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Journal of Ornithology

, Volume 161, Issue 1, pp 297–312 | Cite as

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

  • Fatemeh Ghorbani
  • Mansour AliabadianEmail author
  • Urban Olsson
  • Paul F. Donald
  • Aleem A. Khan
  • Per Alström
Original Article

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.

Keywords

Horned Lark Qinghai–Tibetan Plateau Species complex Phylogeny Taxonomy 

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.

Notes

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.

Supplementary material

10336_2019_1714_MOESM1_ESM.pdf (301 kb)
Fig. S1 ND2 tree for the genus Eremophila, estimated by Bayesian analysis. Outgroups are not shown (PDF 300 kb)
10336_2019_1714_MOESM2_ESM.pdf (265 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)
10336_2019_1714_MOESM3_ESM.pdf (906 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)
10336_2019_1714_MOESM4_ESM.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)
10336_2019_1714_MOESM5_ESM.pdf (293 kb)
Fig. S5 Differentiation of 228 individuals of 14 taxa of Eremophila using Linear Discriminant Analysis (LDA) for residual morphometric dimensions (PDF 293 kb)
10336_2019_1714_MOESM6_ESM.pdf (169 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)
10336_2019_1714_MOESM7_ESM.docx (37 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)

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Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceFerdowsi University of MashhadMashhadIran
  2. 2.Research Department of Zoological Innovations, Institute of Applied Zoology, Faculty of ScienceFerdowsi University of MashhadMashhadIran
  3. 3.Department of Biology and Environmental Sciences, Systematics and BiodiversityUniversity of GothenburgGöteborgSweden
  4. 4.Conservation Science Group, Department of ZoologyUniversity of CambridgeCambridgeUK
  5. 5.Zoology Division, Institute of Pure and Applied BiologyBahauddin Zakariya UniversityMultanPakistan
  6. 6.Animal Ecology, Department of Ecology and Genetics, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  7. 7.Swedish Species Information CentreSwedish University of Agricultural SciencesUppsalaSweden
  8. 8.Key Laboratory of Zoological Systematics and Evolution, Institute of ZoologyChinese Academy of SciencesBeijingChina

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