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Conservation Genetics of the Black-Capped Vireo (Vireo Atricapilla)

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Conservation Genetics of the Black-Capped Vireo (Vireo Atricapilla) FINAL REPORT As Required by THE ENDANGERED SPECIES PROGRAM TEXAS Grant No. E - 57 Endangered and Threatened Species Conservation Conservation Genetics of the Black-capped Vireo (Vireo atricapilla) Prepared by: Bob Zink and Andy Jones Robert Cook Executive Director Matt Wagner Mike Berger Program Director, Wildlife Diversity Division Director, Wildlife December 20, 2006 FINAL REPORT STATE: ____Texas_______________ GRANT NUMBER: ___E - 57____________ GRANT TITLE: Conservation Genetics of the Black-capped Vireo (Vireo atricapilla) REPORTING PERIOD: ____1 October 2004 to 30 September 2006 OBJECTIVE(S): 1) To determine from mitochondrial DNA analysis whether the Black-capped Vireo consists of more than one Distinct Population Segment (DPS), 2) To assess variability and gene flow among populations, or DPSs, and 3) To assess spatio-temporal patterns of colonization in Mexico, Texas, and Oklahoma Significant Deviations: Samples of Dwarf Vireo (V. nelsoni) were not obtained; no recent specimens exist in museums and none were captured for this study. This did not affect results (please see Attachment A). Summary Of Progress: Please see Attachment A. Location: Several sites in Oklahoma, Texas, and Mexico. Cost: __________________________________________________________________ Prepared by: ___Craig Farquhar______ Date: December 20, 2006 Approved by: ______________________________ Date:_______________________ Neil (Nick) E. Carter 2 3 1 ATTACHMENT A 2 FINAL REPORT FOR E-57 3 PI Robert M. Zink, University of Minnesota 4 19 December 2006 5 6 Significant Deviation 7 We were unable to locate and tissues of Dwarf Vireo (V. nelsoni) which has been 8 proposed as the sister taxon of Black-capped Vireo ("probably conspecific" Phillips 1991, 9 p. 195); no tissues are known to exist in any natural history museum (A. T. Peterson, 10 pers. comm.). However, this does not affect the results of this study because there was no 11 phylogenetic structure to the haplotype tree; hence, rooting could not change the outcome 12 or interpretation. 13 14 CONSERVATION GENETICS OF THE BLACK-CAPPED VIREO 15 ABSTRACT 16 The Black-capped Vireo (Vireo atricapilla) breeds in habitat fragments in 17 Oklahoma, Texas, Coahuila, Nuevo Leon, and Tamaulipas, and is endangered throughout 18 its range due to habitat destruction and fragmentation; population declines are accelerated 19 by cowbird parasitism. We used mitochondrial DNA (mtDNA) sequences from the ND2 20 gene to examine population structure. Feather samples from 108 individuals were taken, 21 covering all five states where this bird occurs. Despite the geographic isolation of 22 existing populations, no phylogeographic breaks were found. Sequence divergence was 23 quite low (<1%) and few haplotypes were found, as expected for a species with a small 3 4 24 global distribution and no described subspecific variation. Mismatch distributions were 25 unimodal, suggesting a recent population bottleneck, likely during the Pleistocene. This 26 pattern of recent population growth is repeated when analyzing southern and northern 27 samples separately, precluding inferences of Pleistocene movements. We suggest that 28 recent isolation of populations is of insufficient duration and intensity to cause genetic 29 differentiation in neutral markers in this species. Lack of geographic structure in an 30 endangered bird in North America is a fairly common finding in the literature; we discuss 31 the implications of this result to conservation and management priorities. 32 33 Key words: Endangered Species Act, mtDNA, phylogeography 34 4 5 35 INTRODUCTION 36 The Black-capped Vireo (Vireo atricapillus) is a small passerine that breeds in 37 scrubby habitats in the states of Oklahoma and Texas in the United States, and Coahuila, 38 Nuevo Leon, and Tamaulipas in Mexico. These birds migrate southwest to the lowlands 39 along the Pacific slope of Mexico in winter. This species was formerly more widespread, 40 occurring regularly in Nebraska and Kansas until the early 1900s. Black-capped Vireos 41 have been widely studied (e.g. Grzybowski 1995). Attention has been focused on the 42 Black-capped Vireo because it displays several interesting features. This species has an 43 exceedingly large repertoire of song syllables, high even among the Vireonidae. Further, 44 Black-capped Vireos show sexual dichromatism and delayed plumage maturation 45 (second-year males are visibly distinct from after-second-year males); both of these 46 characteristics are unusual among the Vireonidae (Grzybowski 1995). 