PROGRESS IN NATURAL SCIENCE Vo l .17 , N o .9 , September 2007

Contact and hybrid zone hotspots and evolution of in the Middle East＊

M ansour Aliabadian1 , 2＊＊ , M oham mad Kaboli3 , Bahram Kiabi4 and Vincent Nijman1

(1 .Institute for Biodiversity and Ecosystem Dynamics, Zoological Museum , University of Amsterdam , 1090 GT Amsterdam , The Netherlands;2 .Departmen t of Biology , Faculty of S ciences, Feredow si University , Mashad , ;3 .Department of Fishery and Envi- ronment , Faculty of Natural Resou rces, Tehran University , Iran ;4 .Department of Biology , Faculty of S ciences, University of Shahid Beheshti, Tehran , Iran)

Accepted on Feb ruary 2 , 2007

Abstract The Middle East is an im portant contact zone for a considerable number of taxa from the western and eastern Palearctic and from the great Saharo-Sindian desert belt .Using W ORLDMAP softw are, we analyzed the geographical distribution of sec- ondary contact zones for parapatric species pairs of birds in the Middle East .We identified 56 species(29 species pairs)that make contact in the Middle East.The species pairs belong to three orders, i.e.Falconiformes, Piciformes, and Passeriformes.Almost half (46 %)of these species pairs hybridize in their contact zones.Although contact zones occur over a large part of northern Middle East, spatially they w ere not evenly distributed.Contact zone richness w as highest in the mountain ranges south of the Caspian Sea and the Caucasus.The hottest hotspots, w here up to nine bird species pairs occur sympatrically , are situated in north-eastern Iran and .We discuss the relevance of these hotspots for improving our understanding of the biogeography and evolution of the avifauna in the Middle East .

Keywords: contact zone , hybridisation, Middle East , parapatry , species-pairs, zoogeography.

The importance of documenting contact zones of a considerable number of bird taxa from the w estern related species of org anisms has been lo ng recognized and eastern Palearctic and from the great Saharo-Sin- [ 9, 10] [ 11] by evolutionary biologists[ 1] .Data derived from these dian desert belt .Haffer and Vauri , based on studies can be considered crucial for study ing hy- cursorily observatio ns , found that contact zones of po theses of phylogenetic relationships and speciation parapatric birds are mo re common in the Middle East processes.Contact zones usually are defined as the than in other similar areas .This high occurrence of meeting area of closely related species pairs , implying contact zones is probably best explained by invoking a [ 9, 12] a deg ree of cong ruence in their separate distribu- refuge theo ry , w here populations of birds in the tion[ 2] . They have been frequently reported in Middle East survived the proceeding cold-arid clim atic birds[ 3] , and represent major zones of biogeographic phase of the last g lacial stage in moist refuges .The high diversity of habitats and a fast clinal habitat vari- discontinuity , and probably current or former barri- [ 4] ation along steep clines in the Middle East provided ers .M any , but not all , of the parapatric species ideal opportunities for secondary contact . pairs hybridize in their contact zones , and about 7 % of the species that have produced hybrids in nature , We[ 13] recently analy zed the geographical distri- [ 5] have a parapatric contact zo ne .The identification bution of these contact zones for parapatric species of hybrids between these closely related taxa bears pairs of songbirds in the Palearctic Region .We found relevance for the study of gene flow and the evolution that , although contact zones of 52 species-pairs cov- of mechanisms of genetic isolation , and , hence , of ered large parts of the Palearctic , spatially they w ere [ 6 , 7] speciation . Furthermore , the inbreeding of no t evenly distributed .The contact zone richness species is of pivotal importance in framing ideas about reaches it highest deg ree in the mountain ranges of the nature of taxonomic judgments to be made about south-west Asia , north-w est Africa , north-central A- particular populations[ 8] . sia , and south-central Asia .The hottest hotspots were found in no rth-eastern Iran , w here up to 9 The Middle East is an important contact zone fo r songbird species-pairs occurred sympatrically .

