Diversification Across the Palaearctic Desert Belt Throughout the Pleistocene
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Accepted on 13 June 2013 © 2013 Blackwell Verlag GmbH J Zoolog Syst Evol Res doi: 10.1111/jzs.12036 1Laboratoire des Substances Naturelles, Faculte des Sciences d’Agadir, B.P. 28/S. Universite Ibnou Zohr, Agadir Royaume du Maroc; 2Naturhistorisches Museum der Burgergemeinde Bern, Bern Switzerland Diversification across the Palaearctic desert belt throughout the Pleistocene: phylogeographic history of the Houbara–Macqueen’s bustard complex (Otididae: Chlamydotis) as revealed by mitochondrial DNA 1 2 AMAL KORRIDA and MANUEL SCHWEIZER Abstract Studies on the influence of Pleistocene climatic fluctuations and associated habitat changes on arid-adapted bird species living in the Holarctic region are comparatively rare. In contrast to temperate species, the populations of arid-adapted avian species might be characterized by low genetic differenti- ation because periods of population isolation were associated with the short interglacial periods, while population expansion events might have occurred during the longer glacial periods when steppe-like vegetation might have been prevalent. In this study, we tested this hypothesis in a widespread arid-adapted taxon of the Palaearctic desert belt, the Houbara–Macqueen’s bustard complex. The later includes the Houbara bustard Chlam- ydotis undulata, comprising the North African subspecies Chlamydotis u. undulata and Chlamydotis u. fuertaventurae from the Canary Islands, and the Asian Macqueen’s bustard Chlamydotis macqueenii. A long fragment (1042 bp) of the Cyt-b gene was investigated in 39 representatives of the two species to assess phylogenetic and phylogeographic patterns, and demographic history and to compute divergence time estimates using a Bayesian relaxed molecular clock approach based on different coalescent priors. While the two species are genetically distinct, we found little intraspecific genetic differentiation. The divergence time of the two species falls within a period of extreme aridity at around 0.9 million years ago, which most likely resulted in an east–west vicariance along the Arabo-Saharan deserts. Differentiation within Houbara and Macqueen’s bustard occurred later during the Middle to Upper Pleistocene, and as we have predicted, periods of range expansion were associated to the last glacial period at least in the Macqueen’s bustard. Key words: Aridification – glacial expansion – Houbara bustard – Macqueen’s bustard – Pleistocene Introduction for the diversification of animal species is still poorly understood (Guillaumet et al. 2008). Studies on species’ phylogeography are believed to explain The last period of stepwise desertification was followed evolutionary processes that shape species’ genetic diversity and around 0.9 Mya by an intensification of climatic cycles leading speciation processes over time (Avise 2000). The climate fluctua- to an accentuation in the sequence of glacial and interglacial tions over the last 2 million years had a strong influence on dis- periods (Hewitt 2000; DeMenocal 2004; Guillaumet et al. 2008). tribution and diversification patterns of extant biota. While many During the glacial cycles of this Late Pleistocene period, popula- studies dealing with the influence of historical processes on the tions of steppe- and arid-adapted forms in the Holarctic might assembly of biota have focused on temperate and boreal regions have been conversely affected than those of temperate taxa. of the Northern Hemisphere (e.g. Klicka and Zink 1997; Taberlet While the populations of temperate species might have been iso- et al. 1998; Hewitt 2004; Weir and Schluter 2004; Lovette lated and restricted to refugia during the longer glacial periods, 2005), the evolutionary history of arid zone biota is still compar- steppe- or arid-adapted forms might have reached their maximum atively poorly studied (cf. Byrne et al. 2008). Arid zone biomes range extent during glacial periods when steppe-like communities are widespread on earth. Desert regions in the Northern Hemi- expanded (Garcia et al. 2011a,b). Range restrictions and isolation sphere of the old world range from much of North Africa over might have thus only happened during the short interglacial the Arabian Peninsula into central and South Asia and can be times. As a consequence, a low genetic structuring should be divided into the Saharo-Sindian (Sahara to the Thar Desert of expected between populations of widespread steppe- or arid- Pakistan and India) and Caspian and central Asia deserts (Cowan adapted bird species due to shorter time spent in isolation 1996). Aridification in these regions began during the Miocene (Garcia et al. 2011a,b). with an increased stepwise drying up since the Pliocene with, at A bird species typical