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Genetic and Morphological Variation of the Sooty-Capped Bush Tanager (Chlorospingus Pileatus), a Highland Endemic Species from Costa Rica and Western Panama

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Genetic and Morphological Variation of the Sooty-Capped Bush Tanager (Chlorospingus Pileatus), a Highland Endemic Species from Costa Rica and Western Panama The Wilson Journal of Ornithology 122(2):279–287, 2010 GENETIC AND MORPHOLOGICAL VARIATION OF THE SOOTY-CAPPED BUSH TANAGER (CHLOROSPINGUS PILEATUS), A HIGHLAND ENDEMIC SPECIES FROM COSTA RICA AND WESTERN PANAMA TANIA CHAVARRI´A-PIZARRO,1,2 GUSTAVO GUTIE´ RREZ-ESPELETA,1 ERIC J. FUCHS,1 AND GILBERT BARRANTES1 ABSTRACT.—We examined the effect of geographic isolation on morphology, genetic structure, and abundance of the Sooty-capped Bush Tanager (Chlorospingus pileatus), an endemic species restricted to highlands of Costa Rica and western Panama. Abundance and morphology were measured at five study sites and genetic variation was calculated from three microsatellite loci. We expected geographic discontinuities in this species’ distribution to have an effect on its morphology and genetic structure. Genetic variation was higher within than between populations with no effect of geographic barriers on population genetic divergence in this species, indicating gene flow is high between populations. Unique alleles were detected in each population and Fst values increased with geographic distance between populations. Some morphological traits differed between populations, which may be caused by adaptation to different selective pressures in each population. Molecular data did not differ between the two color morphs that coexist in two isolated populations, which were considered different species. Received 16 July 2009. Accepted 22 November 2009. Highland endemic avian species in the moun- birds (Powell 1985, Stiles and Skutch 1989). A tains of Costa Rica and western Panama currently grayish-green morph of Sooty-capped Bush Tan- show naturally isolated and discontinuous distri- ager (lighter morph) coexists on two high butions, reflecting their confinement to mountain volcanoes (Irazu´ and Turrialba) of central Costa peaks and their isolation from other highland Rica with the darker and more widely distributed regions in the Neotropics (Stiles 1983; Barrantes morph. The grayish-green morph was first con- 2000, 2009). Morphological and molecular diver- sidered a different species (Zeledon’s Chloro- gence documented for some of these endemic spingus, Chlorospingus zeldoni) by Ridgway highland species in Costa Rica correspond to this (1905), and Eisenmann (1955) and Slud (1964) natural isolation (Stiles 1983, Barrantes 2000, continued C. zeledoni as a different species. Barrantes and Sa´nchez 2000). For example, However, Carriker (1910) suggested that C. isolated populations of the Volcano Hummingbird zeledoni was a color morph of Sooty-capped Bush (Selasphorus flammula) and Fiery-throated Hum- Tanager. Johnson and Brush (1972) analyzed the mingbird (Panterpe insignis) differ in coloration structure and pigment composition of feathers of and morphological dimensions (Stiles 1983, both taxa and concluded C. zeledoni was a morph 1985). Similarly, geographic barriers have affect- of Sooty-capped Bush Tanager. However, no ed the genetic and morphological divergence further investigations have been conducted to test among populations of the Black-and-yellow this hypothesis (e.g., using molecular data). Phainoptila (Phainoptila melanoxantha)(Bar- We used molecular data to analyze the effect of rantes 2000, Barrantes and Sa´nchez 2000). isolation (i.e., distance and barriers between The Sooty-capped Bush Tanager (Chlorospin- populations) on genetic structure and morphology gus pileatus) is endemic to the highlands of of the Sooty-capped Bush Tanager. We specifi- Costa Rica and western Panama. This species cally hypothesized that small populations isolated is naturally restricted to the summit of high by effective geographical barriers have a notable mountains and primarily inhabits forest edges and reduction in genetic variation. In addition, we open areas in the cloud forest and pa´ramo. Sooty- searched for genetic differences between the two capped Bush Tanagers forage in flocks of 5–20 color morphs on Irazu´ volcano. To our knowl- individuals, often accompanied by other small edge, this is the first fine-scale genetic analysis, using microsatellites of an avian species endemic to the isolated highland regions of Costa Rica and 1 Escuela de Biologı´a, Ciudad Universitaria Rodrigo Facio, Universidad de Costa Rica, San Jose´, Costa Rica. western Panama´. Most species in this hotspot of 2 Corresponding author; diversity and endemism are restricted to a reduced e-mail: [email protected] portion of the highland forests and have low 279 The Wilson Journal of Ornithology wils-122-02-08.3d 12/3/10 17:12:01 279 Cust # 09-111 280 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 2, June 2010 FIG. 1. Sampling localities in Costa Rican mountain ranges: Talamanca, Central Volcanic, and Tilara´n. Locations of Monterverde, Irazu´, and Cerro de la Muerte are indicated by black arrows. abundance (Jankowski and Rabenold 2007, Bar- of different magnitude such as watersheds and rantes 2009). mountain passes (Fig. 1). We censused birds 4–7 times in each of the METHODS sites to account for possible fluctuations due to Field Data Collection.