＊ Supported by the Iranian Ministry of S cience and Technology and the PA Hens Memorial Fund ＊＊ To w hom correspondence should be addressed .E-mail:aliabadi@science .uva .nl Prog ress in Natural Science Vol.17 No .9 2007 w ww .tandf.co .uk/journals 1115

Given the impo rtance of the M iddle East fo r species as tw o species form a species pair with mo re parapatric species pairs , not just song birds but possi- than one sister taxa)that make contact in the Middle bly other birds , and indeed o ther vertebrates as East as defined above (Table 1).Tw o species , Syrian w ell[ 14] , we expanded our analysis as to include all Woodpecker Dendrocopus syriacus and Ortolan o rders of birds .This in turn allowed us to test Bunting Emberiza hortulana , make secondary con- w hether or not non-Passeriformes and Passeriformes tact w ith tw o species , w hereas all the o thers are in do show the same geographical pattern in the region . contact w ith just one species .These 56 species repre- sent 12 % of the 462 breeding residents recorded in 1 Material and methods the Middle East .How ever , secondary contact is not evenly spread among the different orders .In fact , all The study area encompasses the M iddle East species pairs belong to just three orders , i .e .Falco ni- from in the west to Iran in the east and from formes (birds of prey ), Piciformes (w oodpeckers) Azerbaijan in the north to Yemen in the south .The [ 13] and Passeriformes (song birds).Within these three methodology follow s that of Aliabadian et al . g roups secondary contact is highest in Picifo rmes w hich can be summ arized as follows .Parapatric (25 % or 3 out of 12 breeding residents in the Middle species pairs w ere identified as species w hich inhabit East), followed by Passeriformes (20 % or 45 out of contagious ranges excluding each other geographically 221)and Falconiformes (20 % o r 8 out of 41). w ith no or restricted hybridization along their contact zo nes[ 9, 11] .Records of hybridization among these A relatively large propo rtion of these species species were com piled from Bures et al.[ 15] and Ran- pairs (46 %)hy bridize in their contact zones .Hy- [ 16] bridization does not occur in all areas where the tw o dler .Nomenclature and follow s Dickin- species meet , and hence , not all of the hybridizing son[ 17] .Choice of species concept can have its influ- [ 18 , 19] species-pairs appear to do so in the Middle East ence on the positioning of hotspots in the con- (Table 1). struction of the database we follow ed the biological species concept (see Sangster et al .[ 20] for a review of The overlap zones of the different species pairs in species concepts). the Middle East average 187000 ±302000 km2(range 4000 —1300000 km2);fo r 8 out of 29 species pairs A database w as created of digitized distribution the overlap zones are confined to the M iddle East maps for the species studied w ith the help of the com- [ 21] (Table 1).The combined land area where one or puter program WORLDMAP version 4 .1 .The more species pairs occur covers about a third of the geographic distributions were interactively plotted on Middle East .Contact zo nes cover a large number of an equal area map of the M iddle East , overlaid by a 2 countries , including most of Turkey , , Azer- one deg ree-wide grid (g rid cell area :4062 km ).Fo r baijan, and Lebanon , and large parts of Eastern all parapatric species pairs we com piled distribution Mediterranean region and Iran .Contact zones w ere [ 22] maps based primarily on Porter et al. and Snow et no t recorded for most of the Arabian Peninsula .Al- al .[ 23] , and various other literature sources , supple- though contact zones occur over a large part of north- mented by data obtained from the examination of bird ern Middle East , spatially they were not evenly dis- skins —and specimen labels —in numerous zoological tributed .The contact zone richness is hig hest in the collections[ 24] .We produced com bined m aps for the mountain ranges bordering the southern Caspian Sea tw o taxa in each pair and extracted the overlap of including parts of the Caucasus mountain range (viz . their distribution areas as a new map .Information on eastern Turkey , Armenia , southern Azerbaijan , and secondary contact zones , and w hich species w ere in- no rthern Iran). [ 9, 10] volved , w as taken from Haffer .The contact Six ho tspots covering a mere 8 .3 % of the Mid- zo nes of all species pairs considered herein w ere subse- dle East harbour some 25 % of all species pairs .The quently combined and their geographic distribution ho ttest g rid cells include seven to nine species pairs analy sed . 2 and cover only about 70000 km in Azerbaijan and I- 2 Results ran .

