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Defining the phylogeographic relationship between cis- and trans-Andean populations of Dendrocincla fuliginosa and Xenops minutus in Colombia

Enrique Arbeláez-Cortés *

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Grupo de Estudios en Biodiversidad, Escuela de Biología, Facultad de Ciencias, Universidad Industrial de Santander, Carrera 27 Calle 9, Bucaramanga, Santander, Colombia

*Corresponding author: enriquearbelaez@gmail.com (E. Arbeláez-Cortés)

Abstract

Due to the position of Colombia between Central and South America, and the presence of several ecosystems in its territory, phylogeographic information from populations across this country is fundamental to understand the evolutionary history of widespread Neotropical species. The Andes have long been noted for their influence isolating lowland species into cis- and trans-Andean populations. However, detailed sampling across cis-Andean zones adjacent to the Andes (i.e., Orinoquia) has been lacking in avian phylogeographic studies. Information from DNA sequences, from 2 passerine birds: Dendrocincla fuliginosa and Xenops minutus is presented herein; to depict their phylogeographic patterns, focusing on the relationship between cis- and trans-Andean populations from Colombia. The analyses, regarding Colombian samples indicated that cis-Andean populations (i.e., Orinoquia and Amazon) are not closely related, rather the Orinoquia populations are more closely related to trans-Andean populations in both species. These relationships suggest that populations on both sides of the Andes were connected in the recent past (less than 1 myA). I propose that phylogeographic differentiation in lowland species in this region is not only explained by the presence of the Andean mountains, but also based on the ecological shifts between major ecosystems such as Amazonia and Orinoquia.

Keywords: Amazonia; Birds; Orinoquia; Lowlands; mtDNA; nDNA; South America

© 2020 Universidad Nacional Autónoma de México, Instituto de Biología. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Definiendo las relaciones filogeográficas entre poblaciones cis- y trans-andinas de Dendrocincla fuliginosa y Xenops minutus en Colombia

Resumen

Por su posición entre Centroamérica y Sudamérica, y por presentar varios ecosistemas, la información filogeográfica de poblaciones de Colombia es fundamental para entender la historia evolutiva de especies neotropicales ampliamente distribuidas. Los Andes se consideran como factor de separación de especies de tierras bajas en poblaciones cis- y trans-andinas. Pero un muestreo detallado de zonas cis-andinas adyacentes a los Andes (i.e., Orinoquia) ha estado ausente de los estudios filogeográficos con aves. Se presenta aquí información de secuencias de ADN de 2 aves paseriformes: Dendrocincla fuliginosa y Xenops minutus, para describir sus patrones filogeográficos, enfocando dicha información en la relación entre poblaciones cis- y trans-andinas en Colombia. Los análisis indican que poblaciones cis-andinas (i.e., Orinoquía y Amazonía) no están estrechamente relacionadas entre sí, sino que las poblaciones de la Orinoquía están más relacionadas con poblaciones trans-andinas en ambas especies. Estas relaciones sugieren que las poblaciones en ambos lados de los Andes estuvieron conectadas en el pasado reciente (menos de 1 MA). Se propone que la diferenciación filogeográfica en especies de tierras bajas en esta región no puede explicarse solo por la presencia de las montañas andinas, sino también con base en cambios ecológicos entre ecosistemas mayores como la Amazonía y la Orinoquía.

Palabras clave: Amazonía; Aves; Orinoquía; Tierras bajas; ADNmt; ADNn; Sudamérica

© 2020 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo Open Access bajo la licencia CC BY-NC-ND

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Phylogeographic studies of widespread lowland Neotropical birds usually have indicated a strong genetic differentiation among allopatric populations (Cheviron et al., 2005; Fernandes et al., 2014; Harvey & Brumfield, 2015; Marks et al., 2002; Miller et al., 2008; Nyári, 2007; Rheindt et al., 2009). For lowland species, these studies have usually considered the Andes mountains as a barrier to gene flow between populations to the West (trans-Andean) and to the East (cis-Andean). For species such as Automolus ochrolaemus, A. subulatus (Schultz et al., 2017), Hylophylax naevius/ H. naevioides (Fernandes et al., 2014), Lepidothrix coronata (Cheviron et al., 2005), and Myiopagis viridicata (Rheindt et al., 2009), a clear phylogeographic differentiation between cis- and trans-Andean populations has been found. However, other species such as Glyphorynchus spirurus (Marks et al., 2002), Schiffornis turdina (Nyári, 2007), and Mionectes oleagineus (Miller et al., 2008), exhibit a lower degree of genetic differentiation between trans- and cis-Andean populations. Therefore, recent dispersion (or population connection) across (or around) the Andes, originally proposed by Haffer (1967), has been considered to explain such phylogeographic relationships between cis- and trans-Andean populations. Results of these single-species studies, agree with those studies including several lowland bird species (Smith, Harvey et al., 2014; Smith, McCormack et al., 2014), indicating that phylogeographic relationships among populations in Neotropical lowlands are complex. Connection across the Andes as a cause underlying the actual patterns of species distributions has also been analyzed using geographic models of potential ranges of bird species, and there is evidence of historic ecological continuity across low-lying passes that could promote population connectivity between cis- and trans-Andean regions (Cadena et al., 2016).

