Spanning nearly the entire length of western South America, the Andes mountain range provides a rich natural laboratory for studies of biogeography, geographic variation, and speciation (e.g., Chapman 1917; Remsen 1984; Hillis 1985; Graves 1988; Patton and Smith 1992; Young et al. 2002; Hall 2005). The Andean uplift played important roles in the historical diversification of Neotropical organisms both by isolating lowland organisms on either side of the mountains (Haffer 1967; Gentry 1982; Lynch and Duellman 1997) and by producing a mosaic of montane and inter-Andean valley habitats in which colonization and differentiation could occur (Graham et al. 2004; Hughes and Eastwood 2006). What remain poorly understood are the evolutionary dynamics surrounding the colonization and differentiation of populations in highland habitats as well as the subsequent re-colonization of lowland habitats.
Most Neotropical models of diversification invoke geographic isolation as the primary mode of differentiation (e.g., Haffer 1969; Capparella 1991; Nores 1999). Although the importance of geographic isolation in vertebrate speciation is still debated (reviewed in Fitzpatrick and Turelli 2006), the fact that most vertebrate Neotropical sister taxa are distributed parapatrically or allopatrically argues that geographic isolation should represent the null diversification hypothesis for vertebrates in the Neotropics (Jordan 1905; Mayr 1942; Chesser and Zink 1994; Fjeldså 1994; Cheviron et al. 2005a). The most widely cited exception to allopatric speciation is a model of speciation via primary differentiation along ecological gradients (Endler 1977). Chapman (1926) anticipated this model in trying to explain the differentiation of foothill from lowland populations of birds in Ecuador. Although ecological gradients can produce genetic differentiation among bird populations, empirical demonstrations of speciation via such gradients remain few (Smith et al. 2005). Tests of these hypotheses in the Neotropics used different approaches (population genetic versus phylogenetic), but have generally corroborated geographic isolation as the dominant force in mammals (Patton and Smith 1992) and birds (Fjeldså 1994; Roy et al. 1997, 1999; García-Moreno and Fjeldså 2000; Dingle et al. 2006). In contrast, speciation in Andean anurans (Lynch and Duellman 1997; Graham et al. 2004) and insects (Willmott et al. 2001), which hold smaller ecological niches than birds and mammals, may be more heavily influenced by divergent ecological regimes. For the purposes of this study, we consider geographic isolation to be the primary mechanism of speciation in birds and, in the context of a well-resolved molecular phylogeny, explore potential vicariant processes that could have isolated birds in highland and lowland habitats.
Previous studies of Neotropical organisms suggest that habitat and elevation shifts may occur frequently (Bates and Zink 1994; García-Moreno and Silva 1997; Salazar-Bravo et al. 2001; Aleixo 2002; Donato et al. 2003; Weir 2006), so that studies of taxa composing a suite of habitats are required to provide a complete test of Neotropical diversification mechanisms. Whereas biogeographic analyses of exclusively highland or exclusively lowland species groups provide insights into the historical diversification processes operating within these regions, studies of species groups containing both highland and lowland representatives may offer an evolutionary snapshot of the processes underlying evolution into and out of the Andes. Phylogenetic relationships among Neotropical birds have been elucidated for a number of species groups, but many of these studies analyzed lowland (e.g., Brumfield and Capparella 1996; Aleixo 2002; Marks et al. 2002; Cheviron et al. 2005b; Porzecanski and Cracraft 2005) or high elevation taxa (e.g., Arctander and Fjeldså 1994; Roy et al. 1999; García-Moreno et al. 1999, 2001; Pérez-Emán 2005) exclusively. In cases where a phylogenetic study included taxa from both lowland and highland regions, the analysis did not include ancestral reconstructions of elevational distribution (Burns 1997; Lovette and Bermingham 2001) or, after the phylogenetic analysis, it was unclear if the highland and lowland taxa even represented a clade (Chesser 2000). To examine the interplay between highland and lowland regions explicitly, we present an analysis of historical diversification in an avian genus (Thamnophilus) containing both highland and lowland species.
Nearly all core bird communities (Remsen 1994) of the lowland and foothill forests of Central America and tropical South America include at least one antshrike species from the genus Thamnophilus (Aves: Thamnophilidae) (Terborgh et al. 1990; Ridgely and Tudor 1994; Robinson et al. 2000; Zimmer and Isler 2003). Collectively, Thamnophilus species span humid and arid habitats of the eastern slope of the Andean foothills from Colombia to northern Argentina, and wet and dry lowland habitats in most regions of southern Central America and tropical South America (Zimmer and Isler 2003). Such geographic coverage and breadth of habitats, found in only a handful of other Neotropical suboscine genera (e.g., Myrmotherula antwrens, Elaenia flycatchers), make having a resolved phylogeny of Thamnophilus desirable insofar as the evolutionary relationships of its component species are likely to yield insights into general historical processes of diversification. Because of their widespread distribution, Thamnophilus antshrikes present a unique opportunity to examine the impact of the Andes on the historical diversification of organisms, including evolution both into and out of high elevation habitats (Bates and Zink 1994; García-Moreno and Silva 1997), as well as the diversification of lowland organisms isolated on either side of the mountains (Brumfield and Capparella 1996).
