The Basilinna genus (Aves: Trochilidae): an evaluation based on molecular evidence and implications for the genus Hylocharis

El género Basilinna (Aves: Trochilidae): una evaluación basada en evidencia molecular e implicaciones para el género Hylocharis

Blanca Estela Hernández-Baños^1*, Luz Estela Zamudio-Beltrán¹, Luis Enrique Eguiarte-Fruns², John Klicka³ and Jaime García-Moreno⁴

¹ Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México. Apartado postal 70-399, 04510 México, D. F., México. * behb@ciencias.unam.mx

³ Burke Museum of Natural History and Culture, University of Washington, Box 353010, Seattle, WA, USA.

⁴ Amphibian Survival Alliance, PO Box 20164, 1000 HD Amsterdam, The Netherlands.

Recibido: 11 febrero 2013
Aceptado: 18 febrero 2014

Abstract

Hummingbirds are one of the most diverse families of birds and the phylogenetic relationships within the group have recently begun to be studied with molecular data. Most of these studies have focused on the higher level classification within the family, and now it is necessary to study the relationships between and within genera using a similar approach. Here, we investigated the taxonomic status of the genus Hylocharis, a member of the Emeralds complex, whose relationships with other genera are unclear; we also investigated the existence of the Basilinna genus. We obtained sequences of mitochondrial (ND2: 537 bp) and nuclear genes (AK-5 intron: 535 bp, and c-mos: 572 bp) for 6 of the 8 currently recognized species and outgroups. Our analyses, using 3 different inference methods (Maximun Parsimony, Likelihood and Bayesian methods), corroborate the existence of the hummingbird genus Basilinna as composed of 2 species commonly assigned to the genus Hylocharis: leucotis and xantusii. Our study also supports that Hylocharis is a paraphyletic genus that includes species belonging to the genus Amazilia.

Key words: phylogenetic taxonomy, molecular phylogeny, Basilinna leucotis, Basilinna xantusii, hummingbirds.

Resumen

Los colibríes son una de las familias de aves más diversa y las relaciones filogenéticas dentro del grupo están empezando a entenderse mejor gracias a estudios con datos moleculares. La mayoría de esos estudios se ha enfocado a las relaciones filogenéticas de alto nivel dentro de la familia y ahora también es necesario estudiar las relaciones entre y dentro de los géneros con un enfoque semejante. En este estudio investigamos la situación taxonómica del género Hylocharis, miembro del complejo de las Esmeraldas, cuyas relaciones con otros géneros no están del todo claras; también investigamos la existencia del género Basilinna. Obtuvimos secuencias mitocondriales (ND2: 537 bp) y nucleares (intrón AK-5: 535 bp y c-mos: 572 bp) para 6 de las 8 especies actualmente reconocidas, así como para los grupos externos. Nuestros análisis, usando 3 métodos de inferencia distintos (máxima parsimonia, máxima verosimilitud e inferencia bayesiana), corroboran la existencia del género Basilinna conformado por 2 especies que actualmente se asignan al género Hylocharis: leucotis y xantussi. Nuestro estudio también sugiere que el género Hylocharis es parafilético e incluye especies asignadas al género Amazilia.

Palabras clave: taxonomía filogenética, filogenia molecular, Basilinna leucotis, Basilinna xantusii, colibríes.

Introduction

Hummingbirds are a clearly defined clade of birds whose internal relationships have only recently begun to be understood through a series of molecular studies (Bleiweiss et al., 1997; Bleiweiss, 1998a, b, c; Altshuler et al., 2004; McGuire et al., 2007). Most of these studies have focused on the higher level classification within the family, whereas studies focused on the relationships among and within genera are rather sparse. Inter and intra genera studies are important because phenotypic variation and distributional patterns suggest that the species limits are not always clear (Schuchmann, 1978, 1984, 1989, 1995, 1999; Schuchmann and Duffner, 1993; Schuchmann and Züchner, 1997). However, only a few genera have been studied in detail using molecular tools, such as Metallura (García-Moreno et al., 1999), Lampornis (García-Moreno et al., 2006), Cynanthus (García-Deras et al., 2008), Coeligena (Parra et al., 2009) and Adelomyia (Chaves and Smith, 2011).