Despite advances in the knowledge of the evolution of lowland Neotropical birds, phylogeographic patterns of these lineages have been derived mainly from information from Mexico, Central America, and Brazil; but a gap often exists in phylogeographic information from Colombia. Given the geographic location of Colombia between Central and South America, their complex landscape, and the dynamic history of their environment (Cadena et al., 2007, 2016; Flantua et al., 2007; Haffer, 1967; Nores, 2004); more taxon and geographic sampling across this country is crucial to reconstruct the evolutionary history of Neotropical organisms (Avendaño et al., 2017). To test if Colombian populations adhere to the established cis/trans Andean dichotomy, phylogeographic patterns of 2 widespread lowland species that range on both sides of the Andes and inhabit forests were analyzed: Dendrocincla fuliginosa and Xenops minutus (Furnariidae).

Dendrocincla fuliginosa (Vieillot, 1818) ranges from southeastern Honduras to eastern Brazil, mainly below 1,300 m asl, but occasionally up to 2,000 m asl. This species inhabits humid and savanna forests in lowlands and foothills, generally in mature forests, but it also tolerates secondary vegetation and plantations. Dendrocincla fuliginosa forages for invertebrates and small vertebrates on vertical trunks at low- and mid-levels, usually alone but also follows ant swarms (as facultative) and mixed-species flocks (Del Hoyo et al., 2003; Restall et al., 2006). This species comprises 11 subspecies; 4 of which occur in Colombia (Gill & Donsker, 2018). Molecular information indicated that the diversification of D. fuliginosa began around 4 myA (Derryberry et al., 2011; Weir & Price, 2011).

Materials and methods

Eighteen tissue samples of D. fuliginosa (17 localities from 8 Colombian departments) and 13 tissue samples of X. minutus (12 localities from 9 Colombian departments), covering their main distribution ranges in Colombia (Appendix 1) were used. DNA was isolated from frozen tissues using Qiagen DNeasyTM kit (Qiagen Inc., Valencia, CA, USA), following the manufacturer protocol. I amplified the mitochondrial (mtDNA) gene subunit 2 of the nicotinamide adenine dinucleotide dehydrogenase (ND2), using primers H1056U and L5215U (H. Vázquez-Miranda in litt.) and the nuclear (nDNA) locus 20454 using primers 20454F and 20454R (Backström et al., 2008). All PCR trials were performed in a final volume of 15 μl, containing 1x PCR buffer, 1.5 mM MgCl2, 0.2 mM each dNTP, 0.4-0.5 μM each primer, 1-2 unit DNA polymerase, and around 50-100 ng of DNA. PCR conditions were the same used for those loci in Arbeláez-Cortés et al. (2014).

PCR products were purified using Exo-SAP-ITTM (GE Healthcare Bio-Sciences Corp. Piscataway, NJ, USA), and the sequences were obtained by ABI Prism BigdyeTM v3.1 (Qiagen Inc., Valencia, CA, USA) terminator chemistry in an ABI 3730XL automated sequencer located in an overseas facility (University of Washington, USA). All PCR products were exported from Colombia under the respective permission of Colombian authorities (see Acknowledgments). Sequences were edited and manually aligned using BioEdit (Hall, 1999). For sequences of nDNA, I inspected chromatograms to detect double peaks, which were edited by coding them following a standard IUPAC ambiguity code. Double peaks were scanned across all individuals to check for accuracy and consistency in their identification. The allele phase of the nDNA locus was resolved using a coalescent-based Bayesian method of the Phase algorithm (Stephens & Donnelly, 2003; Stephens et al., 2001) in DNAsp v.5 (Librado & Rozas, 2009) employing default settings. The resulting highest-probability haplotypes for further analyses were used. All sequences are deposited in GenBank (MN486096-MN486154).

For the mtDNA locus ND2, additional sequences of other countries from GenBank were obtained. For D. fuliginosa, 17 sequences from Brazil, 3 from Suriname, 2 from Peru, 2 from Venezuela, 2 from Panama, 1 from Ecuador, and 1 from Trinidad and Tobago were obtained (Claramunt et al., 2010; Naka et al., 2012; Weir et al., 2009). For X. minutus, 21 sequences were obtained from Guyana, 10 from Belize, 9 from Panama, 8 from Brazil, 2 from Venezuela, 1 from Ecuador, and 1 from Paraguay (Derryberry et al., 2011; Naka et al., 2012, M.J. Miller, 2008 unpublished). For each of these GenBank sequences, I obtained the geographical information available either from: their metadata, the database of the biological collection which harbors the sample, the supplementary material of the cited papers, or from other papers in which several of these individuals have been included (C.W. Burney, 2009 unpublished; Smith et al., 2014). Only GenBank sequences for which there was at least country information were included. I georeferenced localities without information using GeoNames (GeoNames, 2013) or Google Earth (Google, 2010). In the cases where only the information for the country or state was available, I used central geographic coordinates to depict their position on a map only for illustrative purposes. I included ND2 sequences from closest congeneric species, Xenops rutilans and Dendrocincla anabantina (Derryberry et al., 2011) as outgroups. A list of samples with GenBank accession numbers is provided in appendix 1. Because the size of the sequences obtained and the ones available from GenBank varied, I trimmed the ND2 alignments to 625 bp, for D. fuliginosa, and to 622 bp for X. minutus. For the nDNA locus 20454 I aligned 285 bp for D. fuliginosa and 381 bp for X. minutus. However, full sequences were deposited in GenBank.

