Journal of the Linnean Society, 2008, 95, 779–789. With 3 figures On the origin of the Galápagos hawk: an examination of phenotypic differentiation and mitochondrial paraphyly JOSHUA M. HULL1*, WESLEY K. SAVAGE2, JENNIFER L. BOLLMER3, REBECCA T. KIMBALL4, PATRICIA G. PARKER3, NOAH K. WHITEMAN3,5 and HOLLY B. ERNEST1,6 1Wildlife and Ecology Unit, Veterinary Genetics Laboratory, University of California, One Shields Avenue, Davis, CA 95616, USA 2Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA 3Department of Biology, University of Missouri – St Louis, St. Louis, MO 63121, USA 4Department of Zoology, University of Florida, PO Box 118525, Gainesville, FL 32611, USA 5Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA 6Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, One Shields Avenue, Davis, CA 95616, USA Received 18 September 2007; accepted for publication 11 March 2008 Previous phylogenetic hypotheses suggest a sister group relationship between mainland and widespread Buteo swainsoni (Swainson’s hawk) and the island archipelago taxon Buteo galapagoensis (Galápagos hawk). We further describe phylogenetic relationships of this clade using molecular data from the mitochondrial control region, and consider the role of niche expansion on phenotype using morphological data from B. galapagoensis, B. swainsoni, and related Buteo jamaicensis (red-tailed hawk). Among 52 unique Buteo haplotypes, phylogenetic analyses support a monophyletic B. galapagoensis clade within a clade of B. swainsoni haplotypes, rendering B. swainsoni paraphyletic with respect to B. galapagoensis. Mitochondrial paraphyly is likely a result of incomplete lineage sorting subsequent to a recent colonization event and exemplifies speciation of peripheral population isolates. Morphological comparisons indicate that metrics associated with prey capture differ significantly between B. galapagoensis and B. swainsoni, but are similar between B. galapagoensis and B. jamaicensis. These results suggest directional selection on B. galapagoensis morphology associated with feeding, possibly an outcome of decreased interspecific competition and change towards a more generalist diet shared by B. jamaicensis. In the B. galapagoensis lineage, our results suggest that genetic drift influences the neutral mitochondrial marker, whereas selection may have driven phenotypic character change. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 779–789. ADDITIONAL KEYWORDS: Buteo galapagoensis – Buteo swainsoni – archipelago – island – morphology – niche expansion. INTRODUCTION may be of varying importance depending upon the character under investigation (Lynch, 1990; Clegg Differentiation between island and mainland popula- et al., 2002). Under the neutral theory, noncoding tions of species may result from several factors, genomic DNA, not closely linked to regions under including population size, genetic drift, selection, and positive selection, will be affected by stochastic pro- the extent of ongoing gene exchange (Wright, 1931; cesses such as genetic drift (Kimura, 1983), with no Barton, 1998). Between sister species, these processes direct connection to phenotypic change (Bromham & Hendy, 2000; Bromham et al., 2002, but see also *Corresponding author. E-mail: [email protected] Omland, 1997). Consequently, divergence in neutral © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 779–789 779 780 J. M. HULL ET AL. molecular markers and phenotype is predicted to Table 1. Sample size for genetic and morphological data proceed independently. (including the number of females and males in parenthe- Rapid phenotypic change from an ancestral main- ses) from Buteo swainsoni, Buteo galapagoensis, and Buteo land phenotype is frequently observed among island jamaicensis taxa (Lack, 1971; Grant, 1998) and has been attrib- uted to several processes, including founder effects, Species Genetic Morphological change in selective landscape, relaxation of interspe- cific competition, and niche expansion (Grant, 1998; Buteo swainsoni 308 104 (38/66) Whittaker, 1998; Rasner et al., 2004). Among birds Buteo galapagoensis 122 217 (91/126) Española 10 19 (10/9) and mammals, morphological changes among island Isabela 20 19 (11/8) species often follow the ‘island rule’ (Foster, 1964; Van Santa Fe 9 18 (9/9) Valen, 1973; Lomolino, 1985; Clegg & Owens, 2002), Santiago 21 128 (54/74) where small-bodied taxa evolve to larger size and Marchena 15 21 (4/17) larger-bodied taxa evolve towards smaller size. Such Pinta 13 12 (3/9) phenotypic changes between island and mainland Fernandina 20 0 taxa can mislead assumptions of phylogenetic rela- Pinzón 10 0 tionships. Phylogenetic