Skip to main content

Advertisement

SpringerLink
Log in

Mitochondrial phylogeography of the genus Eremophila confirms underestimated species diversity in the Palearctic

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Phylogeographic analyses of the genus Eremophila (Horned Lark E. alpestris and Temminck’s Lark E. bilopha) were carried out based on the mitochondrial cytochrome b and ND2 genes. Four primary lineages with para-/allopatric distributions were identified: (1) a Qinghai–Tibetan–Himalayan lineage; (2) a North African and Middle Eastern lineage; (3) a northwest African and southeast European/southwest Asian lineage; and (4) a Northern Palearctic and North American lineage. The relationships between these four lineages were poorly resolved. They were estimated to have diverged in the late Pliocene to early Pleistocene, although the dates are uncertain due to topological ambiguity and wide confidence intervals. The sublineages were estimated to have diverged around the Middle Pleistocene (c. 0.8–0.2 mya). A strong signal of population growth and range expansion was observed from the Middle Pleistocene, at least in the North Palearctic subclade (A2). Morphometric analysis of the Eurasian taxa revealed a high degree of overlap among taxa, although E. bilopha and E. a. longirostris stood out from the others. We support a recent suggestion to split E. alpestris into multiple species, although we propose four instead of six species, corresponding to the four primary lineages identified in this study: (1) Himalayan Horned Lark E. longirostris (by priority and on the premise that the genetically unsampled taxon longirostris belongs to this clade); (2) Temminck’s Lark E. bilopha; (3) Mountain Horned Lark E. penicillata; and (4) Common Horned Lark E. alpestris (sensu stricto). Our results illustrate the discrepancy between phylogenetic relationships and phenotype in larks.

Zusammenfassung

Mitochondriale Phylogeografie der Gattung Eremophila bestätigt eine unterschätzte Artenvielfalt in der Paläarktis.

Phylogeografische Untersuchungen der Gattung Eremophila (Ohrenlerche E. alpestris und Hornlerche E. bilopha) auf der Basis der Analyse des mitochondiralen Cytochrom b und ND2 Gene ergaben vier primäre Abstammungslinien mit para-/allopatrischen Verbreitungen: (1) eine Qinghai–Tibetische–Himalaya Linie; (2) eine nordafrikanische und nahöstliche Linie; (3) eine nordostafrikanische und südosteuropäische/südwestasiatische Linie; und (4) eine nordpaläarktische und nordamerikanische Linie. Die Verbindungen zwischen diesen vier Abstammungslinien waren bisher nur unzureichend aufgeklärt. Die Aufspaltung wurde im späten Pliozän bis ins frühe Pleistozän geschätzt, obwohl diese Daten, aufgrund von räumlichen Unsicherheiten und weiten Konfidenzintervallen, als unsicher gelten. Für die Unterstämme wurde eine Aufspaltung im mittleren Pleistozän geschätzt (c. 0.8–0.2 Millionen Jahre). Deutliche Hinweise auf ein Populationswachstum und eine Arealausweitung gibt es im mittleren Pleistozän, zumindest im nordpaläarktischen Unterstamm (A2). Morphometrische Analysen der eurasischen Taxa ergaben einen hohen Überlappungsgrad zwischen den Taxa, obwohl E. bilopha und E. a. longirostris sich von den anderen abheben. Wir unterstützen einen neuen Vorschlag, E. alpestris in mehrere Arten aufzuspalten. Wobei wir vier anstatt sechs Arten vorschlagen, entsprechend der vier, in dieser Studie identifizierten primären Abstammungslinien: (1) Himalaya Ohrenlerche E. longirostris (vorrangig und unter der Voraussetzung, dass das genetisch bisher nicht beprobte Taxon longirostris zu diesem Stamm gehört); (2) Hornlerche E. bilopha; (3) Gebirgsohrenlerche E. penicillata; und (4) Ohrenlerche E. alpestris (sensu stricto). Unsere Ergebnisse verdeutlichen die Diskrepanz zwischen phylogenetischen Beziehungen und dem Phänotyp bei Lerchen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdi H, Williams LJ (2010) Principal component analysis. Inc. WIREs Comp Stat 2:433–459

    Google Scholar 

  • Aliabadian M, Kaboli M, Forschler MI, Nijman V, Chamani A, Tillier A, Zuccon D (2012) Convergent evolution of morphological and ecological traits in the open-habitat chat complex (Aves, Muscicapidae: Saxicolinae). Mol Phylogenet Evol 65:35–45

