Evolutionary differentiation in the Neotropical montane region: Molecular phylogenetics and phylogeography of Buarremon brush-finches (Aves, Emberizidae)

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Abstract

Studies on Neotropical phylogeography have largely focused on lowland organisms. Because lowland and highland biotas have different histories and are likely affected by different processes influencing population differentiation, understanding Neotropical diversification requires detailed studies on montane taxa. We present the most comprehensive analysis of population differentiation conducted so far on a widespread group of Neotropical montane organisms, focusing on the evolutionary relationships and phylogeography of Buarremon brush-finches (Aves: Emberizidae) in montane areas from Mexico through Argentina. Sequences of mitochondrial and nuclear genes demonstrate that Buarremon is not monophyletic with respect to Arremon and Lysurus. Genetic structure revealed by mtDNA is strong in both B. brunneinucha and B. torquatus. Gene genealogies and nucleotide diversity indicate that B. brunneinucha originated in Mexico and later expanded to South America, where it followed one colonization route through the east, and one through the west of the continent. Differentiation among populations of B. torquatus was substantial, reaching 8% uncorrected sequence divergence within South America. Relationships among major lineages of B. torquatus were not fully resolved owing to rapid differentiation, but the occurrence of closely related taxa in distant locations suggests a complex history of diversification. Some Colombian populations of B. brunneinucha have affinities with populations from Venezuela and the East Andean slope of Ecuador and Peru, and others with those from the Pacific slope of Ecuador. Moreover, five divergent lineages of B. torquatus occur within Colombia, highlighting the importance of dense sampling in northwest South America for studies on diversification of widespread Neotropical lineages.

Introduction

The recent development of comprehensive phylogeographic studies of various groups of organisms has led to important insights on the history of diversification in the Neotropical region that improve our understanding of the genetic structure of populations, the timing of population differentiation, the relationships among areas of endemism, and the role of features of the landscape such as rivers, mountains, or geological arcs as barriers to gene flow (reviewed by Moritz et al., 2000; see also Aleixo, 2004, Cheviron et al., 2005, Dick et al., 2003, Dick et al., 2004, Marks et al., 2002, Ribas and Miyaki, 2006, Ribas et al., 2006, Weigt et al., 2005). Much of this work, however, has focused on lineages occurring in the Neotropical lowlands.

A recent review of avian molecular phylogenies has highlighted apparent differences in the history of diversification between lowland and highland Neotropical regions (Weir, 2006). In contrast to lowland areas, where fauna-wide diversification rates appeared to be highest in the late Miocene and to have decreased towards the present, rates of species production in highland areas appeared to increase substantially following the onset of Pleistocene glacial cycles. Therefore, Weir (2006) concluded that lineages occurring in lowland and highland regions were likely affected differently by Pleistocene climatic fluctuations and other recent events. Although some of the results of this analysis may be compromised by the influence of taxonomic practice (i.e. lowland lineages are likely undersplit by taxonomists in comparison to highland lineages; Bates and Demos, 2001; see also Chek et al., 2003), they imply that generalizations concerning population differentiation in the lowlands (e.g. strong genetic structuring and Pre-Pleistocene population differentiation in birds) may not reflect the extent and timing of population differentiation in montane areas. Indeed, different types of historical events influence differentiation in highland and lowland populations. For example, because many Neotropical montane bird species extend over broad latitudinal expanses within narrow elevational ranges along the Andes (Graves, 1985, Graves, 1988), their populations are susceptible to fragmentation resulting from local extinctions, particularly when climate change reduces suitable habitat (Graves, 1988). Accordingly, we expect montane species to exhibit strong genetic structure along a latitudinal axis, a hypothesis that remains untested. Likewise, low passes and inter-mountain valleys should present strong barriers to genetic exchange for high-elevation species, but empirical evidence documenting these genetic effects is largely lacking for Neotropical organisms (see Bowie et al., 2006 for an example from Africa). In addition, although some studies have identified montane areas of endemism (e.g. Cracraft, 1985), phylogenetic and phylogeographic studies addressing relationships among areas over broad scales are scarce. In sum, because few comprehensive phylogeographic studies of Neotropical montane taxa have been conducted, and because most of those available have focused on relatively narrow geographic regions, our current understanding of historical diversification in the Neotropical highlands is incomplete.

In this study, we present a detailed assessment of evolutionary relationships and patterns of genetic differentiation in Buarremon brush-finches (Aves, Passeriformes, Emberizidae). Because taxa in this group are widely distributed in montane areas of the New World from Mexico through Argentina, a thorough analysis of population differentiation in Buarremon represents an important step in understanding diversification in the Neotropical highlands.