We identified 29 species pairs (involving 56 1116 w ww .tandf.co .uk/journals Prog ress in Natural Science Vol .17 No .9 2007

T able 1 . List of parapatric species pairs tha t do hybridize o r have a secondary contact zone in the M iddle East , with the area of over- lap o f their distribution areas . Ov erlap zone Hybridization recorded Scientific names Order (×1000 km2) (N =no ;Y =yes) Falco biarmicus/ F .cherrug Falconiformes 57 N Falco peregrinus/ F .pelegrinoides Falconiformes 4 Y (outside) Buteo buteo/ B .rufinus Falconiformes 309 ＊ Y (outside) Accipiter brevipes/ A .badius Falconiformes 8 Y Dendrocopos syriacus/ D .assimilis Piciformes 20 Y Dendrocopos syriacus/ D .major Piciformes 142 ＊ Y (outside) Lanius collurio/ Lanius isabellinus Passerifo rmes 69 ＊ Y (outside) Corvus ru ficollis/ C .corax Passerifo rmes 264 ＊ Y (outside) Parus major/ P .bokharensis Passerifo rmes 57 ＊ Y (outside) Parus xanthogenys/ P .spilonotus Passerifo rmes 8＊ N Melanocory pha calandra/ M .bimaculata Passerifo rmes 1300＊ N Calandrella rufescens/ C .cheleensis Passerifo rmes 16 ＊ N Alauda arvensis/ A .gulgula Passerifo rmes 16 ＊ N Eremophila alpestris/ E .bilopha Passerifo rmes 12 ＊ N Acrocephalus arundinaceus/ A .stentoreus Passerifo rmes 49 ＊ Y (outside) Hippolais languida/ H .olivetorum Passerifo rmes 73 N Phylloscopus collybita/ P .lorenzii Passerifo rmes 158 ＊ N Phylloscopus bonelli/ P .sibilatri x Passerifo rmes 8＊ Y (outside) Sy lv ia curruca/ S .althaea Passerifo rmes 20 ＊ Y (outside) Sy lv ia melanocephala/ S .mystacea Passerifo rmes 69 N S itta neumayer/ S .tephronota Passerifo rmes 841 N Luscinia luscinia/ L .megarhynchos Passerifo rmes 49 ＊ Y (outside) Oenanthe pleschanka/ O .hispanica Passerifo rmes 650 ＊ Y Oenanthe xanthopry mna/ O .chrysopygia Passerifo rmes 8 Y Passer domesticus/ P .indicus Passerifo rmes 8＊ Y (outside) Bucanetes githagineus/ B .mongolica Passerifo rmes 475 ＊ N Emberiza hortulana/ E .buchanani Passerifo rmes 459 ＊ N Emberiza hortulana/ E .caesia Passerifo rmes 264 ＊ N Emberiza melanocephala/ E .bruniceps Passerifo rmes 4＊ Y No te :O verlap zo nes refer to the M iddle East only :asterisk (＊)indicates that species do have overlap zones outside the Middle East as well ;Y (outside)indicates that the species tha t make up this species pair do hybridize but hy bridizatio n has not (y et)been recorded in the M iddle East.List compiled from Haffer[ 9 , 10] ;info rmation on hybridisatio n re trieved from Bures et al.[ 15] and Ran- dler[ 16] 3 Discussion ranges southeast into I ran , w hereas that of non- Passeriformes is restricted to the northern part of the Our analy sis has revealed a distinctly uneven ge- Middle East . og raphical distribution of bird contact zones in the M iddle East .Their highest incidence corresponds to Hybridization betw een the tw o members of the mountainous areas in no rthern Middle East .Althoug h species pair w as frequent althoug h not necessarily in the number of non-Passeriformes that make secondary the Middle East .The Turkistan tit Parus bokharen- contact zones in the Middle East is low compared to sis and great tit P .major , for ex ample , hy bridize a- Passeriformes (6 com pared to 23 pairs), the geo- long a narrow contact zone (40000 km2)in south- g raphical distribution of their secondary contact zones eastern but are sym patric without hy- is similar .The most prominent difference is that the bridization in a vast area (120000 km2 )in Iran , [ 25] contact zones fo r songbirds includes the Zag rose , Turkmenistan and . M ountains that runs from the northern mountain Prog ress in Natural Science Vol.17 No .9 2007 w ww .tandf.co .uk/journals 1117