    PubMed  Google Scholar 

  • Alsop FJ III (2001) Birds of North America, Western region. Smithsonian Handbook. DK Publishing Inc., New York

    Google Scholar 

  • Alström P, Barnes KN, Olsson U, Barker FK, Bloomer P, Khan AA, Qureshi MA, Guillaumet A, Crochet PA, Ryan PG (2013) Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, nonmonophyletic genera and hidden species diversity. Mol Phylogenet Evol 69:1043–1056

    PubMed  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Barnosky AD (2004) Biodiversity response to climatic change in the middle Pleistocene: the Porcupine cave Fauna from Colorado. University of California Press, Berkeley

    Google Scholar 

  • Beason RC (1995) Horned lark (Eremophilia alpestris). In: Poole A, Gill F (eds) The birds of North America No. 195. The academy of natural sciences and The American Ornithologists’ Union, Philadelphia and Washington DC, pp 1–21

  • Bianchi V (1904) Key to the Palaearctic species of larks of the genus Otocorys. Ibis 46:370–372

    Google Scholar 

  • Bobek H (1937) Die rolle der eiszeit in nordwestiran. Z Gletscher 25:130–183

    Google Scholar 

  • Boev Z (2002) Neogene avifauna of Bulgaria. In: Zhou Z, Zhang F (eds) Proceedings of the 5th symposium of the society of avian palaeontology and evolution, Beijing, 01–04.06.2000. Science Press, Beiging, pp 29–40

  • Boev Z (2012) Neogene Larks (Aves: Alaudidae (Vigors, 1825)) from Bulgaria. Acta Zool Bulgar 64:295–318

    Google Scholar 

  • Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537

    PubMed  PubMed Central  Google Scholar 

  • Brito PH (2005) The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in Western Europe. Mol Ecol 14:3077–3094

    CAS  PubMed  Google Scholar 

  • Cheng TH (1987) A synopsis of the Avifauna of China. Beijing, pp 1–1223

  • Clements JF, Schulenberg TS, Iliff MJ, Roberson D, Fredericks TA, Sullivan BL, Wood CL (2018) The eBird/Clements checklist of birds of the world: v2018. http://www.birds.cornell.edu/clementschecklist/download/

  • Cramp S (1988) The Birds of the Western Palearctic, vol V. Oxford University Press, Oxford

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Juana E, Suárez F, Ryan P, Alström P, Donald P (2004) Family Alaudidae (Larks). In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the Birds of the World, vol 9. Lynx Edicions, Barcelona, pp 496–601

    Google Scholar 

  • del Hoyo J, Collar NJ (2016) The HBW–BirdLife International illustrated checklist of the birds of the world, 2: passerines. Lynx Edicions, Barcelona

    Google Scholar 

  • Dickinson E (ed) (2003) The Howard and Moore complete checklist of the birds of the world, 3rd edn. Helm, London

    Google Scholar 

  • Dickinson EC, Christidis L (2014) The Howard and Moore complete checklist of the birds of the world. Aves Press, Eastbourne

    Google Scholar 

  • Donald PF (2004) Horned Lark Eremophila alpestris. In: del Hoyo J, Elliott A, Christie D (eds) Handbook of the birds of the world, Lynx Edicions, vol 9. Barcelona and BirdLife International, Cambridge, p 863

    Google Scholar 

  • Donald PF, Alström P, Engelbrecht D (2017) Possible mechanisms of substrate colour-matching in larks (Alaudidae) and their taxonomic implications. Ibis 159:699–702

    Google Scholar 

  • Drovetski SV (2003) Plio–Pleistocene climatic oscilations, Holarctic biogeography and speciation in an avian subfamily. J Biogeogr 30:1173–1181

    Google Scholar 

  • Drovetski SV, Semenov G, Drovetskaya SS, Fadeev IV, Red’kin YA, Voelker G (2013) Geographic mode of speciation in a mountain specialist avian family endemic to the Palearctic. Ecol Evol 3:1518–1528

    PubMed  PubMed Central  Google Scholar 

  • Drovetski SV, Rakovic M, Semenov G, Fadeev IV, Red’kin YA (2014) Limited Phylogeographic signal in sex-linked and autosomal loci despite geographically, ecologically, and phenotypically concordant structure of mtDNA variation in the Holarctic avian genus Eremophila. PLoS One 9:1–10

    Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    PubMed  PubMed Central  Google Scholar 

  • Fjeldså J, Bowie RCK, Rahbek C (2012) The role of mountain ranges in the diversifcation of birds. Annu Rev Ecol Evol Syst 43:249–265

    Google Scholar 

  • Frenzel B (1973) Climatic fluctuations of the ice age. The Press of Case Western Reserve University, Cleveland and London

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth: hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gill F, Donsker D (2018) IOC world bird list (v 8.1). https://doi.org/10.14344/ioc.ml.8.1

  • Harris DJ, Taylor SD, White EP (2018) Forecasting biodiversity in breeding birds using best practices. PeerJ 6:e4278

    PubMed  PubMed Central  Google Scholar 

  • Hellmayr CE (1929) Birds of the James Simpson–Roosevelts Asiatic expedition. Field Mus Nat Hist Zool 17:27–144

    Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    CAS  PubMed  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc Lond B 359:183–195

    CAS  Google Scholar 

  • Hughes P, Woodward J (2017) Quaternary glaciation in the mediterranean mountains, 1st edn. Geological Society of London, Bath (Special Publications)

  • Khan AA (1999) A New Horned Lark Eremophila alpestris deosaiensis, (subsp. Nov.) from Deosai, Baltistan Pakistan. Pak J Ornith 3:27–33

    Google Scholar 

  • Kirwan GM (2006) Comments on two subspecies of passerine birds recently described from Turkey, Eremophila alpestris kumerloevi and Pyrrhula pyrrhula paphlagoniae, with remarks on geographical variation in related forms of bullfinch from the Balkans and Caucasus. Sandgrouse 28:10–21

    Google Scholar 

  • Klicka J, Zink RM (1999) Pleistocene effects on North American songbird evolution. Proc R Soc Lond B 266:695–700

    Google Scholar 

  • Kozlova EV (1933) The birds of south-west Transbaikalia, northern Mongolia and central Gobi. Ibis 13(3):59–87

    Google Scholar 

  • Krinsley DH (1970) A geomorphological and paleoclimatological study of the playas of Iran. USGS Final Scientific Report, Contract, PROCP, pp 700–800

  • Lanfear R, Calcott B, Ho SY, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    CAS  PubMed  Google Scholar 

  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution formolecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773

    CAS  PubMed  Google Scholar 

  • Lei FM, Qu YH, Song G (2014) Species diversification and phylogeographical patterns of birds in response to the uplift of the Qinghai–Tibet plateau and quaternary glaciations. Curr Zool 60:149–161

    Google Scholar 

  • Lei F, Qu Y, Song G, Alström P, Fjeldså J (2015) The potential drivers in forming avian biodiversity hotspots in the East Himalaya Mountains of Southwest China. Integr Zool 10:171–181

    PubMed  Google Scholar 

  • Lerner HRL, Meyer M, James HF, Hofreiter M, Fleischer RC (2011) Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr Biol 21:1838–1840

    CAS  PubMed  Google Scholar 

  • Li X, Dong F, Lei F, Alström P, Zhang R, Ödeen A, Fjeldså J, Ericson PGP, Zou F, Yang X (2016) Shaped by uneven Pleistocene climate: Mitochondrial phylogeographic pattern and population history of white wagtail Motacilla alba (Aves: Passeriformes). J Avian Biol 47:263–274

    Google Scholar 

  • Liu B, Alström P, Olsson U, Fjeldså J, Quan Q, Roselaar KCS, Saitoh T, Yao C, Hao Y, Wang W, Qu Y, Lei F (2017) Explosive radiation and spatial expansion across the cold environments of the Old World in an avian family. Ecol Evol 7:6346–6357

    PubMed  PubMed Central  Google Scholar 

  • Ludlow F, Kinnear NB (1933) A contribution to the Ornithology of Chinese Turkestan. Ibis 13(3):658–694

    Google Scholar 

  • Mason NA, Unitt P (2018) Rapid phenotypic change in a native bird population following conversion of the Colorado Desert to agriculture. J Avian Biol. https://doi.org/10.1111/jav.01507

    Article  Google Scholar 

  • Mason NA, Title PO, Cicero C, Burns KJ, Bowie RCK (2014) Genetic variation among western populations of the Horned Lark (Eremophila alpestris) indicates recent colonization of the Channel Islands off southern California, mainland-bound dispersal, and postglacial range shifts. Auk 131:162–174