It should be noted that Weir and Price (2011) indicated that D. fuliginosa is paraphyletic. These authors found that the eastern South American populations are distantly related from the western populations. For this reason, I analyzed both the whole set of sequences available for D. fuliginosa and a subset from its western range, but I focus my results and discussion on the latter. Here, I refer to these populations as D. fuliginosa, even though the information in Weir and Price (2011) indicates that they can be considered under a different name.

BEAST version 1.7.4 (Drummond et al., 2012; Drummond et al., 2012) was used to reconstruct phylogenetic relationships among ND2 haplotypes. The best-fit model for each alignment was selected using Akaike’s information criterion in Modeltest, version 3.7 (Posada & Crandall, 1998). I ran BEAST for 200,000,000 steps, sampling every 2,000 steps, using a Yule speciation tree prior, a UPGMA starting tree, and a strict molecular clock with a mutation rate of 2.9 × 10-8 substitutions ⁄ site ⁄ year for ND2 according to rates previously reported in passerine birds (Lerner et al., 2011). After this analysis, TreeAnnotator, version 1.7.4 (Rambaut & Drummond, 2012) was used to generate a tree file with 25% burn-in and a posterior probability limit of 0.5. Sequences of the nDNA locus, available just for Colombia, were examined using Network (Bandelt et al., 1999) to generate an allele network depicting their relationships.

I acknowledge that the estimates of time trees depend on the selected substitution rate for the loci. For instance, looking broadly for externally calibrated rate estimates of the ND2 rate in birds, one finds variation ranging from 1.94% to 12.3% per my (Arbogast et al., 2006; Benham et al., 2015; Fuchs et al., 2011; Johnson & Weckstein, 2011; Patel et al., 2011; Weir & Schluter, 2008). However, my principal aim is to depict the phylogeographic pattern of both species in northwestern South America and not to detail divergence times among clades. The only temporal issue discussed here is the differentiation between cis-Andean (Orinoquia) and trans-Andean populations for both species to compare it with information on the Andes orogenic formation. Because the substitution rate I used is towards the low end of estimated rates for birds it would lead to ancient dates.

Xenops minutus (Sparrman, 1788) ranges from southern Mexico to southeastern South America (below 1,000 m asl, but locally up to 1,500 m asl), and inhabits tropical lowland forests where it forages for arthropods, usually alone or in mixed-species flocks, climbing along branches and woody vines in low- to mid-level vegetation (Del Hoyo et al., 2003; Restall et al., 2006). This species comprises 10 subspecies; 5 of which occur in Colombia (Gill & Donsker, 2018). Molecular information suggests that the split of X. minutus from its sister species occurred around 10 myA (Derryberry et al., 2011). Harvey & Brumfield (2015) used genome-wide single nucleotide polymorphisms to investigate the phylogeography of this taxon, and found the presence of at least 3 deeply divergent clades that seem to represent different species.

For both species, the Andes have been considered as a barrier involved in their diversification (Harvey & Brumfield, 2015; Weir & Price, 2011), but these studies lack Colombian samples. Smith et al. (2014) included Colombian samples of Xenops minutus and D. fuliginosa in a phylogeographic study, but analyzed general patterns across multiple species. The aim here is to depict the phylogeographic patterns of both species, focusing on defining relationships among cis- and trans-Andean populations from Colombia.

Results

I gathered new mtDNA sequences (ND2) of 29 individuals of D. fuliginosa and X. minutus from Colombia, which I combined along with 82 sequences, publically available, from other regions (Appendix 1). mtDNA phylogeographic structure were found in both species across their ranges (Fig. 1). The 20454 nDNA locus, examined only for Colombian samples, presented different alleles on both species, and geographic structure seems to be present in X. minutus but not in D. fuliginosa (Fig. 1). The phylogenetic trees indicated that there are 6 mtDNA lineages for X. minutus and 4 mtDNA lineages for D. fuliginosa (Fig. 1).