of the Saharo-Sindian and Caspian- least in Africa, three shifts towards more arid conditions near central Asian deserts is the Houbara bustard (Chlamydotis undulata, 2.8, 1.7 and 1.0 million years ago (Mya) (Flower and Kennett s. l., Houbara–Macqueen’s bustard complex hereafter). These bus- 1994; Guo et al. 2002; Douady et al. 2003; DeMenocal 2004; tards live almost exclusively in arid environments and belong to Guillaumet et al. 2008; Wu et al. 2011). The beginning of the the Otididae family (Cramp and Simmons 1980; Sibley and Ahl- desertification of the Sahara was revealed as a vicariance agent quist 1990). Chlamydotis undulata has for a long time been in elephant shrews (Macroscelidae) (Douady et al. 2003). More- regarded as a polytypic species and divided into three subspecies over, climate variability from the Pliocene onwards with stepwise according to geographic distribution and morphology (Cramp and increased aridity mediated faunal changes in Africa (DeMenocal Simmons 1980). The nominate subspecies, C. u. undulata (Jacquin 2004) and led to vicariance across the Saharo-Sindian deserts in 1784) (Cuu hereafter), is found across North Africa from Morocco Galerida larks (Guillaumet et al. 2008). However, the Sahara and northern Mauritania to western Egypt, while the populations was found not to be a permanent barrier through geological found in the Canary Islands have been separated as C. u. fuertaven- times, and the role of the stepwise aridification of these deserts turae (Rothschild and Hartert 1894) (Cuf hereafter). Chlamydotis u. macqueenii (Gray 1832) (Cm hereafter) occurs further east from eastern Egypt, Arabian Peninsula, Pakistan to central Asia. Overall, Corresponding author: Amal Korrida ([email protected]) Houbara bustard is listed by the IUCN (2012) as threatened Contributing authors: Manuel Schweizer ([email protected]) throughout its range and classified as ‘vulnerable’,asdifferent Journal of Zoological Systematics and Evolutionary Research (2014) 52(1), 65--74 66 KORRIDA and SCHWEIZER populations have suffered substantial declines in recent times fying the genetic variation between and within the different popu- mainly from habitat alterations, overgrazing and hunting pressure lations of the entire complex and at identifying the historical and (Malik 1985; Lavee 1988). demographic factors, which might have shaped its phylogeograph- Several recent molecular genetic studies of the Houbara– ic patterns. Based on the conflicting results of previous studies Macqueen’s bustard complex have demonstrated that Cuu/Cuf (Idaghdour et al. 2004; Pitra et al. 2004), we wanted to test and Cm form reciprocally monophyletic population groups with whether the phylogeographic structure of the Houbara– a unique and divergent evolutionary history (Broders et al. 2003; Macqueen’s bustard complex was shaped by periods of increased Idaghdour et al. 2004; Pitra et al. 2004; Lesobre et al. 2010). aridification of the Sahara and adjacent desert regions from the Pli- Based on these results and studies on courtship behaviour and ocene until the Middle Pleistocene, or whether it was influenced plumage features (Gaucher et al. 1996) as well as vocalization by glacial cycles in the Late Pleistocene. Moreover, we wanted to (Alekseev 1985; Gaucher et al. 1996), the taxonomic subcommit- infer whether periods of population expansions indeed fall into gla- tee of the British Ornithologist Union has recommended that the cial periods as was predicted for steppe- and arid-adapted species. Houbara bustard should be treated as two separate species according to the guidelines of Helbig et al. (2002), with the Materials and methods monotypic Macqueen’s bustard C. macqueenii and the polytypic Houbara bustard C. undulata comprising the subspecies Source of samples, DNA extraction and PCR amplification C. u. undulata and C. u. fuertaventurae (Knox et al. 2002; A total of 39 individuals of the Houbara–Macqueen’s complex were Collinson 2004; Sangster et al. 2004). fi investigated in this study. Twenty-four specimens were newly sampled, The biogeographic history and temporal diversi cation patterns comprising six Cuu from eastern and southern Morocco, six Cuf from – ’ of the Houbara Macqueen s bustard complex in the context of Fuerteventura (Canary Islands), eight Cm from Baluchistan, Negev desert the climate fluctuations during the last million of years have been and Afghanistan. In addition, one sample each of Eupodotis humilis, controversially discussed. Idaghdour et al. (2004) used demo- Eupodotis senegalensis, Ardeotis kori and Ardeotis arabs were used as graphic approaches and an approximation of the mutation rate in outgroup taxa. The remaining 19 cytochrome-b sequences were obtained the mitochondrial DNA control region to estimate divergence from GenBank (Table 1 and Fig. 1). Blood and tissue samples