    Google Scholar 

  • Olsson U, Alström P, Ericson PGP, Sundberg P (2005) Non-monophyletic taxa and cryptic species-evidence from a molecular phylogeny of leaf-warblers (Phylloscopus, Aves). Mol Phylogenet Evol 36:261–276

    CAS  PubMed  Google Scholar 

  • Pavlova A, Zink RM, Drovetski SV, Redkin Y, Rohwer S (2003) Phylogeographic patterns in Motacilla flava and Motacilla citreola: species limits and population history. Auk 120:744–758

    Google Scholar 

  • Pereira SL, Baker AJ (2006) A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock. Mol Biol Evol 23:1731–1740

    CAS  PubMed  Google Scholar 

  • Peters JL (1960) Family Alaudidae. In: Mayr E, Greenway JC Jr (eds) Check-list of birds of the world, vol IX. Museum of comparative zoology. Cambridge, Mass, pp 3–80

    Google Scholar 

  • Qu Y, Lei F, Zhang R (2010) Comparative phylogeography of five avian species: implications for Pleistocene evolutionary history in the Qinghai–Tibetan plateau. Mol Ecol 19:338–351

    CAS  PubMed  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Rajaguru SN, Deo SG, Gaillard C (2014) Pleistocene geoarchaeology of Thar Desert. Ann Arid Zone 53:63–76

    Google Scholar 

  • Rambaut A (2016) FigTree. Version 1.4.3. http://tree.bio.ed.ac.uk/software/figtree

  • Rambaut A, Drummond AJ (2013) Tracer. v1.6.0. http://tree.bio.ed.ac.uk/

  • Rambaut A, Drummond AJ (2015) TreeAnnotator. Version 2.2.1. http://beast2.org

  • Rambaut A, Suchard M, Xie D, Drummond A (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Roselaar CS (1995) Songbirds of Turkey, an atlas of boidiversity of Turkish passerine birds. Haarlem

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    CAS  PubMed  Google Scholar 

  • Saitoh T, Alström P, Nishiumi I, Shigeta Y, Williams D, Olsson U, Ueda K (2010) Old divergences in a boreal bird supports long-term survival through the ice ages. BMC Evol Biol 10:35. https://doi.org/10.1186/1471-2148-10-35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandel B, Arge L, Dalsgaard B, Davies RG, Gaston KJ, Sutherland WJ, Svenning JC (2011) The influence of Late Quaternary climate-change velocity on species endemism. Science 334:660–664

    CAS  PubMed  Google Scholar 

  • Schenekar T, Weiss S (2011) High rate of calculation errors in mismatch distribution analysis results in numerous false inferences of biological importance. Heredity 107:511–512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Google Scholar 

  • Sharpe RB (1890) Catalogue of the passeriformes of perching birds in the collection of the British Museum, Sturnifonnes. Trustees of the Brit Mus (Nat Hist), London

    Google Scholar 

  • Sher AV (1997) Nature restructuring in the East-Siberian Arctic at the Pleistocenee Holocene boundary and its role in mammal extinction and emerging of modern ecosystems. Earth Cryosphere 1:21–29

    Google Scholar 

  • Sher AV, Kuzmina SA, Kuznetsova TV, Sulerzhitsky LD (2005) New insights into the Weichselian environment and climate of the east Siberian Arctic, derived from fossil insects, plants, and mammals. Quat Sci Rev 24:533–569

    Google Scholar 

  • Shirihai H, Svensson L (2018) Handbook of Western Palearctic birds. Hel, London

    Google Scholar 

  • Shroder JF, Bishop MP (2010) Glaciers of Pakistan. In: Williams RS, Ferrigno JG (eds) Satellite image atlas of glaciers. US Geological Survey Professional Paper, 1386-F-4

  • Smith BT, Klicka J (2013) Examining the role of effective population size on mitochondrial and multilocus divergence time discordance in a songbird. PLoS One 8:e55161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song G, Zhang R, Alström P, Irestedt M, Cai T, Qu Y, Ericson PGP, Fjeldså J, Lei F (2018) Complete taxon sampling of the avian genus Pica (magpies) reveals ancient relictual populations and synchronous Late-Pleistocene demographic expansion across the Northern Hemisphere. J Avian Biol 49:e01612