The 4 D. fuliginosa mtDNA lineages exhibited phylogeographic structure (Fig. 1). In addition to the differentiated lineage from eastern South America, a widespread mtDNA lineage was found including the Amazonian individuals from Brazil, Venezuela, Colombia, Ecuador, and Peru. This Amazonian lineage was sister to the clade including 2 sister lineages, one of these includes the Colombian individuals from the Orinoquia and 1 individual from Trinidad and Tobago, while the trans-Andean individuals from Colombia and Panama comprised the other lineage. The Orinoquian individuals (cis-Andean) were sister to the trans-Andean lineage, rather than with the Amazon (cis-Andean) lineage. The network representation of nDNA alleles (Fig. 1) did not show such structure. However, only the most common allele of the 20454 nDNA locus was shared by individuals from the 3 mtDNA lineages, while the other 6 alleles were exclusive of different mtDNA lineages (Fig. 1). Besides these general patterns in D. fuliginosa, it is also notable that the trans-Andean individuals showed geographic differences in their mtDNA haplotypes. For instance, Colombian inter Andean valley’s individuals did not share haplotypes with Caribbean individuals, and these Caribbean individuals in spite to be close to Panama individuals harbor a different haplotype (Fig. 1).

The 6 X. minutus mtDNA lineages also exhibited phylogeographic structure (Fig. 1). One individual from Paraguay (not depicted in the map in figure 1) and 5 individuals from the Amazon in Brazil (but without locality information) comprise a clade with posterior probability (pp) = 0.66 that is sister to the poorly supported clade (pp = 0.34) including the remaining individuals. One mtDNA lineage including individuals from Venezuela, Brazil, and Guyana appeared as sister (pp = 0.81) to a lineage including individuals from Colombian Amazon. On the other hand, the lineage with individuals from Belize is a sister to a lineage including individuals from Panama, western Ecuador, Colombia (trans-Andean and Orinoquia), and northwestern Venezuela. Colombian individuals from Orinoquia (cis-Andean) are again clustered with trans-Andean individuals and not with the other cis-Andean individuals from the Amazon. This result for X. minutus is paralleled by the Network analysis of the nDNA (Fig. 1) that showed that individuals from the Orinoquia (cis-Andean) shared alleles with other Colombian trans-Andean individuals, while individuals from the Colombian Amazon (cis-Andean) not share alleles with the remaining Colombian individuals. As in the case of D. fuliginosa, the trans-Andean individuals of X. minutus also showed geographic differences in their haplotypes. The Belize haplotypes were well differentiated, while the Ecuador, Panama, and Colombia individuals did not share haplotypes among them. In addition, Colombian individuals from the inter-Andean valleys harbor 1 haplotype that is different from those found in the Caribbean Colombian individuals.

The BEAST analysis (Fig. 1) indicated that divergence of mtDNA lineages in D. fuliginosa began approximately 0.5 my (95% HPD between 266,000 and 608,000 years ago), while divergence of lineages in X. minutus was older, beginning approximately 1.5 my (95% HPD between 1.17 and 1.9 myA). Haplotypes within each mtDNA lineage of D. fuliginosa appear to have coalesced during the last 150,000 years, whereas the mtDNA lineages of X. minutus coalesced during the last 370,000 years. Regarding the Colombian haplogroups, the lineage of D. fuliginosa in the Orinoquia diverged from its sister trans–Andean lineage approximately 300,000 years ago, and both of them diverged from the Amazon lineage around 400,000 years ago (Fig. 1). In the case of X. minutus, the divergence of the 2 lineages present in Colombia occurred probably more than 1 million years ago, but the alleles comprising a clade for the Orinoquia (Andean) and trans-Andean samples likely coalesced less than 1 my.

Figure 1. Phylogeography of D. fuligionosa and X minutus. Left, phylogenetic reconstruction of the mtDNA (ND2) dataset in BEAST, depicting posterior probabilities (pp) for nodes with values larger than 0.75. The 95% high posterior density calculated for divergence times are presented as error bars for some nodes of interest. Right, and allele network of the nDNA (locus 20454) for Colombian individuals. In the tips of the trees (among brackets) are indicated the IAvH-CT numbers for Colombian samples and the number of sequences used for the other countries. The inset maps depicts the range of each major haplogroup (circles with same color as in the phylogenetic reconstruction and allele network), and elevations above 1,500 m are in dark grey.

Discussion

Molecular information for X. minutus and D. fuliginosa was analyzed, and I agree with other authors (e.g., Avendaño et al., 2017; Cadena et al., 2007) in considering the inclusion of samples from Colombia as necessary to draw conclusions about recent biological diversification in the Neotropics, which was the focus of this paper for 2 species of passerine birds. Both species exhibited phylogeographic structure in their whole geographic distribution, suggesting the occurrence of historic processes (i.e., vicariance) separating their populations. Regarding Colombian samples both species show a clear separation of individuals from the Amazon (cis-Andean), while individuals from the Orinoquia (cis-Andean) and the trans-Andean lowlands are more related. These patterns agree with the biogeographic regionalization of the Neotropics which indicates that the Orinoquia and trans–Andean lowlands conform a biogeographic dominion, which is different from the Amazon (Morrone, 2014), but contrast with the idea of the Andes as a barrier for lowland species.

