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Subtle Edge-Of-Range Genetic Structuring in Transcontinentally Distributed North American Tree Swallows

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Subtle Edge-Of-Range Genetic Structuring in Transcontinentally Distributed North American Tree Swallows The Condor 111(3):470–478 ¡ The Cooper Ornithological Society 2009 SUBTLE EDGE-OF-RANGE GENETIC STRUCTURING IN TRANSCONTINENTALLY DISTRIBUTED NORTH AMERICAN TREE SWALLOWS LAURA M. STENZLER1,5, CHRISTOPHER A. MAKAREWICH1, AURÉLIE COULON1,3, DANIEL R. ARDIA4, IRBY J. LOVETTE1,2, AND DAV I D W. WINKLER2 1Fuller Evolutionary Biology Program, Laboratory of Ornithology, Cornell University, Ithaca, NY 14850 2Museum of Vertebrates and Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853 3UMR 7179 Muséum National d’Histoire Naturelle/Centre National de la Recherche Scientifique, 1 avenue du Petit Château, 91800 Brunoy, France 4Department of Biology, Franklin and Marshall College, Lancaster, PA 17604 Abstract. Understanding how genetic variation in the Tree Swallow (Tachycineta bicolor) is geographically structured is informative because this broadly distributed North American bird is increasingly used as a model for studies of mating systems, life-history traits, and physiology. We explored patterns of phylogeographic differentia- tion across the Tree Swallow’s breeding range by using nine microsatellite loci and a mitochondrial DNA sequence marker. Contrary to this species’ high population-level variation in life-history traits and other ecologically impor- tant characteristics, we found no genetic structuring across the majority of its distribution, spanning Tennessee, New York, and Alaska, but we found that birds from California form a distinct yet subtly differentiated genetic cluster. The Tree Swallow can be characterized as a species with both continent-wide genetic panmixia and slight differentiation at one edge of its breeding distribution. This pattern of genetic variation has implications for under- standing the underlying basis of geographic variation in this species’ life history and other phenotypic traits. Key words: genetic structure, geographic variation, microsatellites, mitochondrial DNA, Tachycineta bicolor, Tree Swallow. Sutil Estructuración Genética en el Borde del Área de Distribución Transcontinental de Tachycineta bicolor Resumen. Entender la estructuración geográfica de la variación genética de Tachycineta bicolor es infor- mativo debido a que esta especie, que se distribuye ampliamente en Norteamérica, se está usando cada vez más como modelo para estudios sobre sistemas de apareamiento, caracteres de historia de vida y fisiología. Explora- mos los patrones de diferenciación filogeográfica en todo el área de distribución reproductiva de T. bicolor usando nueve loci microsatelitales y un marcador de secuencia de ADN mitocondrial. De modo contrastante a la alta variación que se observa a nivel poblacional en los caracteres de historia de vida y otras características ecológi- cas importantes, no encontramos estructuración genética en la mayor parte del área de distribución, que incluye los estados de Tennessee, Nueva York y Alaska. Sin embargo, encontramos que las aves de California forman un agrupamiento genético distintivo aunque sutilmente diferenciado. Esta golondrina puede ser caracterizada tanto como una especie con panmixia continental, como una especie con una pequeña diferenciación geográfica en un extremo de su distribución geográfica. Este patrón de variación genética tiene implicaciones importantes para el entendimiento de la variación geográfica de las características de historia de vida y otros caracteres fenotípicos de esta especie. species is taxonomically monotypic with no described sub- INTRODUCTION species, it shows substantial geographic variation in reproduc- Owing to the hundreds of studies that have taken advantage tive effort (Dunn et al. 2000, Ardia 2005, Monroe et al. 2008), of its tractability, the Tree Swallow (Tachycineta bicolor) offspring development (McCarty 2001, Ardia 2006), and im- has been termed a “model species” for research topics span- mune responses (Ardia 2005, Ardia 2007). Little is known, ning mating systems to immunology to climate change (Jones however, about patterns of genetic differentiation or connec- 2003). Tree Swallows breed across nearly all of temperate tivity among Tree Swallow populations or about the extent to North America, and past research on them has taken place at which the observed geographic variation in phenotypic traits many locations across this broad distribution. Although the is related to underlying population structuring. Manuscript received 6 October 2008; accepted 29 April 2009. 5E-mail: [email protected] The Condor, Vol. 111, Number 3, pages 470–478. ISSN 0010-5422, electronic ISSN 1938-5422. 