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In Vanuatu Zosterops Divergence in Two Species of the Influence Of Downloaded from rstb.royalsocietypublishing.org on March 1, 2010 The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu Sonya M. Clegg and Albert B. Phillimore Phil. Trans. R. Soc. B 2010 365, 1077-1092 doi: 10.1098/rstb.2009.0281 Supplementary data "Data Supplement" http://rstb.royalsocietypublishing.org/content/suppl/2010/02/22/365.1543.1077.DC1.ht ml References This article cites 72 articles, 15 of which can be accessed free http://rstb.royalsocietypublishing.org/content/365/1543/1077.full.html#ref-list-1 Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1543/1077 Subject collections Articles on similar topics can be found in the following collections molecular biology (214 articles) evolution (1458 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on March 1, 2010 Phil. Trans. R. Soc. B (2010) 365, 1077–1092 doi:10.1098/rstb.2009.0281 The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu Sonya M. Clegg1,2,* and Albert B. Phillimore1,3 1Division of Biology, Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY, UK 2Biodiversity and Geosciences Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland 4101, Australia 3NERC Centre for Population Biology, Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY, UK Colonization of an archipelago sets the stage for adaptive radiation. However, some archipelagos are home to spectacular radiations, while others have much lower levels of diversification. The amount of gene flow among allopatric populations is one factor proposed to contribute to this variation. In island colonizing birds, selection for reduced dispersal ability is predicted to produce changing pat- terns of regional population genetic structure as gene flow-dominated systems give way to drift- mediated divergence. If this transition is important in facilitating phenotypic divergence, levels of genetic and phenotypic divergence should be associated. We consider population genetic structure and phenotypic divergence among two co-distributed, congeneric (Genus: Zosterops) bird species inhabiting the Vanuatu archipelago. The more recent colonist, Z. lateralis, exhibits genetic patterns consistent with a strong influence of distance-mediated gene flow. However, complex patterns of asymmetrical gene flow indicate variation in dispersal ability or inclination among populations. The endemic species, Z. flavifrons, shows only a partial transition towards a drift-mediated system, despite a long evolutionary history on the archipelago. We find no strong evidence that gene flow constrains phenotypic divergence in either species, suggesting that levels of inter-island gene flow do not explain the absence of a radiation across this archipelago. Keywords: Vanuatu; regional population structure; gene flow; allopatric divergence; island birds 1. INTRODUCTION Vogler 2000; Coyne & Price 2000; Phillimore et al. The role of geographical separation and consequent 2008a). elimination of gene flow in driving population diver- Fragmented landscapes, such as archipelagos, pro- gence was a central tenet of the speciation models vide a tractable setting to assess the influence of that emerged from the modern synthesis (Dobzhansky geography on genetic and phenotypic divergence 1937;Mayr1942, 1954). While allopatric speciation, (e.g. Clegg et al. 2002a; Petren et al. 2005; Jordan & with zero or very low levels of gene flow, is probably Snell 2008; Phillimore et al. 2008b). For insular popu- the most common geographic mode for many taxa lations at the beginning of the speciation continuum (Barraclough & Vogler 2000; Coyne & Orr 2004; (sensu Mayr & Diamond (2001), e.g. populations Phillimore et al. 2008a; Price 2008), some contempor- lacking (subspecific) geographic variation, subspecies ary views place greater emphasis on ecological or allospecies), the characterization of patterns of divergence and diversifying selection pressures, rather genetic connectivity among island populations can than the geographic context of divergence (Ogden & contribute to an understanding of the influence of Thorpe 2002; Jordan et al. 2005; Rundle & Nosil geographical isolation on gene flow patterns and 2005; Bolnick & Fitzpatrick 2007; Butlin et al. 2008; phenotypic divergence. Nosil 2008). Nonetheless, in birds, only a few cases Correspondence between geographic and genetic of potential sympatric or parapatric speciation have isolation largely depends on an organism’s vagility been identified (Sorenson et al. 2003; Huber et al. (Burney & Brumfield 2009), an attribute