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Land Connectivity Changes and Global Cooling Shaped the Colonization Journal of Biogeography (J. Biogeogr.) (2015) ORIGINAL Land connectivity changes and global ARTICLE cooling shaped the colonization history and diversification of New World quail (Aves: Galliformes: Odontophoridae) Peter A. Hosner1*, Edward L. Braun1,2,3 and Rebecca T. Kimball1,2,3 1Department of Biology, University of Florida, ABSTRACT Gainesville, FL, USA, 2Genetics Institute, Aim Range disjunctions are frequent in birds, but the relative roles of vicari- University of Florida, Gainesville, FL, USA, 3 ance and long-distance dispersal in producing them are debated. Odontophorid Florida Museum of Natural History, University of Florida, Gainesville, FL, USA quail are widespread in tropical and temperate habitats in the Americas, yet recent phylogenetic studies support the view that they are sister to sub-Saharan African Ptilopachus rather than the widespread Phasianidae as formerly believed. To understand how this 10,000 km range disjunction arose in rela- tively non-vagile birds, we reconstructed colonization history and diversifica- tion of odontophorids with respect to hypothesized dry-land connections between continents (North Atlantic, Beringian, Panamanian) that would have facilitated faunal exchange. Location Africa, Nearctic and Neotropics. Methods We inferred a fossil-calibrated odontophorid phylogeny from DNA sequences (three mitochondrial genes and eight nuclear introns) and modelled ancestral ranges with six probabilistic biogeographical models. We used the Akaike information criterion (AIC) to select the best-fit biogeographical model. Results Ptilopachus and New World quail shared an Old World ancestor c. 32 Ma. During this period, Beringia connected the Nearctic and Palaearctic, and global temperatures were high, such that presence of temperate organisms at high latitudes and direct dispersal across land connections were feasible. The extant New World quail began diversifying in Central America c. 18 Ma; tim- ing estimates and ancestral range reconstructions support the hypothesis that New World quail colonized and diversified in South America following closure of the Isthmus of Panama. Main conclusions The Africa/New World range disjunction between New World quail and Ptilopachus is the result of changes in Earth and climate his- tory, combined with range expansion and diversification in the New World, and range contraction in the Old World. We find no evidence for overwater *Correspondence: Peter A. Hosner, dispersal in New World quail. Department of Biology, PO Box 118525, Keywords University of Florida, Gainesville, FL 32611, USA. Beringia, climate change, dispersal, faunal interchange, Isthmus of Panama, E-mail: hosner@ufl.edu phylogeny, Ptilopachus, range disjunction, vicariance. (Wiley, 1988; de Queiroz, 2005); that is, does long-distance INTRODUCTION dispersal or ancient vicariance produce these distributions? Organisms with limited dispersal capacity often exhibit Beyond understanding historical biogeography, understand- widely disjunct distributions. Ideas about the evolutionary ing the relative roles of dispersal and vicariance in creating processes that produce range disjunctions date to the foun- disjunct distributions is critical to understanding macroevo- dations of biogeography (Nelson, 1978; Sanmartın et al., lutionary patterns, such as geographical disparity in diversifi- 2001) and are central to the dispersal–vicariance debate cation rates (Rabosky, 2009). If driven by dispersal, range ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12555 P. A. Hosner et al. disjunctions are indicative of range expansion and increased connected Asia to North America (Simpson, 1947; Hopkins, potential for diversification. Alternatively, if driven by 1967; Marincovich & Gladenkov, 1999; Brikiatis, 2014). The ancient vicariance, disjunct distributions are relictual, and history and timing of North Atlantic land bridges is complex, indicative of range contraction and extinction. confusing and not wholly understood (e.g. Denk et al., 2011; In birds, continental range disjunctions are frequent in Brikiatis, 2014). In general, geological evidence supports the higher taxa. Common patterns include groups that are view that eastern North America and Europe were largely diverse in Afrotropical, Indomalayan and Neotropical regions connected until at least 55 Ma via the De Geer Route, and (e.g. barbets, Capitonidae; and trogons, Trogoniformes; later the Thulean Route (Brikiatis, 2014). Subaerial connec- Moyle, 2004; Hosner et al., 2010). In other groups, range tions established across Beringia around 100 Ma facilitated disjunctions are coupled with disparity in diversity, with faunal turnover until the late Miocene (Hopkins, 1967; Mar- species-rich clades inhabiting