analysis using character Santa Cruz 4 0 information from neutral molecular markers (particu- Buteo jamaicensis 5 132 (45/87) larly those with smaller effective population sizes), in conjunction with morphological characters, can facili- tate an objective examination of the relationships The present study aimed to describe the phylo- among closely-related taxa and an understanding of genetic relationship between B. swainsoni and B. the evolutionary processes leading to their divergence galapagoensis with fine-scale sampling, and to inves- (Scott et al., 2003). tigate the extent of molecular and morphological Buteo swainsoni (Swainson’s hawks; Bonaparte) differentiation. Accordingly, we describe the phyloge- and Buteo galapagoensis (Galápagos hawks; Gould) netic relationship between these Buteo species using are phenotypically distinct in body size, plumage, samples from throughout their current ranges to test diet, and mating system, and their geographic ranges the monophyly of each lineage and to evaluate the are entirely non-overlapping and differ greatly in strength of morphological differentiation. We investi- extent. Buteo swainsoni is an abundant raptor species gate phenotypic divergence by comparing five mor- that breeds throughout western North America and a phological characters among B. galapagoensis, B. large number of individuals migrate through central swainsoni, and Buteo jamaicensis (red-tailed hawk; America to the grasslands of South America Gmelin). We include B. jamaicensis to provide a con- (England, Bechard & Houston, 1997). Limited micro- trast between a generalist mainland Buteo and a satellite population genetic structure exists across generalist island taxon (B. galapagoensis). their breeding range (Hull et al., 2008) and regional differences in morphology have not been documented MATERIAL AND METHODS (England et al., 1997). By contrast, B. galapagoensis are restricted to eight (historically eleven) islands of SAMPLE COLLECTION the Galápagos archipelago (de Vries, 1975, 1976). We collected whole blood and feathers from 365 B. Extremely limited dispersal occurs among the islands swainsoni and 122 B. galapagoensis, as well as and most populations are genetically distinct five Buteo regalis (ferruginous hawk), three Buteo (Bollmer et al., 2005) and differ in morphology lagopus (rough-legged hawk), six Buteo lineatus (red- (Bollmer et al., 2003). Until recently, the obvious phe- shouldered hawk), five B. jamaicensis, and one Buteo notypic and behavioural differences between B. albicaudatus (white-tailed hawk) for outgroup com- swainsoni and B. galapagoensis (de Vries, 1975, 1976) parison. Blood was stored in lysis buffer and feathers have been regarded as untested evidence for the rec- were stored dry. Three hundred and thirty-six B. ognition of two divergent Buteo species. Moreover, a swainsoni were sampled on breeding grounds (from sister relationship between these two species was not June to July) in North America (for locality informa- evident based on phenotypic evidence (de Vries, 1973). tion, see Table 1) between 2003 and 2005, and the Recent mitochondrial phylogenetics of the genus remaining 29 B. swainsoni were captured on wintering Buteo shows a close sister relationship between B. grounds in central Argentina during January 2003, as swainsoni and B. galapagoensis (Riesing et al., 2003) described previously (Whiteman et al., 2006). Samples with an estimated Galápagos colonization 126 000 were collected from 122 B. galapagoensis (Table 1) years ago (95% confidence interval = 51 000–254 000 captured with either bal-chatris or rope nooses on years; Bollmer et al., 2006). poles. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 779–789 PARAPHYLY IN B. SWAINSONI AND B. GALAPAGOENSIS 781 LABORATORY METHODS 3.1 (Kumar, Tamura & Nei, 2004) to confirm our For B. swainsoni samples, we isolated total cellular approximation of the most parsimonious tree recon- DNA from 25 ml of the blood/buffer solution using struction (closest-neighbour-interchange with search Qiagen DNeasy kits (QIAGEN Inc.). We extracted level 3, random addition trees with 900 replications). genomic DNA from B. galapagoensis samples using a MODELTEST, version 3.7 (Posada & Crandall, modification of phenol/chloroform extraction (Sam- 1998) was used to evaluate the best-fit model of brook, Fritsch & Maniatis, 1989) with final purification nucleotide evolution and parameter estimation to the control region sequence data for the ML tree search. by dialysis against TNE2. A total of 367 bp of domain I of the mitochondrial control region were amplified
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