—We conducted field climatic conditions. Censuses started at 0545 hrs work in highland forests of three Costa Rican and all individuals heard and seen within 25 m of mountain ranges: Talamanca Mountain Range, each side of the transect were recorded. Length of Central Mountain Range, and Tilara´n Mountain transects varied from 1.9 to 3.0 km among sites. Range (Fig. 1) from July 2003 through December Thus, abundance was expressed as individuals/km 2005. Censuses and tissue collections were to allow comparison among sites. We used conducted at five different sites: Monteverde abundance categories based on mean values (10u 199 N, 84u 479 W; 1,550 m asl) in the across censuses for each site. Categories were Tilara´n Mountain Range; Poa´s Volcano definedasverycommon(.20 individuals (10u 119 N, 84u 139 W; 2,700 m asl), Irazu´ Vol- observed/census), common (10–19 individuals/ cano (09u 599 N, 83u 529 W; 3,200 m asl), and census), uncommon (5–9 individuals/census), and Barva Volcano (10u 089 N, 84u 069 W; 2,800 m rare (,5 individuals/census). We calculated the asl) in the Central Mountain Range; and Macizo area of the potential available habitat for Sooty- Cerro de la Muerte (09u 339 N, 83u 439 W; capped Bush Tanagers on each mountain range 3,100 m asl) in the Talamanca Mountain Range. using Geographical Information Software (Arc- Mountain ranges and field sites within mountain View GIS 3.3) on a digital elevation map of ranges are separated by geographic discontinuities Costa Rica (1:200,000; Lambert conformal con- The Wilson Journal of Ornithology wils-122-02-08.3d 12/3/10 17:12:26 280 Cust # 09-111 Chavarrı´a-Pizarro et al. N GENETICS AND MORPHOLOGY OF SOOTY-CAPPED BUSH TANAGER 281 ical projection) (Fig. 1). This area was estimated each locus as described in Hanotte et al. (1994). from the lower limit of the altitudinal distribution Genotypes were obtained using an automatic of Sooty-capped Bush Tanager to the summit of sequencer (ABI Prism 310, Applied Biosystems, the mountains in each mountain range. Palo Alto, CA, USA). Alleles were sized using the We set 5–8 mist nets (12 m long) during each program GENOTYPER (3.7NT, Applied Biosys- visit to a study site. The following measurements tems, Palo Alto, CA, USA). were taken for each individual captured: body We counted the number of alleles per locus and mass, length of the bill from distal end of nares to calculated their frequencies in each population. the bill tip, width of the bill at front of nares, We tested deviations of these alleles from Hardy- length of the culmen from the front of the skull to Weinberg equilibrium with a Chi-square test the bill tip, tarsus from the tibiotarsus joint to the using the program GENALEX 6 (Peakall and distal end of the tarsometatarsus, flattened wing Smouse 2006); sequential Bonferroni correction cord, and tail length. These morphological traits was applied due to performance of multiple were chosen as they are expected to respond simultaneous tests (Rice 1989). The observed adaptively to ecological differences in habitat (Ho) and expected (He) heterozygosity per locus (Grant 1986, Price and Boag 1987) and were in each population were calculated using program taken by the same person (GB). Birds were ARLEQUI´N Version 3.1 (Schneider et al. 2000, banded (plastic bands) to avoid re-measuring the Excoffier et al. 2005). An analysis of molecular same individuals. Morphological data were first variance (AMOVA) was used to assess population analyzed using a stepwise (forward) discriminant structure with 30,000 permutations to infer function analysis (DFA). This option excludes significance of Fst values (Weir and Cockerham those variables that have no further effect in 1984). AMOVA calculations were conducted explaining the between-population variance. We using ARLEQUI´N Version 3.1 (http://cmpg. used a MANOVA on those variables included in unibe.ch/software/arlequin3). We also checked the DFA. Statistical analyses were performed in all loci for the presence of null alleles (Chakra- Statistica Version 6.0 (StatSoft Inc., Tulsa, OK, borty et al. 1992, Brookfield 1996) using Micro- USA). Checker Version 2.2.3 (University of Hull, Hull, Laboratory Procedures.—DNA was extracted UK; http://www.microchecker.hull.ac.uk/; van from liver tissue of 56 individuals that had been Oosterhout et al. 2004). All loci were tested based obtained in previous years and maintained in the on a dinucleotide repeat motif and 1,000 permu- tissue collection at the Zoology Museum at the tations. University of Costa Rica. We collected blood We further examined population structure and samples from five additional individuals for a admixture using a model-based clustering method total of 61 individuals (14 from Cerro de la as implemented in the Bayesian clustering Muerte, 9 from Irazu´ Volcano, 18 from Barva program STRUCTURE (Pritchard et al. 2000, Volcano, 11 from Poa´s Volcano, and 9 from Falush et al. 2003).
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