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Multilocus Phylogeny of the Avian Family Alaudidae (Larks) Reveals Complex Morphological Evolution, Non-Monophyletic Genera and Hidden Species Diversity

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Multilocus Phylogeny of the Avian Family Alaudidae (Larks) Reveals Complex Morphological Evolution, Non-Monophyletic Genera and Hidden Species Diversity See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/241692441 Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic... Article in Molecular Phylogenetics and Evolution · June 2013 DOI: 10.1016/j.ympev.2013.06.005 · Source: PubMed CITATIONS READS 15 430 10 authors, including: Urban Olsson Frederick Keith Barker University of Gothenburg University of Minnesota Twin Cities 152 PUBLICATIONS 1,813 CITATIONS 181 PUBLICATIONS 3,373 CITATIONS SEE PROFILE SEE PROFILE Aleem Ahmed Khan Peter G Ryan Bahauddin Zakariya University Percy FitzPatrick Institute of African Ornithol… 67 PUBLICATIONS 1,249 CITATIONS 431 PUBLICATIONS 8,138 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Foraging ecology of African Penguins and Cape Cormorants at Stony Point and Dyer Island - developing tools to inform marine ecosystem management View project PATHOCENE: Prehistoric pathogen research initiative: Microscopic and genomic analysis of disease vectors and pathogens from southern African Pleistocene archaeological contexts View project All content following this page was uploaded by Aleem Ahmed Khan on 30 August 2017. The user has requested enhancement of the downloaded file. YMPEV 4625 No. of Pages 14, Model 5G 25 June 2013 Molecular Phylogenetics and Evolution xxx (2013) xxx–xxx 1 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev 6 7 3 Multilocus phylogeny of the avian family Alaudidae (larks) reveals 4 complex morphological evolution, non-monophyletic genera and hidden 5 species diversity a,b,c,⇑ c d e f 8 Q1 Per Alström , Keith N. Barnes , Urban Olsson , F. Keith Barker , Paulette Bloomer , g g h i 9 Aleem Ahmed Khan , Masood Ahmed Qureshi , Alban Guillaumet , Pierre-André Crochet , c 10 Peter G. Ryan 11 a Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, PR China 12 b Swedish Species Information Centre, Swedish University of Agricultural Sciences, Box 7007, SE-750 07 Uppsala, Sweden 13 c Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch 7700, South Africa 14 d Systematics and Biodiversity, Gothenburg University, Department of Zoology, Box 463, SE-405 30 Göteborg, Sweden 15 e Bell Museum of Natural History, Department of Ecology, Evolution and Behavior, University of Minnesota, 1987 Upper Buford Circle, St. Paul, MN 55108, USA 16 f Percy FitzPatrick Institute, Centre of Excellence, Department of Genetics, University of Pretoria, Hatfield 0083, South Africa 17 g Institute of Pure & Applied Biology, Bahauddin Zakariya University, 60800 Multan, Pakistan 18 h Department of Biology, Trent University, DNA Building, Peterborough, ON K9J 7B8, Canada 19 i CEFE/CNRS, Campus du CNRS, 1919, Route de Mende, 34293 Montpellier, France 2120 22 article info abstract 3624 25 Article history: The Alaudidae (larks) is a large family of songbirds in the superfamily Sylvioidea. Larks are cosmopolitan, 37 26 Received 1 November 2012 although species-level diversity is by far largest in Africa, followed by Eurasia, whereas Australasia and 38 27 Revised 6 June 2013 the New World have only one species each. The present study is the first comprehensive phylogeny of 39 28 Accepted 7 June 2013 the Alaudidae. It includes 83.5% of all species and representatives from all recognised genera, and was 40 29 Available online xxxx based on two mitochondrial and three nuclear loci (in total 6.4 kbp, although not all loci were available 41 for all species). In addition, a larger sample, comprising several subspecies of some polytypic species was 42 30 Keywords: analysed for one of the mitochondrial loci. There was generally good agreement in trees inferred from 43 31 Phylogeny different loci, although some strongly supported incongruences were noted. The tree based on the 44 32 Taxonomy 33 Morphological evolution concatenated multilocus data was overall well resolved and well supported by the data. We stress the 45 34 Nodal support importance of performing single gene as well as combined data analyses, as the latter may obscure 46 35 significant incongruence behind strong nodal support values. The multilocus tree revealed many unpre- 47 dicted relationships, including some non-monophyletic genera (Calandrella, Mirafra, Melanocorypha, 48 Spizocorys). The tree based on the extended mitochondrial data set revealed several unexpected deep 49 divergences between taxa presently treated as conspecific (e.g. within Ammomanes cinctura, Ammomanes 50 deserti, Calandrella brachydactyla, Eremophila alpestris), as well as some shallow splits between currently 51 recognised species (e.g. Certhilauda brevirostris–C. semitorquata–C. curvirostris; Calendulauda barlowi–C. 52 erythrochlamys; Mirafra