The genus Buarremon includes three species: B. torquatus, which ranges from central Costa Rica to northern Argentina, B. brunneinucha, occurring from central Mexico to southern Peru, and B. virenticeps, endemic to western and central Mexico (American Ornithologists’ Union, 1998; Remsen et al., 2006). Both B. torquatus and B. brunneinucha were originally described in the genus Embernagra, but they were placed in Buarremon by Bonaparte (1850), who, without a clear rationale, erected the genus including these two taxa and several other species of emberizines, most of which are now placed in the genus Atlapetes. Buarremon virenticeps was described a few years later, also by Bonaparte (1855). Based on similarities in bill shape, Hellmayr (1938) merged Buarremon with Atlapetes, a treatment followed without question by all subsequent authors until mtDNA and allozyme evidence indicated that Buarremon (i.e. B. brunneinucha and B. torquatus) and Atlapetes are not each other’s closest relatives (Hackett, 1992). This prompted the resurrection of Buarremon for brunneinucha, torquatus, and virenticeps, now widely accepted (Remsen and Graves, 1995; American Ornithologists’ Union, 1998; Remsen et al., 2006). Ongoing studies with broad taxon sampling support this rearrangement, and suggest that together with the genera Arremon and Lysurus, the three species of Buarremon form one of six major clades within the Emberizidae (J. Klicka et al., unpubl. data). However, relationships among these three genera are uncertain, and the long-held assumption of the monophyly of Buarremon has not been rigorously tested.

At a lower level, relationships among Buarremon taxa are not well established. Based on the morphological similarity between juvenile B. torquatus and adult B. virenticeps, Paynter (1970) considered these taxa to be conspecific, but later regarded them as distinct sister species (Paynter, 1978), which has been the more common position of systematists notwithstanding the lack of a phylogenetic appraisal. Species delimitation has been contentious within what is currently treated as B. torquatus (Remsen and Graves, 1995). Different authors have argued this taxon may comprise as many as three species, yet there is disagreement over how these should be circumscribed, partly as a result of the phenotypic diversity of the group, which consists of 14 subspecies among which plumage characters vary rather chaotically, with no clear correspondence between geographic proximity and phenotypic similarity (Chapman, 1923, Paynter, 1978). There has also been some discussion regarding species limits in B. brunneinucha, with some authors favoring the treatment of the Mexican subspecies apertus as a separate species (Navarro-Sigüenza and Peterson, 2004).

Here, we first reconstruct phylogenetic relationships among Buarremon and related genera, among species of Buarremon, and among lineages of each species occurring in different regions based on sequences of mitochondrial and nuclear genes. Guided by this framework, we use mtDNA data to examine the relationships of population lineages in more detail, to describe the geographic distribution of genetic variation, and to assess the extent of migration between populations separated by potential barriers to gene flow. To our knowledge, this study represents the most comprehensive analysis of population genetic differentiation conducted for a widespread group of Neotropical montane organisms. In addition to furthering our general understanding of the history of diversification in the tropical and subtropical mountains of Central and South America, our results provide a framework for forthcoming studies on the evolution of phenotypic diversity, species limits, and the role of interspecific interactions in the origin of elevational distributions in Buarremon and allies (Cadena, 2006, Cadena, 2007).

Section snippets

Taxon and geographic sampling

We followed different taxon sampling and DNA sequencing strategies to reconstruct evolutionary relationships and to examine patterns of population differentiation at various hierarchical levels. We generated sequence data for 238 samples, including 138 individuals representing eight of the nine subspecies of B. brunneinucha, 78 representing 13 of the 14 subspecies of B. torquatus, eight B. virenticeps, and one for each of four species of Arremon, the two species of Lysurus, and outgroups in the

Phylogenetics—mitochondrial data

Mitochondrial data support the monophyly of Arremon and Lysurus, but suggest that Buarremon is not monophyletic (Fig. 2). Results obtained using different methods of phylogenetic inference were congruent with each other except for a few nodes that were not strongly supported in any analysis. All analyses placed Arremon as sister to B. torquatus, a result strongly supported by Bayesian analyses (0.96 posterior probability), but less so by maximum-likelihood (64% bootstrap), or parsimony (53%

Phylogenetics

The monophyly of Buarremon is dubious. Although support for relationships among major groups of Buarremon, Arremon, and Lysurus was variable in analyses using different methods (e.g. Bayesian vs. parsimony) and employing different data (mitochondrial vs. nuclear), the most telling fact is that we never recovered a monophyletic Buarremon in any analysis of mitochondrial, nuclear, or combined data. Indeed, an exclusive clade formed by B. torquatus, B. brunneinucha, and B. virenticeps was not

Acknowledgments

We thank G. Spellman and J. DaCosta for assistance with laboratory work, and J. D. Palacio (Instituto Alexander von Humboldt) and M. Linares (Universidad de los Andes), who allowed access to laboratories in Colombia. J. Pérez-Emán provided help on various fronts through the development of this study. For help in the field or for collecting samples at our request, we thank A.M. Cuervo, C. Devenish, O. Laverde, G. Barrantes, J.C. De las Casas, P. Pulgarín, J.L. Parra, and G. Servat. For logistic

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