Comparative Phylogeography of Some Aridland Bird Species1

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Comparative Phylogeography of Some Aridland Bird Species1 The Condor 103:1±10 q The Cooper Ornithological Society 2001 COMPARATIVE PHYLOGEOGRAPHY OF SOME ARIDLAND BIRD SPECIES1 ROBERT M. ZINK2,ANN E. KESSEN,THERESA V. L INE AND RACHELLE C. BLACKWELL-RAGO J. F. Bell Museum, 100 Ecology Building, University of Minnesota, St. Paul, MN 55108 Abstract. We compared mitochondrial DNA sequences for six species distributed across the aridlands of North America to document phylogeographic patterns and assess levels of congru- ence. The Curve-billed Thrasher (Toxostoma curvirostre) and Canyon Towhee (Pipilo fuscus) show genetic divisions between the Sonoran and Chihuahuan Deserts, whereas the Cactus Wren (Campylorhynchus brunneicapillus), Black-tailed Gnatcatcher (Polioptila melanura), and Verdin (Auriparus ¯aviceps) do not. Most likely, species without phylogeographic structure only recently colonized their entire current range. Therefore, although these species are today part of a wide- spread avifauna, species' distributions were historically different from today. In Baja California, the Cactus Wren and the Verdin show phylogeographic breaks at 288±308N, consistent with a division previously described in the LeConte's Thrasher (Toxostoma lecontei) and in some mem- bers of the herpetofauna. These genetic divisions were likely caused by isolation resulting from a mid-peninsular seaway that existed one million years ago. Hence, these species appear to have been broadly sympatric for at least one million years. In contrast, the California Gnatcatcher (Polioptila californica) lacks such a phylogeographic division, and apparently only recently expanded into the northern part of its current range. Thus, not all species in Baja California have had similar histories, although further sampling might reveal a general pattern. Comparative phylogeography therefore provides an indirect method of evaluating the long-term stability of faunas via assessment of levels of phylogeographic congruence, and can show whether particular species are likely to have had a long period of co-association. Key words: Black-tailed Gnatcatcher, Cactus Wren, Canyon Towhee, Curve-billed Thrasher, mitochondrial DNA, phylogeography, Verdin. Resumen. Comparamos secuencias de ADN mitocondrial de seis especies distribuidas a traveÂs de las zonas aÂridas de NorteameÂrica para documentar los patrones ®logeogra®cos y valorar los niveles de congruencia. El cuitlacoche piquicurvo (Toxostoma curvirostre) y el rascador arroyero (Pipilo fuscus) muestran divisiones geneÂticas entre los desiertos de Sonora y Chihuahua, mientras que la matraca deseÂrtica (Campylorhynchus brunneicapillus), la perlita colinegra (Po- lioptila melanura) y el baloncillo (Auriparus ¯aviceps) no lo hacen. Probablemente, las especies sin estructura ®logeogra®ca han colonizado recientemente su actual aÂrea de distribucioÂn. Por lo tanto, aunque estas especies actualmente forman parte de una avifauna muy ampliamente distri- buida, su distribucioÂn fue histoÂricamente diferente a la actual. En Baja California, la matraca deseÂrtica y el baloncillo muestran interrupciones ®logeogra®cas a los 288±308N, consistente con la divisioÂn previa descrita en el cuitlacoche paÂlido (Toxostoma lecontei) y algunos miembros de la herpetofauna. Estas divisiones geneÂticas fueron aparentemente causadas por el aislamiento resultado de un brazo marino que existio hace un milloÂn de anÄos en la parte media de la PenõÂnsula. De ahõ que estas especies parecen haber sido simpaÂtricas por al menos un milloÂn de anÄos. En contraste, la perlita californiana (Polioptila californica) carece de tal divisioÂn ®logeo- gra®ca, y aparentemente soÂlo recientemente se ha expandido hacia la parte norte de su distri- bucioÂn actual. De esta manera, no todas las especies en Baja California han tenido historias similares, aunque futuros muestreos podrõÂan revelar un patroÂn general. La ®logeografõÂa compa- rada, por lo tanto, provee un meÂtodo indirecto de evaluacioÂn de la estabilidad prolongada de faunas a traveÂs de la valoracioÂn de los niveles de congruencia ®logeogra®ca y puede mostrar que especies en particular pudieran haber tenido un largo periodo de co-asociacioÂn. INTRODUCTION se 1994). Ideally, individuals are sampled from Inferences about the history of populations can throughout a species' range, and a molecular be derived from phylogeographic analyses (Avi- marker such as mitochondrial DNA (mtDNA) is assayed. Phylogenetic analysis of individuals' mtDNA haplotypes produces a tree, which can 1 Received 9 March 2000. Accepted 2 October 2000. be superimposed on the species' geographic dis- 2 E-mail: [email protected] tribution to show whether the history of the pop- [1] 2 ROBERT M. ZINK ET AL. ulations has been one of