cantillans–M. javanica). Based on our results, we propose a revised generic clas- 53 sification, and comment on some species limits. We also comment on the extraordinary morphological 54 adaptability in larks, which has resulted in numerous examples of parallel evolution (e.g. in Melanocory- 55 pha mongolica and M. leucoptera [latter here proposed to be moved to Alauda]; Ammomanopsis grayi and 56 Ammomanes cinctura/deserti; Chersophilus duponti and Certhilauda spp.; Mirafra hova [here proposed to be 57 moved to Eremopterix] vs. several other Mirafra spp.), as well as both highly conserved plumages (e.g. 58 within Mirafra) and strongly divergent lineages (e.g. Mirafra hova vs. Eremopterix spp.; Calandrella cinerea 59 complex vs. Eremophila spp.; Eremalauda dunni vs. Chersophilus duponti; Melanocorypha mongolica and 60 male M. yeltoniensis vs. other Melanocorypha spp. and female M. yeltoniensis). Sexual plumage dimor- 61 phism has evolved multiple times. Few groups of birds show the same level of disagreement between 62 taxonomy based on morphology and phylogenetic relationships as inferred from DNA sequences. 63 Ó 2013 Elsevier Inc. All rights reserved. 6564 66 1. Introduction 67 ⇑ Corresponding author at: Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing 100101, PR China. The family Alaudidae, larks, comprises 97 species in 21 genera 68 E-mail address: [email protected] (P. Alström). (Gill and Donsker, 2012; Spottiswoode et al., in press), including 69 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.06.005 Please cite this article in press as: Alström, P., et al. Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic genera and hidden species diversity. Mol. Phylogenet. Evol. (2013), http://dx.doi.org/10.1016/j.ympev.2013.06.005 YMPEV 4625 No. of Pages 14, Model 5G 25 June 2013 2 P. Alström et al. / Molecular Phylogenetics and Evolution xxx (2013) xxx–xxx 70 the Eurasian Skylark Alauda arvensis (‘‘the lark’’), which is familiar 1966, 1980; Dean et al., 1992; de Juana et al., 2004; Dickinson, 135 71 to many Europeans because of its widespread occurrence in agri- 2003; Harrison, 1966; Macdonald, 1952a,b, 1953; Maclean, 1969; 136 72 cultural land, local abundance, and beautiful song. Many other spe- Meinertzhagen, 1951; Pätzold, 2003; Peters, 1960; Roberts, 1940; 137 73 cies of larks are well known for similar reasons. Larks are found on Vaurie, 1951; Verheyen, 1958; Wolters, 1979). Certain genera, 138 74 six continents, but the family’s distribution and diversity is highly notably Mirafra, have acted as ‘‘dumping grounds’’, while several 139 75 skewed. In terms of current distribution and diversity, the Alaudi- monotypic genera (e.g. Pseudalaemon, Lullula, Ramphocoris), and 140 76 dae is primarily an African and secondarily a Eurasian family. Sev- enigmatic species (e.g. Eremalauda dunni, Alauda razae) and genera 141 77 enty-eight species occur in Africa, with 60 endemic to sub-Saharan (e.g. Alaemon, Chersomanes) have defied consistent placement. Lark 142 78 Africa. Eurasia has 37 species, with one, Mirafra javanica, extending taxonomy has received much attention in Africa (Clancey, 1989; 143 79 its range to Australia, as the only representative of this family on Lawson, 1961; Meinertzhagen, 1951; Winterbottom, 1957), and 144 80 that continent (de Juana et al., 2004; Gill and Donsker, 2012). A sin- Eurasia (Dickinson and Dekker, 2001; Meinertzhagen, 1951; Vau- 145 81 gle widespread species, the Horned Lark Eremophila alpestris, is na- rie, 1951, 1954). Recent studies based on molecular and/or vocal 146 82 tive to the New World as well as much of the Palearctic. All 21 data have revealed considerable hidden diversity and taxonomic 147 83 genera are represented in Africa, with 13 in Eurasia and one each confusion in some taxa (Alström, 1998; Ryan et al., 1998; Ryan 148 84 in Australasia and the New World (de Juana et al., 2004; Gill and and Bloomer, 1999; Guillaumet et al., 2005, 2006, 2008), and it 149 85 Donsker, 2012). In Africa, lark species richness is greatest in seems likely that the total number of recognised lark species is 150 86 semi-arid and arid regions (Dean and Hockey, 1989). There are underestimated. 151 87 two primary centres of endemism, one in the north-east arid zone Previously, only one molecular phylogeny has been published, 152 88 (Kenya, Ethiopia and Somalia), where 23 of the 34 species are en- based on mitochondrial sequences from a small number of mostly 153 89 demic or near-endemic, and another one in the south-west arid African species (Tieleman et al., 2002). The present study is the first 154 90 zone (South Africa, Namibia and Botswana), where 26 of the 31 comprehensive phylogeny of the Alaudidae (although part of the 155 91 species are endemic or near-endemic (de Juana et al., 2004). data for the African and some of the Western Palearctic species 156 92 Most lark species share a similar plumage pattern: brownish or have been analysed in an unpublished PhD thesis; Barnes, 2007).
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