47 Black-capped Vireo populations have declined recently due primarily to habitat 48 loss and cowbird parasitism. As a result of this decline this species is listed as 49 endangered by the United States Fish and Wildlife Service. Their specific habitat is 50 dominated by oaks or junipers and is declining at a fairly high rate; this habitat is also 51 home to the Federally endangered (in the United States) Golden-cheeked Warbler 52 (Dendroica chrysoparia). Management efforts have focused on minimizing effects from 53 the cowbirds that parasitize them, and establishment and maintenance of appropriate 54 habitat (Grzybowski 1995). 55 Despite the attention paid to this species for various aspects of its natural history, 56 its evolutionary history is not well known. Conservation efforts should be informed with 57 genetic data whenever possible, and for a species that exists in fragmented populations 5 6 58 documentation of cryptic lineages or other population subdivision is important when 59 prioritizing land conservation and management efforts. The Black-capped Vireo was the 60 subject of an allozyme analysis (Fazio et al. 1992); from limited sampling (three Texas 61 populations and one Oklahoma population) they found significant population 62 differentiation. However, their data included two loci that were under selection, biasing 63 their conclusions. 64 In this paper we include samples from all states where Black-capped Vireos are 65 extant, present findings on population differentiation in this species, and discuss how 66 these findings are relevant to management goals in endangered species. 67 METHODS 68 Sampling 69 Feathers were collected from live birds in the states of Oklahoma and Texas 70 (United States of America) and Coahuila, Tamaulipas, and Nuevo Leon (Mexico) during 71 the breeding seasons of 2002-2005. Exact locations are detailed in Appendix 1. Permits 72 for feather sampling are detailed in the Acknowledgments section. Voucher specimens 73 were not obtained due to conservation issues across the range of this taxon. The 74 following outgroup sequences were taken from Genbank: Vireo olivaceus (AY136614), 75 V. solitarius (AY030137), V. gilvus (AY030135), V. latimeri (AF281020), V. leucophrys 76 (AY030134), and V. plumbeus (AY030136). We were unable to locate and tissues of 77 Dwarf Vireo (V. nelsoni) which has been proposed as the sister taxon of Black-capped 78 Vireo ("probably conspecific" Phillips 1991, p. 195); no tissues are known to exist in any 79 natural history museum (A. T. Peterson, pers. comm.). 80 Laboratory Techniques 6 7 81 Feathers were sent to RMZ's laboratory at the University of Minnesota. Two to 82 three contour feathers (or, occasionally only a single rectrix was available) were then 83 extracted using a Qiagen DNeasy Tissue Extraction kit (Qiagen Inc., Valencia, 84 California), following manufacturer's protocols except that the initial addition of Buffer 85 ATL and Proteinase K was supplemented with 30 uL of DTT (Dithiothreitol) and 86 incubated at 55° C for 24h. Extracts were amplified with polymerase chain reactions 87 (PCR) with the following conditions: 15m at 94°, 35 cycles of [45s at 94°, 45s at 50°, 88 and 90s at 72°], 5m at 72°, and then held at 4°. The mitochondrial ND2 (NADH 89 dehydrogenase subunit 2) gene was amplified in all individuals in either two or three 90 pieces, depending on how degraded the DNA was. Primers are listed in Table 1; three 91 were designed by MCW for this study. These PCR products were then cleaned with a 92 QIAquick PCR cleaning kit, and submitted in 6 uL sequencing reactions to the 93 BioMedical Genomics Center at the University of Minnesota. Sequences were aligned 94 with Sequencher 4.1.1 (Gene Codes Corp., Ann Arbor, Michigan). Mitochondrial origin 95 was confirmed in Sequencher by inspecting for unexpected stop codons and insertions or 96 deletions. 97 Population Genetic Analyses 98 Sequences were reduced to unique haplotypes, and a neighbor-joining tree 99 produced to depict population subdivision, using the program DnaSP 4.10 (Rozas et al. 100 2003). Sequences from all individuals were analyzed for patterns of population size 101 changes over time using mismatch distributions (Rogers and Harpending 1992). Samples 102 were pooled for mismatch analyses into three groups: Oklahoma (10 individuals), Texas 103 (80), and Mexico (16), with significance judged by Tajima's D (Tajima 1989) and Fu's Fs 7 8 104 (Fu 1997). Sequences with more than 5% missing data were deleted from mismatch 105 analyses. 106 RESULTS 107 We obtained 1041 base pairs, representing the entire mitochondrial ND2 gene 108 from 108 sampled Black-capped Vireos. The 39 variable sites (22 parsimony 109 informative) resolved 27 unique haplotypes, with a haplotype diversity of 0.866. No stop 110 codons or indels were observed. 111 A neighbor-joining phylogeny of haplotypes demonstrated no major phylogenetic 112 breaks, and no visible geographic structuring within the topology (Figure 1). Further, no 113 haplotypes
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