that can 2007; Ryan et al. 2007; Smith & Friesen 2007) and change over time in island colonizing species. Evi- the majority of sister-species have contemporary range dence from plants (Cody & Overton 1996) and birds distributions that do not overlap (Barraclough & (McNab 1994; Adler et al. 1995) suggests that island dwelling can result in selection for reduced dispersal abilities (see also Grant 1998). The changing patterns * Author for correspondence ([email protected]). of population connectivity among islands are expected Electronic supplementary material is available at http://dx.doi.org/ to produce distinct signatures of regional population 10.1098/rstb.2009.0281 or via http://rstb.royalsocietypublishing.org. genetic structure at neutral loci (Hutchison & One contribution of 13 to a Theme Issue ‘Darwin’s Gala´pagos Templeton 1999). If the colonizing ability of a species finches in modern evolutionary biology’. were maintained over time, then there would be weak 1077 This journal is q 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on March 1, 2010 1078 S. M. Clegg & A. B. Phillimore Gene flow and drift in island Zosterops relationships expected between the level of geographic Moyle et al. (2009) suggested that rapid evolutionary isolation and genetic variation within and among shifts in dispersal ability, rather than adaptive ecologi- populations. cal explanations were important for high speciation Even in highly vagile organisms, ongoing within- rates in the family. At a population level therefore, archipelago dispersal and gene flow can be affected waning gene flow among Zosterops populations on by behavioural or morphological changes that reduce different islands may be an important catalyst of diver- the inclination or ability to effectively disperse gence. Divergent natural selection on phenotype has across water barriers (Diamond et al. 1976; Mayr & been demonstrated in a number of island white-eye Diamond 2001). Distance-limited dispersal is populations (Clegg et al. 2002a, 2008) but the facili- expected to generate a gene flow-mediated population tating effects of shifts in dispersal ability and gene structure evidenced by a negative relationship between flow are not clear. neutral genetic diversity and geographic isolation While the distribution and morphological variation (Jordan & Snell 2008), the establishment of of southwest Pacific avifauna provided the foundation isolation-by-distance patterns of genetic differentiation for many early ideas about island speciation (Mayr (Slatkin 1993; Hutchison & Templeton 1999) and low 1954; Mayr & Diamond 2001), phylogeographic and probabilities of alleles being identical by descent population genetic studies of the avifauna of this within populations (Ciofi et al. 1999). If geographically region are only now beginning to accumulate separated populations become progressively more (Kirchman & Franklin 2007; Smith & Filardi 2007; genetically isolated over time, gene flow is expected Phillimore et al. 2008b), lagging behind other well- to yield to drift as the predominant mechanism shap- studied island groups such as the Gala´pagos (Petren ing population structure, producing a positive et al. 1999), the Caribbean (see Ricklefs & relationship between neutral genetic diversity and Bermingham (2007) and references therein) and population size (approximated by island area), but Hawaii (Fleischer & McIntosh 2001). In the Vanuatu not isolation (Lande & Barrowclough 1987; e.g. archipelago, two Zosterops species, the endemic Hinten et al. 2003; Jordan & Snell 2008), a breakdown Z. flavifrons and the later colonizer Z. lateralis have lar- of isolation by distance patterns (Hutchison & gely coincident distributions, but are at different stages Templeton 1999) and a high probability that alleles of divergence (Mees 1969; Phillimore 2006; Black within a population are identical by descent (Ciofi 2010). This situation allows us to contrast genetic et al. 1999). These represent extremes in a spectrum and phenotypic patterns across the same landscape and intermediate patterns may also arise as regional in related, ecologically similar species that differ in population structure shifts, e.g. partial isolation-by- age across islands. We compare regional population distance patterns (Hutchison & Templeton 1999) structure in the two species, examining the relative and generation of geographic patterns for types of importance of gene flow and drift across the variation most sensitive to demographic change (e.g. archipelago and within-individual island populations.
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