As currently recognized (Remsen et al. 2006), the genus Thamnophilus is composed of 27 species, all of which are insectivorous, socially monogamous, and sexually dichromatic, and which exist in the under- to mid-story of forest interiors, forest edge, or scrub (Table 1). The genus appears to be monophyletic based on similarities in vocalizations and behavior (Zimmer and Isler 2003), with the important caveat that one or more species from the antshrike genus Sakesphorus could fall within it. Sakesphorus has long been thought to be polyphyletic based on vocal and behavioral similarities of some of its species to Thamnophilus (Zimmer and Isler 2003). Within Thamnophilus, two main groups are readily recognizable by plumage pattern: (1) 7 barred species, the males of which have at least some horizontal black-and-white barring on the breast (the barring extends to other regions of the body in some taxa); and (2) 20 mostly solid species (ranging from pale gray to black), the males of which lack barring on the breast. As barred and solid plumages are found in other thamnophilid genera known to fall phylogenetically outside Thamnophilus (Irestedt et al. 2004), they are clearly homoplasious characters, but they provide a useful characterization of the two basic Thamnophilus plumage patterns. Variation within Sakesphorus includes solid plumage as well as a third readily recognizable plumage pattern exhibited by four of the six species (S. canadensis, S. cristatus, S. melanonotus, and S. bernardi): solid plumage, but with a contrasting white belly. Plumage and morphological variation in Thamnophilus and Sakesphorus do not offer a rich palette of characters from which to reconstruct a robust phylogeny (Zimmer and Isler 2003). It is thus not surprising that previously published hypotheses of intrageneric relationships are few and largely relegated to statements of probable affinities in a nonphylogenetic context, or to taxonomic sequence in linear classifications. Most of the previously proposed phylogenetic relationships involve likely sister relationships between recently elevated allotaxa, with essentially no previously proposed hypotheses of higher level interspecific relationships.
|Species||Tissue number1||Locality||Elevation2||Habitat3||Collector or preparator|
|Thamnomanes caesius||B9482 (LSUMZ)||Guyana: Northwest District; Baramita||L||R. T. Brumfield|
|Cymbilaimus lineatus||B18168 (LSUMZ)||Bolivia: depto. Santa Cruz; Velasco; Parque Nacional Noel Kempff Mercado, 86 km ESE Florida||L||A. W. Kratter|
|Frederickena unduligera||B4281 (LSUMZ)||Peru: depto. Loreto; Lower Río Napo region, E bank Río Yanayacu, ca. 90 km N Iquitos||L||D. L. Dittmann|
|Sakesphorus canadensis||MBR6243 (KU)||Guyana: along Washikunhmra River||L||Tropical deciduous and gallery forest||M. B. Robbins|
|Sakesphorus cristatus||B1188||Brazil: Minas Gerais; Bocaiuva||L||Tropical deciduous forest and arid scrub||L. Carrara|
|Sakesphorus luctuosus||B7012 (USNM)||Brazil: Para; 52 km SSW Altamira||L||Flooded tropical evergreen and river-edge forest||G. R. Graves|
|Sakesphorus bernardi||B5136 (LSUMZ)||Peru: depto. Lambayeque; Las Pampas, km 885 Pan-American Hwy, 11 road km from Olmos||L (0–1000 m)||Tropical deciduous forest, arid lowland scrub, riparian thickets||D. L. Dittmann|
|Sakesphorus melanonotus||ML768||Venezuela: edo. Zulia; Campo Boscán, Hda. Grano de Oro||L (0–500 m)||Tropical deciduous forest||M. Lentino|
|Sakesphorus melanothorax||B46298 (LSUMZ)||Brazil: Amapá; Alto Rio Araguiri (collected in 1963)||L (0–550 m)||Flooded tropical evergreen forest||M. M. Moreira|
|Thamnophilus atrinucha||B393 (USNM)||Panama: prov. Bocas del Toro; Isla San Cristobal, Bocatorito||L (0–1500 m)||Tropical lowland evergreen forest||T. J. Parsons|
|Thamnohilus bridgesi||B16149 (LSUMZ)||Costa Rica: prov. Puntarenas; 2 km SE Dominical||L (0–1100 m)||Tropical lowland evergreen, gallery, mangrove, and secondary forest||S. J. Hackett|