isolation and diver- gence, high levels of gene ¯ow, or some com- bination. Analyses using coalescence theory per- mit additional inferences about the nature of population increases and magnitude and direc- tion of gene ¯ow. Extending phylogeographic analyses to sets of broadly sympatric species comprises compara- tive phylogeography (Bermingham and Avise 1986, Zink 1996). In theory, species that are part of a modern widespread fauna should have been affected by the same isolating barriers and ought to show similar phylogeographic patterns (Zink 1996). Hence, comparisons of species' phylo- geographic patterns leads to inferences about the FIGURE 1. Map showing general locations of sam- historical stability of the current avifauna. For pling sites (see GenBank accessions for precise local- example, Zink et al. (1997) showed that an iso- ities). Locality codes: PV (Palos Verde peninsula), LS lated population of LeConte's Thrasher (Toxos- (Laguna Salada), VT (Valle de Trinidad), SM (Ejido San Matias), CL (Camalu), SF (San Felipe), MSF (Mi- toma lecontei) in west-central Baja California sion San Fernando), ER (El Rosarito), SI (San Igna- possessed a reciprocally monophyletic set of cio), SR (Santa Rosalia), VI (Villa Insurgentes), LP mtDNA haplotypes relative to haplotypes in the (La Paz), TS (Todos Santos), SA (Santa Anita), CA rest of the range. That is, there was a phylogeo- (Salton Sea), AZ (near Tucson), NM (southern New Mexico), TX (near San Antonio), SO (Sonora near Te- graphic break at 288±308N corresponding to a coripa), CH (Chihuahua, west of city of Chihuahua), mtDNA distance of 3.5%. In contrast, a similar DU (Durango, north of city of Durango), ZA (Zaca- mtDNA survey (Zink et al. 2000a) of the Cali- tecas), CO (Coahuila, north of Saltillo), SLP (San Luis fornia Gnatcatcher (Polioptila californica) found Potosi, Rio Verde), AG (Aguascaliente), MX (Mexico no evidence of a phylogeographic split in Baja City). California or anywhere in the range. Coales- cence analyses (Zink et al. 2000a) suggested that fornia Gnatcatcher (Zink et al. 2000a). Because the California Gnatcatcher has recently expand- not all species occur in Baja California, our ed its range northward and colonized the area comparisons include two regions: Baja Califor- presently inhabited by the northernmost of the nia, and the Chihuahuan plus Sonoran Deserts. two historically isolated groups of LeConte's Our goals were to search for major phylogeo- Thrasher. Therefore, two species in the modern graphic divisions and, if they existed, assess avifauna that presently occupy parts of the same whether they were congruent. Additionally, area have had different histories. The LeConte's where sample sizes permitted, we attempted to Thrasher experienced a major episode of isola- infer aspects of recent population history from tion and divergence, whereas the California analyses based in coalescence theory. Gnatcatcher underwent recent range expansion to achieve its current distribution. Studies of METHODS more species are needed to assess whether either Sampling localities (Fig. 1) encompass most of of these histories is typical. the arid regions of North America as de®ned by In this paper we compare species broadly dis- Hubbard (1973); locality information is given in tributed across the aridlands of North America GenBank accessions (see Results). We attempt- (Hubbard 1973), including Baja California. We ed to obtain enough samples to represent large combine new mtDNA sequence information for fractions of each species' range. Voucher spec- the Cactus Wren (Campylorhynchus brunneica- imens are housed at the Bell Museum of Natural pillus), Black-tailed Gnatcatcher (Polioptila me- History, University of Minnesota; American lanura), Canyon Towhee (Pipilo fuscus), and Museum of Natural History, New York; Muse- Verdin (Auriparus ¯aviceps) with that available um of Natural Science, Louisiana State Univer- for the LeConte's Thrasher (Zink et al. 1997), sity; and the Universidad Autonoma Nacional de Curve-billed Thrasher (Toxostoma curvirostre, MeÂxico. Zink and Blackwell-Rago 2000) and the Cali- Template DNA was extracted using standard EVOLUTION OF ARIDLAND BIRDS 3 phenol chloroform (Hillis et al. 1996) and Che- cludes information on both the number of hap- lex/Proteinase K protocols (Ellegren 1992, Zink lotypes and their relative differentiation, and has and Blackwell 1996). For many specimens, we been used to reconstruct the spatial history of used puri®ed mtDNA; hence, we are con®dent range expansion in other birds (Merila et al. that we analyzed authentic mitochondrial se- 1996). Tajima's D measures departures from se- quences and not nuclear copies (Zhang and He- lective neutrality, and Fst is a measure of the witt 1996). We performed PCR using the follow- amount of variance distributed among popula- ing
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