    Google Scholar 

  • Sorenson MD, Ast JC, Dimchev DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114

    CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thévenot M, Vernon R, Bergier P (2003) The birds of Morocco (BOU Checklist Series No. 20). Tring: British Ornithologists’ Union

  • Tieleman BI, Williams JB, Bloomer P (2003) Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc R Soc Lond B 270:207–214

    Google Scholar 

  • Tzedakis PC, Lawson IT, Frogley MR, Hewitt GM, Preece RC (2002) Buffered tree population changes in a Quaternary refugium: evolutionary implications. Science 297:2044–2047

    CAS  PubMed  Google Scholar 

  • van den Berg AB (2005) Morphology of Atlas Horned Lark. Dutch Birding 27:256–258

    Google Scholar 

  • Vaurie C (1951) A study of Asiatic larks. Bull Am Mus Nat Hist 97:435–526

    Google Scholar 

  • Vaurie C (1954) Systematic notes on Palearctic birds. No. 7. Alaudidae and Motacillidae (Genus Anthus). Am Mus Novit 1672:1–13

    Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Google Scholar 

  • Voelker G (1999) Dispersal, vicariance, and clocks: historical biogeography and speciation in a cosmopolitan passerine genus (Anthus: Motacillidae). Evol 53:1536–1552

    Google Scholar 

  • Weir JT, Schluter D (2004) Ice sheets promote speciation in boreal birds. Proc R Soc Lond Biol Sci 271:1881–1887

    Google Scholar 

  • Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328

    CAS  PubMed  Google Scholar 

  • Whistler H (1932) On some larks of the Kashmir State. Ibis 13:470–479

    Google Scholar 

  • Yurtsev BA (1981) Relict Steppe complexes in Northeast Asia (problems of reconstruction of cryoxerotic landscapes of Beringia). Nauka, Novosibirsk (in Russian)

    Google Scholar 

  • Zelenkov NV, Kurochkin EN (2012) The first representative Pliocene assemblages of passerine birds in Asia (northern Mongolia and Russian Transbaikalia). Geobios 45:323–334

    Google Scholar 

  • Zhao N, Dai CY, Wang WJ, Zhang RY, Qu YH, Song G, Chen K, Yang XJ, Zou FS, Lei FM (2012) Pleistocene climate changes shaped the divergence and demography of Asian populations of the great tit Parus major: evidence from phylogeographic analysis and ecological niche models. J Avian Biol 43:297–310

    Google Scholar 

  • Zheng H, Powell CM, An Z et al (2000) Pliocene uplift of the northern Tibetan Plateau. Geology 28:715–718

    Google Scholar 

  • Zheng H, Chen H, Cao J (2002) Palaeoenvironmental implication of the Plio–Pleistocene loess deposits in southern Tarim Basin. Chin Sci Bull 47:700–704

    CAS  Google Scholar 

  • Zhu B, Yu J, Qin X, Patrick R, Liu Z, Xiong H (2014) Formation and evolution of sand deserts in Xinjiang, Northwest China: I. Provenances of desert sands. J Geogr Sci 24:177

    Google Scholar 

  • Zink RM, Drovetski SV, Rohwer S (2002) Phylogeographic patterns in the great spotted woodpecker Dendrocopos major across Eurasia. J Avian Biol 33:175–178

    Google Scholar 

Download references

Acknowledgements

This research was supported by the Faculty of Science, Ferdowsi University of Mashhad (FUM) (Grant No. 3/29628 to FG). Permission to collect samples in Iran was authorized by the Iranian Department of Environment (Permission Number: 93/52337; 2015; 25th January). We are indebted to Lars Svensson for morphometric data of Eremophila bilopha; to Takema Saitoh for providing photographs of the type of Eremophila alpestris deosaiensis; and to Tommy Tyrberg for information on fossils. P.A. acknowledges support from the Swedish Research Council (Grant No. 2015-04402) and Jornvall Foundation. We also acknowledge all the museums that helped us and provided DNA samples or allowed access to their specimen collections: Pierre-André Crochet and Alban Guillaumet, the Burke Museum, University of Washington, Seattle, USA; Swedish Museum of Natural History, Stockholm, Sweden and The Natural History Museum, Tring, UK. FG is also grateful to Dr. Zeinolabedin Mohammadi and Dr. Asghar Khajeh for their kind cooperation in sampling and to the staff of the University of Gothenburg, Department of Biology and Environmental Sciences for their kind cooperation. The study complied with the laws of the countries in which sampling was undertaken. We also thank five anonymous reviewers for their valuable comments.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Fatemeh Ghorbani & Mansour Aliabadian