The uplift of the Andes as a process associated with differentiation between Orinoquia (Andean) and trans-Andean populations of D. fuliginosa and X. minutus can be ruled out because such mountains reached their actual elevation in Colombia 2.7 myA (Gregory-Wodzicki, 2000), while populations of D. fuliginosa and X. minutus on both sides probably diverged less than 0.5 myA (95% HPD between 450,000 – 175,000 years ago for D. fuliginosa, and less than 250,000 years ago for X. minutus). However, I do not discard the presence of the Andes as related to genetic differentiation, in the sense that its mountains have facilitated isolation of populations that were connected recently (a possible scenario for D. fuliginosa) or have promoted differentiation in the trans-Andean zone followed by dispersal over (or around) these mountains (a possible scenario for X. minutus). Another possible scenario for X. minutus is that their populations in the Orinoquia and the trans-Andean populations have been connected throughout their history because they are part of the same mtDNA lineage.

Close relationships between Orinoquia and trans–Andean lowlands have been also revealed by biogeographical and ecological analyses of other animal taxa (Lozano-Zambrano & Fernández, 2007; Sigrist & Carvalho, 2009). Similarly, this relationship between cis- and trans-Andean populations has been found in other phylogeographic studies. For instance, in monkey species (Lynch et al., 2015) and another bird (Chrysomus icterocephalus, Cadena et al., 2011). Weir & Price (2011) also noted the recent separation of D. fuliginosa ridgwayi (trans-Andean) from D. f. meruloides (cis–Andean). Several additional works have found sister relationships between populations in Central America or Choco, and populations in Amazonia (e.g., Marks et al., 2002; Miller et al., 2008; Nyári, 2007; Rheindt et al., 2009), but they did not include Colombian samples that I show here are key to a complete understanding of these lineages’ phylogeographic patterns.

Close phylogeographic relationships between cis– and trans-Andean populations are not new for vertebrates (Lynch et al., 2015; Nyári, 2007). However, another result is more novel. I found that the major phylogeographic break for D. fuliginosa and X. minutus in Colombia is between Orinoquia and Amazonia (both cis-Andean regions), and not among cis- and trans-Andean populations. This phylogeographic break (Amazon/Orinoquia) has been also found in monkeys (Lagothrix lagotricha, Botero et al., 2015), and is a noteworthy result, suggesting that ecological differences between Orinoquia and Amazon could be involved in maintaining genetic isolation, which is in line with Brumfield (2012) who considers a secondary role of barriers in the Neotropics in structuring variation that arose elsewhere, and that could be in secondary contact (in this case) in the border between Amazon and Orinoquia. An alternative explanation for this phylogeographic pattern is to consider a major role for the ecological shifts between Orinoquia and Amazonia as the reason for genetic differentiation in these species. Whatever the explanation (either as a zone of division or as a zone of contact); the Amazon/Orinoquia transition must be considered as a necessary factor to explain genetic differentiation in widespread lowland taxa in the Neotropics.

In spite of the large genomic information used by Harvey and Brumfield (2015), which allowed understand several issues of the history of X. minutus, the lack of Colombian individuals in their analyses made impossible to appreciate that individuals from Orinoquia (cis-Andean) and from the trans-Andean zone are included in the same lineage. However, Harvey and Brumfield (2015) found evidence of migration from the Amazon into the trans-Andean populations. The close relationship of cis- and trans-Andean populations of birds inhabiting forests suggests that lowlands on both sides of the Andes in northwestern South America have (or recently had) a connection. This observation agrees with the scenario proposed by Haffer (1967), who considered that during glacial periods of the Pleistocene, the climate in northern Colombia was more humid, and then these lowlands were forest-covered much more extensively than they are at present, which provided a broad connection between cis- and trans-Andean lowland forests. This effect was increased by a lower sea level (about 100 m), which promoted the emergence of a large area of land in northern South America (Haffer, 1967; Nores, 2004). For Ateles E. Arbeláez-Cortés / Revista Mexicana de Biodiversidad 91 (2020): e912984 7 https://doi.org/10.22201/ib.20078706e.2020.91.2984

monkeys, this scenario has been considered to explain their distribution in cis– and trans-Andean zones (Lynch et al., 2015). However, a northern connection between cis– and trans-Andean regions is not the only way supported by analyses of species ranges in lowland species (Cadena et al., 2016). In addition, Avendaño et al. (2013) presented evidence of recent crossings of cis-Andean bird species into the trans-Andean lowlands, apparently promoted by human modifications to the landscape, suggesting that ecological changes could facilitate the interchange of some species between both zones.

Considering only the trans-Andean samples, the differences in their mtDNA haplotypes are noteworthy, particularly these observed between the inter-Andean valleys and the Caribbean Colombian populations that probably occurred during the last 250,000 years. This result parallels the result for C. icterocephalus that also shows different haplotypes between the Magdalena valley and the Caribbean lowlands (Cadena et al., 2011), but contrasts with the lack of genetic structure found in the monkey Ateles hybridus and other bird species in this same area (Link et al., 2015; Sandoval et al., 2017). Differences found in the 2 species analyzed here could be explained by historic processes of isolation among trans-Andean populations due to climatic fluctuations. For instance, the repeated change of dry and wet climatic periods during the Pleistocene (Haffer, 1967) and fluctuations in sea level in the Caribbean coastal zone (Nores, 2004) could be related to population isolation in trans-Andean lowlands, thus allowing the origin of the genetic patterns observed. Further phylogeographic studies are warranted to depict detailed phylogeographic patterns in this zone and to test the role of these paleoclimatic processes in the genetic differentiation of populations.