|Thamnophilus doliatus||RTB390 (UWBM)||Bolivia: depto. Santa Cruz; prov. Cordillera, 10.6 km E Abapo||LH (0–2000 m)||River-edge forest, second-growth scrub, riparian thickets, river-island scrub||R. T. Brumfield|
|Thamnophilus multistriatus||B52717 (LSUMZ)||Colombia: depto. Santander; Gomez (collected in 1962)||H (900–2200 m)||Edge of montane evergreen and tropical deciduous forest, and second-growth scrub||M. A. Carriker, Jr.|
|Thamnophilus zarumae||B191 (LSUMZ)||Peru: depto. Piura; km 34 on Olmos-Bagua Chica Hwy||H (800–2100 m)||Tropical deciduous forest||J. P. O'Neill|
|Thamnophilus tenuepunctatus||B1686 (ANSP)||Ecuador: prov. Zamora Chinchipe; Zaruma, 1400 m||H (500–2500 m)||Montane evergreen forest||B. Slikas|
|Thamnophilus palliatus||MAB2 (UWBM)||Bolivia: depto. Santa Cruz; prov. Florida, 23.2 km E Samaipata||LH (0–2200 m)||Montane and tropical lowland evergreen forest, and second-growth scrub||M. A. Blendinger|
|Thamnophilus torquatus||B13900 (LSUMZ)||Bolivia: depto. Santa Cruz; Serrania de Huanchaca, 45 km E Florida||L (0–1000 m)||Riparian thickets, gallery forest, cerrado||G. H. Rosenberg|
|Thamnophilus ruficapillus||RTB347 (UWBM)||Bolivia: depto. Santa Cruz; prov. Cordillera, El Tambo, 14 km SE Comarapa||LH (0–3050 m)||Riparian thickets, montane evergreen forest, semihumid and humid montane scrub||R. T. Brumfield|
|Thamnophilus schistaceus||B12559 (LSUMZ)||Bolivia: depto. Santa Cruz; Velasco; 50 km ESE Florida, Arroyo de Encanto||L (0–1100 m)||Tropical and tropical flooded lowland evergreen forest||C. G. Schmitt|
|Thamnophilus murinus||B9206 (USNM)||Guyana: Northwest District; Baramita||L (0–1000 m)||Tropical lowland evergreen forest||R. T. Brumfield|
|Thamnophilus aethiops||B14649 (LSUMZ)||Bolivia: depto. Santa Cruz; Serrania de Huanchaca, 21 km SE Catarata Arco Iris||LH (0–2000 m)||Tropical lowland evergreen forest||M. D. Cardeño|
|Thamnophilus aroyae||RTB395 (UWBM)||Bolivia: depto. Cochabamba; prov. Chapare, San Onofre, ca 43 km W Villa Tunari||H (600–1700 m)||Montane evergreen forest, secondary forest||R. T. Brumfield|
|Thamnophilus unicolor||B12144 (LSUMZ)||Ecuador: prov. Pichincha; Mindo||H (1200–2300 m)||Montane evergreen forest||J. Kennard|
|Thamnophilus caerulescens||395426 (FMNH)||Brazil: Sao Paulo; Boraceia||LH (0–2800 m)||Montane, tropical lowland evergreen, gallery and tropical deciduous forest||D. F. Stotz|
|Thamnophilus cryptoleucus||B7285 (LSUMZ)||Peru: depto. Loreto; Amazonas I. Pasto, 80 km NE Iquitos||L||River-edge and secondary forest||A. P. Capparella|
|Thamnophilus nigrocinereus||B20233 (LSUMZ)||Brazil: Amazonas; Munic. Novo Airao; Arquipelago das Anavilhanas||L||Flooded tropical evergreen, river-edge, and gallery forest||M. Cohn-Haft|
|Thamnophilus punctatus||B4172 (USNM)||Guyana: Berbice; West bank Dubulay ranch||L (0–1000 m)||Tropical lowland evergreen and secondary forest||C. M. Milensky|
|Thamnophilus stictocephalus||B13850 (LSUMZ)||Bolivia: depto. Santa Cruz; Serrania de Huanchaca, ca 45 km E Florida||L (0–700 m)||Tropical lowland evergreen and secondary forest||A. Castillo|
|Thamnophilus nigriceps||20238 (UAM)||Panama: prov. Panama, Lago Bayano||L (0–600 m)||Tropical lowland evergreen and secondary forest||M. J. Miller|
|Thamnophilus praecox||B3190 (ANSP)||Ecuador: prov. Sucumbios; Imuya Cocha||L||Flooded tropical evergreen forest||F. Sornoza|
|Thamnophilus amazonicus||B13045 (LSUMZ)||Bolivia: depto. Santa Cruz; Velasco, W bank Río Paucerna, 4 km upstream from Río Itenez||L||Tropical and flooded lowland evergreen, river-edge, and gallery forest||D. C. Schmitt|
|Thamnophilus insignis||B7486 (LSUMZ)||Venezuela: terr. Amazonas; Cerro de la Neblina camp VII||H (900–2000 m)||Montane evergreen and elfin forest||J. P. O'Neill|
|Thamnophilus divisorius||228 (PNSD)||Brazil: Acre, Munic. Mâncio Lima, Parque Nacional da Serra do Divisor||L (500 m)||Tropical lowland evergreen forest||B. M. Whitney|