2009 by The Cooper Ornithological Society. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.com/ reprintInfo.asp. DOI: 10.1525/cond.2009.080052 470 08_MS080052.indd 470 8/27/09 12:46:30 PM GENETIC VARIABILITY OF TREE SWALLOWS 471 Despite the paucity of information on genetic structur- As the Tree Swallow has the broad distribution and low mor- ing, the ease with which cavity-nesting Tree Swallows can be phological variation often associated with this type of recent banded and monitored during the breeding season has resulted range enlargement, we explored whether its pattern of genetic in a large and well-documented collection of information on variation in mitochondrial DNA is consistent with a history of direct dispersal distances (Hosner and Winkler 2007), which demographic expansion. To examine distribution-wide levels allows us to make a priori predictions about the likely ge- of genetic population structuring further, we obtained sam- netic population structure of the species. Tree Swallows breed ples from sites that span the range of the species north–south throughout central and northern North America and are con- and east–west, and we tested for differentiation among these tinuously distributed from Maine to Alaska and as far south populations by using both microsatellite and mitochondrial as Tennessee and southern California (Robertson et al. 1992). sequence markers. Banding recoveries indicate that Tree Swallows have sub- stantial potential for long-distance dispersal from where they METHODS fledge or breed (Winkler et al. 2004, 2005). Recapture data SAMPLE COLLECTION from the U.S. Bird Banding Laboratory and the more spatially focused Swallow Dispersal Study allowed Hosner and Win- Tree Swallows frequently use man-made nest boxes for breed- kler (2007) to document dispersal distances of up to 2367 km, ing, which made it possible for us to collect blood from adult although the majority (85%) of known dispersals occurred birds trapped when they entered to brood or feed young. Sam- among sites separated by less than 15 km. Nevertheless, even pled individuals were banded with a U.S. Fish and Wildlife rare long-distance dispersal could be sufficient to homogenize Service band before blood was collected (100–200 µl) from allele frequencies across long distances (Wright 1931, Slat- the brachial vein into heparinized microhematocrit tubes and kin 1987). This combination of a continuous distribution with stored at room temperature in 0.5 ml of lysis buffer (0.1 M no known major physical barriers to movement, annual mi- Tris [pH 8.0], 0.1 M EDTA, 10 mM NaCl, 0.5% SDS) (White gration, and documented long-distance dispersal leads to the and Densmore 1992). The geographic coordinates of sampled potential for high genetic exchange and little or no spatial ge- boxes (or clusters of closely located boxes) were obtained with netic structure in the Tree Swallow, as was found in one of the a handheld GPS unit. No voucher specimens were collected classic first phylogeographic surveys of a broadly distributed because all swallows were from study sites used for active North American songbird, the Red-winged Blackbird (Age- monitoring of reproductive success and other ecological and laius phoeniceus), whose geographic variation in morphology behavioral variables. is greater (Ball et al. 1988). Some other North American birds We sampled birds from four sites that together span the also have little genetic structure over large portions of their majority of the species’ breeding range: sites in New York and breeding ranges (e.g., Gibbs et al. 2000, Milot et al. 2001, Zink Ontario were sampled in 1998 and 1999, sites in Alaska, Cali- et al. 2006). However, geographic patterns of genetic differ- fornia, and Tennessee in 2003. The spatial distribution of sam- entiation may arise even in highly dispersive taxa as a result of pled birds differed somewhat by site: 300 birds came from 15 evolutionary forces opposing gene flow, such as local adapta- sites in New York and one in Ontario (11–412 km apart) (Sten- tion in response to strong selection and/or genetic drift acting zler 2001), 37 birds were sampled from three sites in Alaska on small effective population sizes within locally interbreed- (3–8 km apart), 46 birds were from three sites in California ing populations (Slatkin 1987, Freeman-Gallant 1996), from (separated by up to 500 km), and 25 birds were sampled from barriers to dispersal that would have otherwise gone unrec- one site in Tennessee. ognized (e.g., Mackenzie et al. 2004, Zardi et al. 2007), and even from random sorting of neutral genetic markers across MOLECULAR METHODS geography (Irwin 2002). Overall, North American birds show We extracted total genomic DNA from blood samples by using a high degree of taxon-specific variation in phylogeographic DNeasy Tissue Kits (Qiagen,
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