It is also noteworthy that trans-Andean samples show genetic differences which contrast with an apparent lack of genetic differences among Amazonian samples. For instance, western Amazonian individuals clustered together, despite that they are widespread and represent localities in 2 or more endemism areas (Cracraft, 1985). Colombian individuals of both species, in this study, from the Napo and Imeri endemism areas shared haplotypes, indicating that these areas are not separable based on the molecular information. For D. fuliginosa individuals from Venezuela (Guiana area of endemism) and Peru (Inambari) harbor haplotypes like the ones found in the Colombian Amazon (Imerí and Napo). These results suggest a more active (and recent) genetic differentiation in the trans-Andean lowlands than in the Amazon.

The Colombian Orinoquia (cis-Andean) and Caribbean (trans-Andean) are 2 gaps in biodiversity knowledge (Arbeláez-Cortés, 2013). The Caribbean and the inter-Andean valleys in Colombia have undergone major anthropogenic changes in their landscapes (Armenteras et al., 2011; Etter et al., 2006), while the Orinoquia is undergoing significant changes in its natural ecosystems (Armenteras et al., 2005; Romero-Ruiz et al., 2012). Therefore, it is urgent to better understand the biodiversity in these zones to have scientific support for its conservation. Further works should test if the close phylogeographic relationship between trans-Andean and Orinoquia (cis-Andean) populations regarding the Amazon (cis-Andean) populations is a generality for birds and other taxa. If such pattern is common, then the genetic differences among populations in this region of the Neotropics will not be explained only by the presence of Andean mountains or large rivers, but also by the ecological shift between ecosystems such as those represented by Amazonia and Orinoquia or by an historical barrier to gene flow between ecosystems that has shifted.

Acknowledgments

This work was supported by the Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Colombia, under funds allocated to Colecciones Biológicas; and by the Vicerrectoría de Investigación y extensión of Universidad Industrial de Santander, Colombia under grant “Proyecto de investigación capital semilla 2300”. I also thank the family Arbeláez-Cortés and A. G. Navarro-Sigüenza for their support. L. A. Sánchez González, N. Trujillo-Arias, and two anonymous reviewers made valuable comments and corrections that improved this work. A special acknowledgment to the specimen and tissue collectors of the material used in this study. Samples were exported to sequencing overseas under: “Permiso para la exportación de especímenes de la diversidad biológica no listados en los apéndices de la convención CITES número 385 de 2014 de la Autoridad Nacional de Licencias Ambientales, Colombia”.

Appendix 1. List of individuals of D. fuliginosa and X. minutus with GenBank accession numbers and locality information for samples and sequences included in this work. Source of the sequences information is indicated.

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

D. fuliginosa

STRI TR-DFU1

GU215371

Trinidad and Tobago

Arima

Simla Research Station

Weir et al. (2009)

D. fuliginosa

IAvH-CT 4900, IAvH-A 13106

MN486096 / MN486131

Colombia

Sucre

San Onofre

Corregimiento La Barce, Santuario de Fauna y Flora El Corchal El Mono Hernandez

This study

D. fuliginosa

IAvH-CT 13108, IAvH-A 15248

MN486112 / MN486143

Colombia

Sucre

Toluviejo

Corregimiento El Cañito, Monte de Los Navas

This study

D. fuliginosa

IAvH-CT 12935, IAvH-A 15075

MN486102 / MN486141

Colombia

Sucre

Colosó

Estación Primatologica, Montes de María

This study

D. fuliginosa

IAvH-CT 12997

/ MN486142

Colombia

Sucre

This study

D. fuliginosa

STRI JTW253

GU215373

Panama

Bocas del Toro

Valle de Risco

Not locality information-Valle de Risco

Weir et al. (2009)

D. fuliginosa

STRI JTW744

GU215374

Panama

Darien

Puerto Piña

Not locality information-Puerto Piña

Weir et al. (2009)

D. fuliginosa

IAvH-CT 10744, IAvH-A 14722

MN486109 / MN486139

Colombia

Arauca

Arauquita

Extracciòn de Arenas Remolinos, Rìo Arauca

This study

D. fuliginosa

IAvH-CT 10812, IAvH-A 14795

MN486107 / MN486140

Colombia

Arauca

Arauquita

Plataforma Cosecha G

This study

D. fuliginosa

AMNH 11848

JQ445335

Venezuela

Bolivar

Cerro Guaiquinima

Naka et al. (2012)