one continent and ‘relict’ incovich & Gladenkov, 1999; Brikiatis, 2014) when continu- lineages in another (Moyle et al., 2006, 2012; Reddy & ous land connections were interrupted by elevated sea levels Cracraft, 2007). There are similarly notable continental range (3–7.5 Ma, Marincovich & Gladenkov, 1999; 10–12 Ma, disjunctions documented in the fossil record (Mayr, 2004; Hopkins, 1967). From the late Pliocene until the present, Ksepka & Clarke, 2010; Nesbitt et al., 2011). land connections were periodically restored during glacial Birds are justly viewed as vagile organisms, and long-dis- maxima, the most recent of which ended c. 10 ka (Marinco- tance dispersal is a cause of range disjunction in some vich & Gladenkov, 1999; Miller, 2005). groups and species (Clegg et al., 2002; Billerman et al., Distributions of tropical/temperate organisms occurring 2011). However, despite having powered flight, birds fre- across high latitudes in Europe, Asia and North America in quently evolve limited ability to disperse to and colonize the warm early Tertiary would later be restricted to lower novel environs. In continental systems, tropical forest under- latitudes owing to massive global cooling events (first in the storey birds are often poor dispersers adapted to continuous early/middle Oligocene, and later in the late Miocene). Thus, habitats (Moore et al., 2008; Burney & Brumfield, 2009). climate-driven vicariance could widely explain avian distribu- Reduction of dispersal is considered advantageous for land tional disjunctions between the New World and the Old birds in island systems where dispersal ability may have World. Coincident with global cooling in the late Miocene, extreme fitness costs (Cody & Overton, 1996; Moyle et al., land connections initiated between Africa and the Mideast 2009). An extreme example of reduced dispersal is complete allowed dispersal and faunal interchange between Eurasia loss of flight, which has evolved multiple times in avian and Africa (Bibi, 2011). Similar faunal exchange occurred groups as diverse as rails (Rallidae), ducks (Anatidae) and between North and South America across the Isthmus of grebes (Podicipedidae) (Livezey, 1989; Fulton et al., 2012; Panama, in two pulses. An initial, minor pulse was the result Kirchman, 2012). of a brief or near (as a peninsula or archipelago) formation Avian biogeographers have historically favoured vicariant of an isthmus in the late Miocene (8–9 Ma, Coates et al., explanations for range disjunctions, particularly in pan-tropi- 2004; Montes et al., 2015). The second, major pulse was the cal groups. This view was fuelled by putative Gondwanan result of complete and permanent isthmus closure 3–4Ma distributions of poorly dispersing groups like the flightless (Webb, 1976; Weir et al., 2009; Leigh et al., 2013; Barker ratites (Cracraft, 2001). Molecular phylogenies now reject a et al., 2015). Gondwanaland origin for ratites, and instead support the Galliformes (landfowl) are almost worldwide in distribu- hypothesis that flighted ratite ancestors colonized continents tion, yet are among the least vagile orders of flying birds. across marine barriers, followed by convergent losses of flight There are two exceptions to this generalization. Megapodes (Smith et al., 2013; Mitchell et al., 2014). However, more (which are sister to all other Galliformes) are extremely vag- recent vicariance-driven disjunction remains a plausible ile and multiple lineages have colonized islands across the explanation for avian groups distributed across Africa, Asia Indo-Pacific region (Harris et al., 2014). Also, small-bodied and the New World. Facilitated by changing land connectiv- species in or related to the genus Coturnix (Old World quail) ity and climates, now-disjunct representatives of tropical/ are frequent on oceanic islands and have crossed Wallace’s temperate groups of Laurasian origin could conceivably and Lydekker’s lines. They are often nomadic or capable of occupy all continents except Australia and Antarctica without trans-continental seasonal migration (Johnsgard, 1988). Out- ever having crossed a marine barrier. side of megapodes and Old World quail there are no clear Land connections existed between the Palaearctic and examples of Galliformes occurring naturally on oceanic Nearctic through much of the Tertiary (reviewed in Brikiatis, islands (those without recent mainland connections during 2014). This extended connectivity, in combination with mild low sea-level stands, or connected by arctic sea ice in the global temperatures (Zachos, 2001), permitted broad distri- unique case of ptarmigans, Lagopus), suggesting that most butions of tropical and temperate organisms across Europe, Galliformes are incapable of crossing marine barriers. Based Asia and North America in the Palaeocene
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