  2. Research Department of Zoological Innovations, Institute of Applied Zoology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Mansour Aliabadian

  3. Department of Biology and Environmental Sciences, Systematics and Biodiversity, University of Gothenburg, Box 463, 405 30, Göteborg, Sweden

    Urban Olsson

  4. Conservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Paul F. Donald

  5. Zoology Division, Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan, Pakistan

    Aleem A. Khan

  6. Animal Ecology, Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    Per Alström

  7. Swedish Species Information Centre, Swedish University of Agricultural Sciences, PO Box 7007, 75007, Uppsala, Sweden

    Per Alström

  8. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China

    Per Alström

Authors
  1. Fatemeh Ghorbani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mansour Aliabadian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Urban Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul F. Donald
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aleem A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Per Alström
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mansour Aliabadian.

Additional information

Communicated by M. Wink.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

ND2 tree for the genus Eremophila, estimated by Bayesian analysis. Outgroups are not shown (PDF 300 kb)

Fig. S2

Cytochrome b tree for the genus Eremophila, estimated by Bayesian analysis. The Genbank sequence KF060442 (Swedish Museum of Natural History No. NRM 20046759) was mislabeled “E. a. flava Sweden” in Alström et al. (2013), but concerned E. a. penicillata from Iran, and was thus relabeled in our analyses. Outgroups are not shown (PDF 265 kb)

Fig. S3

Skyline plots for ND2 based on 310 individuals mentioned in Table S2. The Bayesian skyline plots indicate effective population sizes (scaled by 2% divergence rate per million years for ND2) plotted as a function of time in million years. The skyline plot for clade D based on 32 sequences (cf Table S2) is labeled D (cyt b) (PDF 906 kb)

Fig. S4

Box-plots showing the variation of four variables among 14 taxa of Horned Lark. Variable and unit is shown on the y-axis. The black line within the box displays the median. Gray boxes indicate 50% of the sample points and are limited by the 1st (Bottom) and 3rd quartiles (Top) (PDF 905 kb)

Fig. S5

Differentiation of 228 individuals of 14 taxa of Eremophila using Linear Discriminant Analysis (LDA) for residual morphometric dimensions (PDF 293 kb)

Fig. S6

Scatter-plot of Principal Components Analysis examining differences in four morphometric traits (wing length, tail length, tail/wing [%] and bill length) for 222 individuals categorized by four clades on the phylogenetic tree. Eremophila a. montana (n = 6) was not included in this analysis, because it was not included in the phylogenetic analyses (PDF 169 kb)

Table S1

Genetic diversity of cyt b (70 individuals) and ND2 (310 individuals) mitochondrial genes. Statistical parameters indicate number of samples (N), number of haplotypes (nH), haplotype diversity (Hd ± SD), nucleotide diversity (π ± SD), singleton variable sites (S), number of variable sites (V), parsimony informative sites (P), Tajima’s D, Fu’s Fs, and R2 (Ramos-Onsin and Rozas’ statistic). P < 0.05 is in bold. Abbreviations: (A): alpestris; (B): penicillata; (C): bilopha; (D): longirostris; (Tau): age of expansion in units of mutational time; (Texp): time since onset of population expansion (thousand years ago), calculated only for populations inferred to deviate from demographic equilibrium by the majority of the estimators. Table S2 Multiple comparisons of means: Tukey contrasts for four characters (wing, tail, tail/wing [%], and bill) from 14 taxa (Abbreviations: Esti = Estimate; al = albigula; ar = argalea; at = atlas; bi = bicornis; bil = bilopha; br = brandti; el = elwesi; fl = flava; kh = khamensis; lo = longirostris; mo = montana; ni = nigrifrons; pe = penicillata, and pr = przewalski) (DOCX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghorbani, F., Aliabadian, M., Olsson, U. et al. Mitochondrial phylogeography of the genus Eremophila confirms underestimated species diversity in the Palearctic. J Ornithol 161, 297–312 (2020). https://doi.org/10.1007/s10336-019-01714-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-019-01714-2

Keywords

Search

Navigation