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Molecular Evolutionary Relationships in the Avian Genus Anthus (Pipits

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Molecular Evolutionary Relationships in the Avian Genus Anthus (Pipits Molecular Phylogenetics and Evolution Vol. 11, No. 1, February, pp. 84–94, 1999 Article ID mpev.1998.0555, available online at http://www.idealibrary.com on Molecular Evolutionary Relationships in the Avian Genus Anthus (Pipits: Motacillidae) Gary Voelker1 Burke Museum and Department of Zoology, Box 353010, University of Washington, Seattle, Washington 98195 Received December 1, 1997; revised April 8, 1998 habitats, and this diversity along with distributional Nucleotide sequences for 1035 bp of the mitochon- differences have contributed to considerable variation drial cytochrome b gene were used to determine the in a number of life history traits such as migratory molecular evolutionary relationships of species in the behavior, clutch size, and molt pattern (Hall, 1961; cosmopolitan avian genus Anthus. Phylogenetic analy- Clancey, 1990; Voelker, unpublished data). Yet these sis of these mtDNA sequences supported four major differences in life history have received little attention clades within the genus: (1) the small-bodied African from a phylogenetic standpoint. pipits, (2) a largely Palearctic clade, (3) a largely South The striking similarity in morphology and plumage American clade, and (4) an African–Eurasian–Austra- across Anthus has historically been a barrier to resolv- lian clade. Anthus hellmayri, A. correndera, and A. rubescens are shown to be paraphyletic. The possibil- ing relationships within the genus (Ridgway, 1904; ity of paraphyly within A. similis is instead inferred to Hall, 1961; Clancey, 1990), although the similarity has be the discovery of a new species and supported by not precluded the description of numerous subspecies reference to the museum voucher specimen. Sequence (e.g., Hellmayr, 1935; Clancey, 1990 and references divergence suggests a Pliocene/Miocene origin for the therein). Previous works have speculated to a limited genus. Although Anthus cytochrome b is found not to extent on the relationships of a few species (e.g., Hall, be behaving in a clocklike fashion across all taxa, 1961; Clancey, 1990), relying primarily on limited speciation during the Pleistocene epoch can be reason- variation across morphological characters. A good gen- ably inferred for the 66% of sister pairs that are eral description of an Anthus species would be: plum- diverging in a clocklike manner. Base compositions at age color generally brown or some combination of each codon position are similar to those found across a brown, white, and black, with black ventral streaking, growing number of avian lineages. The resulting phylo- a long hindclaw, and weighing between 18 and 30 g. A genetic hypothesis is compared to previous hypoth- few species do have red (e.g., roseatus Rosy Pipit), green eses of Anthus relationships, all of which deal with (e.g., hodgsoni Olive-backed Pipit), or yellow color relationships of a particular species or a particular patches (e.g., crenatus Yellow-tufted Pipit), and the species complex; roughly half of these previous hypoth- body mass of several species are smaller or larger, but eses are supported. ௠ 1999 Academic Press deviations from this general description are limited; thus, reliable means to determine relationships have INTRODUCTION been lacking. Only recently have attempts been made to unravel the phylogenetic relationships of any pipits With approximately 40 species, the avian genus using ecological and molecular differences (Zink et al., Anthus (pipits; Motacillidae) is one of the more speciose 1995; Arctander et al., 1996; Foggo et al., 1997). For genera of oscine passerines. Anthus is globally distrib- example, Nazarenko (1978) defined habitat differences uted, being found on every continent except Antarctica between two species within the ‘‘Water Pipit’’ complex (Sibley and Monroe, 1990). Individual species distribu- (spinoletta (Water Pipit) versus rubescens (American tions range from island endemics (e.g., antarcticus on Pipit)), while Knox (1988) summarized ecological and South Georgia Island) to continental endemics (e.g., behavioral differences supporting recognition of three lineiventris from Africa) to intercontinental migrants species within the same species complex (spinoletta, (e.g., trivialis Eurasia to Africa) to species breeding on rubescens, and petrosus (Rock Pipit)). Using molecular multiple continents (e.g., cervinus in Eurasia and North data, Zink et al. (1995) found a high level of divergence America). There is substantial diversity in breeding between Siberian and American forms of rubescens, Foggo et al. (1997) found large differences between 1 Present address: Barrick Museum, Box 454012, University of populations of novaeseelandiae (‘‘New Zealand’’ Pipit) Nevada Las Vegas, Las Vegas, NV 89154. from New Zealand and nearby islands, and Arctander 84 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. Anthus SYSTEMATICS 85 et al. (1996) addressed the relationships of berthelotii considered here was amplified via PCR as a single unit (which is endemic to the Canary and Madeira Islands). using primers L14841 (Kocher et al., 1989) and H16065 While each of these studies has focused on a limited, (Helm-Bychowski and Cracraft, 1993). These two prim- and in some cases historically contentious, problem of ers were also used in various combinations along with pipit relationships, a more general understanding of L15114, L15299, L15609, H15547 (Edwards et al., pipit systematics is not available. 1991), and H15299 (Hackett, 1996) to amplify DNA In this paper, a segment of mitochondrial cytochrome from several taxa in overlapping segments. For sequenc- b sequence was obtained from 41 Anthus individuals ing, I used the above primers, H15915 (Edwards representing 35 previously recognized species, as well and Wilson, 1990), and the following primers de- as from 5 previously determined outgroup taxa. I use signed specifically from Anthus sequences (numbers these data to generate phylogenies, compare these correspond to 3Ј position in domestic fowl sequence results to previous studies, and provide a framework (Dejardins and Morais, 1990) ): L15086 (5Ј-CTCTG- for future studies of life history strategies and biogeog- TAGCTCACATATGCC-3Ј), L15376 (5Ј-CTAGCAGAAT- raphy across the genus. GAGCCTGAGG-3Ј), L15616 (5Ј-GTTGCCCTAACCC- TATTCTC-3Ј), L15811 (5Ј-CCCCTACTCCA-CACATCA- Ј Ј Ј MATERIALS AND METHODS AA-3 ), H15345 (5 -GTAATAACGGTAGCTCCTCA-3 ), H15671 (5Ј-GGTGTGAAGTTTTCTGGGTC-3Ј), H15853 I sequenced 1035 bp of the mitochondrial cytochrome (5Ј-GGCGGAAGGTTATTGATC-3Ј). I also used L15350 b gene from the 35 Anthus species available in genetic (5Ј-TTACAAACCTATTCTCAGC-3Ј), designed by J. resources collections. This number represents over 80% Klicka. of the species recognized by Sibley and Monroe (1990) Fragments were amplified in 50- or 100-µL PCRs; and includes the recently described longicaudatus amplification conditions were 30 s at 94°C, 30 s at 50°C, (Liversidge, 1996). Multiple specimens from 6 species and 30 s at 72°C, for 35 cycles. The exception was A. were included to provide a preliminary insight into sokokensis which was annealed at 61°C due to multiple species monophyly in cases where the species has a bands at lower temperatures. Amplified products were disjunct breeding range (similis, hellmayri, correndera) prepared as templates for automated sequencing by or has been previously postulated to be polytypic based purification and concentration in up to 22-µL of water on other evidence (spinoletta/rubescens/petrosus com- after three passes through Ultrafree-MC filters (Milli- plex). I did not include the Yellow-breasted Pipit (chlo- pore) by centrifugation. Two microliters of the purified ris), a species which has been placed in the genus and concentrated PCR product were used as a template Hemimacronyx (Cooper, 1985; Voelker and Edwards, in a 10-µL DyeDeoxy Cycle Sequencing reaction (ABI), 1998). As outgroups, I use three members of the genus along with one of the above primers, as per manufactur- Motacilla (confamilial with Anthus). I also include an er’s instructions (Perkin–Elmer). After cycle sequenc- accentor (Prunellidae) and an Old World sparrow (Pas- ing, products were placed on coarse-grained Sephadex seridae) suggested as close relatives of pipits and columns and cleaned of excess nucleotides via centrifu- wagtails based on molecular evidence (Sibley and Ahl- gal passage through the columns (1500 rpm for 7 min). quist, 1981, 1990; Voelker and Edwards, 1998). Both light and heavy strands of the entire 1035-bp fragment considered were sequenced using flourescent Cytochrome b Isolation, Amplification, and Sequencing dye-deoxy chemistry on an ABI Model 373 automated From 1993 to 1995 I collected Anthus specimens in sequencer. Sequences were aligned unambiguously by Russia, Kazakhstan, South Africa, and Argentina. All eye using Genetic Data Environment (developed and specimens were prepared in the field as either skin/wing/ maintained by S. Smith, with compilation of programs tissue or skeleton/wing/tissue combinations; the tissue by various authors; available free from ftp.bio.indiana. samples were preserved in liquid nitrogen. Frozen edu, in molbio/unix/GDE) and have been submitted to tissues were available for all University of Washington GenBank (pending). Burke Museum specimens (except A. roseatus and A. spragueii) (Table 1), and mtDNA was isolated from Phylogenetic Analysis and Test of Molecular Clock these specimens via a cesium chloride gradient (Dowl- All analyses were performed using PAUP* (written ing et al.,
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