The hig h degree of cong ruence of the geographi- Martins and Hirschfeld[ 34] in their study on the cal positioning of contact zones between different or- limits of Western Palearctic noted the relationships ders of birds suggests that the Middle East could have betw een the distributions of related species that occu- been an important centre for the evolution of the avi- pying similar niches in Iran .They concluded that fauna and other anim als alike[ 26—28] .Birds are a rela- no rth and w est Iran are best considered to fo rm part tively young g roup that first appeared in the fossil of the Western Palearctic , w hereas the low land east- record in the Late Oligocene-Early Miocene[ 29] . ern areas are best viewed as a transitional zone , w here Their main radiation took place in M iocene-Pliocene several Palearctic species with eastern affinities have times , and w ould have been completed by the mid-to their westernmost limits .Our results from the distri- late Pleistocene[ 30] .This period w as m arked by sig- bution of hybrid —and contact zone hotspots show [ 31] that this transition zone also includes southern Azer- nificant climatic oscillations that had profound im- [ 32] baijan, Armenia , and eastern Turkey .A detailed pacts on the geographic distribution of birds .This analysis into the patterns of distribution of species climatic change started w ith the g radual g lobal cooling pairs (avian and other)in these areas , as w ell as ex- during the mid-Oligocene (30 Mya)and w as followed ploring the phylogenetic relationship betw een these by a series of about 20 strong short-term w et-dry and tax a , may be a promising avenue for further re- cool-w arm fluctuation in the Late Pliocene and the search . Pleistocene .This resulted in periodic shifts of bird distributions, i .e ., w ithdraw al of tropical birds from Acknowledgements W e are gra teful to Dr .P .H . the northern hemisphere to the equator (g lacial peri- Williams (Natural Histo ry Museum , L ondo n)for making avail- ods)and re-expansion to the north (interg lacial peri- able the WO RLDM A P pro gram , and fo r implementing our [ 28] Palearctic map in that pro gram .K ees (C.S .)Roselaar, Prof . ods) .The geographical and climatic history of the Dr.F .R .Schram , Dr.R.Sluy s (all University of Amster- M iddle East allow ed sig nificant shifts in species distri- dam), and Prof .M .V ences (T echnical U niversity of Braun- butions and large mig ratory movements[ 27] .The in- schweig)are thanked for help and support .W e also thank an termittent presence of species and subsequent isolation anonymous reviewer for sug gestions to impro ve the paper. of rem aining populations has led to regionally differ- References entiated taxa .The patterns of seco ndary contact zo nes in the Middle East as observed at present sug- 1 Mayr E . Species and Evolution .Cambridge:Harvard Uni- versity Press, 1963 gest that the no rthern part of the Middle East —espe- 2 Short LL .Taxonomic aspects of avian hyb ridization .Auk , 1969 , cially the area south of the Caspian Sea —can be seen 86 :84 —105 as a major biogeographical crossroad betw een the west 3 Dixon KL .Contact zones of avian congenens on the southern Great (i .e .Palearctic Region)and the east (i .e .Oriental Plains.Condor , 1989 , 91 :15 —22 [ 33] 4 Haffer J.Contact zones between birds of southern Amazonia.Or- Region) . nithological Monographs, 1997 , 48 :281 —305 5 Aliabadian M and Nijman V .Avian hyb rids:incidence and geo- g raphic distribution of hybridisation in birds.Contribution to Zoolo- gy , 2006 , 76 :57 —60 6 Barton NH .The role of hybridization in evolution .Molecular Ecol- ogy , 2001 , 10 :551 —568 7 Roselaar CS , Prins TG, Aliabadian M , et al.Hybrids in divers (Gaviiformes).Journal of Ornithology , 2006 , 147 :24 —30 8 Veith M , Fromhage L , Kosuch J, et al.Historical biogeog raphy of Western Palearctic pelobatid and pelodytid frogs:a molecular phy- logenetic perspective .Contributions to Zoology , 2006 , 75 :107 — 120 9 Haffer J.S econdary contact zones of birds in northern Iran .Bonner Zoölogischer M onographs, 1977 , 10 :1 —64 10 Haffer J.Parapatric species of birds.Bulletin of the British Or- nithologists' Club , 1992 , 112 :250 —264 11 Vauri C .S ystematic notes on Palearctic birds.No .5 , 6 , 9 , 24 , 26 , 27 , 35 , 44 , 46 , 49 .American Museum Novitates, 1954 — 1965 , 1668 , 1669 , 1685 , 1814 , 1852 , 1863 , 1946 , 2035 , Fig .1 . Pattern of contact zones in the Middle East :the hottests 2039 , 2058 hotspots are situated in moun tain ranges sou th of the Caspian Sea 12 Haffer J and Prance GT .Climatic forcing of evolution in Amazonia and in the Caucasus M ountains. during the Cenozoic :On the refuge theory of biotic differentiation . Amazoniana , 2001 , 16 :579 —607 1118 w ww .tandf.co .uk/journals Prog ress in Natural Science Vol .17 No .9 2007

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