D. fuliginosa

IAvH-CT 4696, IAvH-A 13282

MN486098 / MN486130

Colombia

Caldas

Vereda La Miel

This study

D. fuliginosa

IAvH-CT 6840, IAvH-A 14175

MN486110 / MN486133

Colombia

Casanare

Pore

Corregimiento Altamira, Vereda Altamira La Esperanza

This study

D. fuliginosa

IAvH-CT 6784, IAvH-A 14146

MN486104 / MN486132

Colombia

Cundinamarca

Puerto Salgar

Not locality information-Puerto Salgar

This study

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

D. fuliginosa

FMNH FM391298

GU215370

Brazil

Amapá

Not locality information-Amapá

Weir et al. (2009)

D. fuliginosa

FMNH 391303

JQ445317

Brazil

Amapá

Not locality information-Amapá

Naka et al. (2012)

D. fuliginosa

IAvH-CT 382, IAvH-A 11047

MN486099 / MN486126

Colombia

Caquetá

Parque Nacional Natural Serranía de Chiribiquete, Río Mesay

This study

D. fuliginosa

INPA A1940

JQ445330

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A650

JQ445327

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A1230

JQ445333

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A1165

JQ445331

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A694

JQ445328

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A1220

JQ445323

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A2007

JQ445321

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A1596

JQ445320

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

INPA A1938

JQ445319

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

D. fuliginosa

IAvH-CT 596, IAvH-A 11276

MN486105 / MN486127

Colombia

Caquetá

Parque Nacional Natural Serranía de Chiribiquete Río Sararamano, afluente del río Messay

This study

D. fuliginosa

STRI EC-DFU1

GU215372

Ecuador

Napo

Jatun Sacha

Not locality information-Jatun Sacha

Weir et al. (2009)

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

D. fuliginosa

IAvH-CT 10585, IAvH-A 14562

MN486111 / MN486138

Colombia

Amazonas

Leticia

Reserva Forestal Rio Calderon, Estacion Biologica El Zafire

This study

D. fuliginosa

LSUMZ B6895

JQ445325

Peru

Loreto

Not locality information-Loreto

Naka et al. (2012)

D. fuliginosa

LSUMZ B2723

JQ445326

Peru

Loreto

Not locality information-Loreto

Naka et al. (2012)

X. minutus

UAM 24522; ABJ415

FJ175798

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller, 2008 unpublished document

X. minutus

UAM ABJ428

FJ175799

Belize

Not locality information-Belize

M.J. Miller (2008) unpublished document

X. minutus

UAM ABJ622

FJ175800

Belize

Not locality information-Belize

M.J. Miller (2008) unpublished document

X. minutus

UAM ABJ607

FJ175801

Belize

Not locality information-Belize

M.J. Miller (2008) unpublished document

X. minutus

UAM 24355; ABJ294

FJ175802

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

X. minutus

UAM 24347; ABJ266

FJ175803

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

X. minutus

UAM 14330; KSW3706

FJ175804

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

X. minutus

UAM 24348; ABJ270

FJ175805

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

X. minutus

UAM 24357; ABJ296

FJ175806

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

X. minutus

UAM 24356; ABJ295

FJ175807

Belize

Toledo District

Not locality information-Toledo District

M.J. Miller (2008) unpublished document

X. minutus

IAvH-CT 13109, IAvH-A 15249

MN486118 / MN486154

Colombia

Sucre

Toluviejo

Corregimiento El Cañito, Monte de Los Navas

This study

X. minutus

IAvH-CT 12980, IAvH-A 15120

MN486123 / MN486153

Colombia

Sucre

Colosó

Estación Primatologica, Montes de María

This study

X. minutus

UAM 20495; MJM410

FJ175809

Panama

Panama

Cerro Azul: ANAM Station

M.J. Miller (2008) unpublished document

X. minutus

UAM KSW4392

FJ175810

Panama

Not locality information-Panama

M.J. Miller (2008) unpublished document

X. minutus

UAM 20492; MJM407

FJ175812

Panama

Not locality information-Panama

M.J. Miller (2008) unpublished document

X. minutus

UAM MJM1462

FJ175814

Panama

Not locality information-Panama

M.J. Miller (2008) unpublished document

X. minutus

UAM 22105; MJM675

FJ175815

Panama

Panama

Not locality information-Cerro Azul: ANAM Station

M.J. Miller (2008) unpublished document

X. minutus

UAM 22110

FJ175816

Panama

Panama

Not locality information-Cerro Azul: ANAM Station

M.J. Miller (2008) unpublished document

X. minutus

UAM 20338; MJM244

FJ175808

Panama

Cocle

Molejon, Finca Moreno

M.J. Miller (2008) unpublished document

X. minutus

UAM 20326; MJM232

FJ175811

Panama

Cocle

Molejon, Finca Moreno

M.J. Miller (2008) unpublished document

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

X. minutus

UAM 20350

FJ175813

Panama

Cocle

Molejon, Finca Moreno

Molejon, Finca Moreno

M.J. Miller (2008) unpublished document

X. minutus

USNM 14628

JQ445992

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

AMNH DOT11942

JQ445967

Venezuela

Bolivar

Not locality information-Bolivar

Naka et al. (2012)

X. minutus

USNM 9164

JQ445982

Guyana

Northwest

Not locality information-Northwest

Naka et al. (2012)

X. minutus

USNM 9333

JQ445983

Guyana

Northwest

Not locality information-Northwest

Naka et al. (2012)

X. minutus

IAvH-CT 84, IAvH-A 10842

MN486114 /

Colombia

Norte de Santander

Toledo

Vereda El Diamante Río Negro Parque Nacional Natural Tamá

This study

X. minutus

IAvH-CT 2178

MN486113

Colombia

Antioquia

Amalfi

Vereda Las Animas, Bosque Las Animas, Cuenca de la quebrada Las Animas

This study

X. minutus

USNM 14183

JQ445989

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 14260

JQ445990

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 4266

JQ445979

Guyana

Berbice

Not locality information-Berbice

Naka et al. (2012)

X. minutus

USNM 4331

JQ445980

Guyana

Berbice

Not locality information-Berbice

Naka et al. (2012)

X. minutus

IAvH-CT 4719, IAvH-A 13305

MN486115 / MN486146

Colombia

Caldas

Vereda La Miel

This study

X. minutus

IAvH-CT 6829, IAvH-A 14164

MN486117 / MN486147

Colombia

Casanare

Pore

Vereda Altamira, La Esperanza

This study

X. minutus

USNM 5132

JQ445981

Guyana

Essequibo

Not locality information-Essequibo

Naka et al. (2012)

X. minutus

IAvH-CT 8687, IAvH-A 12848

MN486124 / MN486150

Colombia

Vichada

Cumaribo

Corregimineto Santa Rita, Parque Nacional Natural El Tuparro, Bosque de Guaipé

This study

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

X. minutus

USNM 15759

JQ445993

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 14525

JQ445991

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

LSUMZ B48433

JQ445975

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

LSUMZ B48452

JQ445976

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

LSUMZ B48478

JQ445977

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

UKNHM 1225

JQ445973

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

UKNHM 1276

JQ445974

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

IAvH-CT 8100, IAvH-A 14317

MN486121 / MN486148

Colombia

Vichada

Cumaribo

Selva de Mataven,Caño Cajaro

This study

X. minutus

IAvH-CT 8152, IAvH-A 14370

MN486125 / MN486149

Colombia

Vichada

Cumaribo

Selva de Mataven,Caño Matavén

This study

X. minutus

IAvH-CT 10817, IAvH-A 14208

MN486116 / MN486152

Colombia

Cundinamarca

Anapoima

Club campestre Mesa de Yeguas

This study

X. minutus

ANSP 7407

JQ445968

Guyana

Potaro-Siparuni

Not locality information-Potaro-Siparuni

Naka et al. (2012)

X. minutus

INPA A1709

JQ445972

Brazil

Roraima

Not locality information-Roraima

Naka et al. (2012)

X. minutus

USNM 12223

JQ445987

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 12772

JQ445988

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

AMNH:DOT8845

JF975328

Venezuela

Amazonas

Not locality information-Amazonas

Derryberry et al. (2011)

X. minutus

FMNH 391346

JQ445969

Brazil

Amapá

Not locality information-Amapá

Naka et al. (2012)

X. minutus

USNM 11810

JQ445986

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 10412

JQ445984

Guyana

Not locality information-Guyana

Naka et al. (2012)

X. minutus

USNM 10887

JQ445985

Guyana

North West

Not locality information-Northwest

Naka et al. (2012)

Taxon

Collection number

GenBank number: ND2 / 20454

Country

Department or State

County

Locality

Source

X. minutus

IAvH-CT 793, IAvH-A 11395

MN486119 / MN486145

Colombia

Caquetá

San José de Fragua

Corregimiento La Esmeralda

This study

X. minutus

LSUMZ:B11948

JF975329

Ecuador

Esmeraldas

El Placer

Not locality information-El Placer

Derryberry et al. (2011)

X. minutus

IAvH-CT 378, IAvH-A 11043

MN486120 / MN486144

Colombia

Caquetá

Parque Nacional Natural Serranía de Chiribiquete, Río Mesay

This study

X. minutus

AMZ 118 (MPEG 59473)

JQ445964

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

AMZ 119 (MPEG 59474)

JQ445965

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

AMZ 325 (MPEG 59475)

JQ445966

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

INPA A71

JQ445970

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

INPA A1610

JQ445971

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

JAP 662 (MPEG 62739)

JQ445978

Brazil

Amazonas

Not locality information-Amazonas

Naka et al. (2012)

X. minutus

IAvH-CT 10616, IAvH-A 14593

MN486122 / MN486151

Colombia

Amazonas

Leticia

Reserva Forestal Rio Calderon, Estacion Biologica El Zafire

This study

X. minutus

LSUMZ:B25938

JF975330

Paraguay

Caaguaz

Not locality information-Caaguaz

Derryberry et al. (2011)

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Vol. 91, 2020: enero Genetic diversity of the Common Black Hawk (Buteogallus anthracinus) population in Los Tuxtlas, Mexico, based on microsatellite markers

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