Both DNA-DNA hybridization (Bleiweiss et al., 1997) and DNA sequencing (Altschuler et al., 2004; McGuire et al., 2007) point out to the same main clades within the family. The most basal node is an unresolved polytomy between Hermits (e.g., Eutoxeres, Glaucis, Threnetes and Phaethornis), non-Hermits, and a small clade formed by Topaza and Florisuga (McGuire et al., 2007). Within the non-Hermits there are 6 large groups originally identified by Bleiweiss et al. (1997) and later corroborated by DNA sequencing studies (Altschuler et al., 2004), with the Mangoes (e.g., Doryfera, Colibri, Anthracothorax) being the most basal of them. Brilliants (e.g., Heliodoxa, Boissonneaua, Coeligena, Aglaeactis, Eriocnemis, Haplophaedia) are the sister clade to Coquettes (e.g., Heliangelus, Sephanoides, Discosura, Lophornis, Aglaiocercus, Oreotrochilus, Lesbia, Chalcostigma, Metallura), and together they form a clade sister to Patagona, Emeralds, Bees, and Mountain Gems. The relationships among these latter groups are unresolved. Mountain gems (e.g., Lampornis, Heliomaster) are the sister group to Bees (e.g., Selasphorus, Calypte, Archilochus, Calliphlox), and the clade formed by these 2 is part of an unresolved polytomy with Patagona gigas and the Emeralds (e.g., Chlorostilbon, Campylopterus, Chalybura, Thalurania, Eupherusa, Elvira, Amazilia, Hylocharis). Moreover, addition of species to the larger DNA-sequence phylogeny has resulted in local topological changes in this part of the tree (compare figure 1 from Altschuler et al., 2004 with figure 2 from McGuire et al., 2007), but Mountain Gems in particular remain poorly sampled in the overall hummingbird phylogeny.

Ridgway (1911) proposed that H. leucotis and H. xantusii belong to a different genus, Basilinna, created by Boie in 1831. According to Ridgway (1911), Basilinna is "similar to Hylocharis, but wing relatively longer (3 times as long as exposed culmen) and style of coloration very different, the side of head with a broad white postocular streak and a black (male) or dusky (female) auricular stripe" (p. 377); those 2 characteristics (wing and white postocular stripe) are not present in the other species of the genus Hylocharis. More recently, Howell and Webb (1995) and Schuchmann (1999) resurrected this proposal. In a molecular study focused in the genus Lampornis, García-Moreno et al. (2006) also found evidence suggesting the existence of a clade formed by Basilinna leucotis and B. xantusii. This work included an analysis of mitochondrial DNA sequences from a broad sample of hummingbird species (100 species from 62 genera) and found several things relevant to the present study: the 3 species of Hylocharis included in the sampling scheme nested unambiguously within the Emerald group, and not with Lampornis as was suggested by Schuchmann (1999). Within this Emerald clade, Hylocharis did not form a monophyletic group: whereas H. leucotis and H. xantusii formed a well supported clade sister to Chlorostilbon, the third Hylocharis species was deeply nested in another clade together with Chrysuronia, Lepidopyga, Amazilia, Taphrospilus, and Elvira.

Here we evaluate the taxonomic status of H. leucotis and H. xantusii using data from mitochondrial and nuclear genes –both coding and non-coding– looking for further evidence for the existence of the Basilinna genus, as well as of its relationships with other genera (Lampornis and Hylocharis).

Materials and methods

Taxon sampling. Table 1 presents a full list of the taxa included in this study. We took advantage of many sequences already deposited in GeneBank and complemented these with our own generated DNA sequences. We obtained tissue samples from Hylocharis leucotis and H. xantusii, as well as selected species that could be related to these of the Emerald group (Amazilia candida and A. beryllina, Cynanthus, Chlorostilbon), Bee group (Selasphorus sasin, S. rufus, Doricha eliza, Calypte costae, C. anna, Atthis heloisa and Archilochus colubris) and Mountain Gem group (Lamprolaima rhami, Lampornis hemileucurus, L. cinereicauda, L amethystinus, Heliomaster constantii and Eugenes fulgens). We also included several other species of the genus Hylocharis: grayi, sapphirina, eliciae and cyanus, resulting in the broadest sampling of Hylocharis species in a molecular study as far as we know (Table 1) –though unfortunately the analysis of the genus is incomplete, as we lack samples of H. chrysura and H. humboldtii. We sequenced several other species of hummingbirds in order to have a well represented outgroup that included species from clades basal to the Emeralds according to the most current understanding of the Trochilidae phylogeny (Altshuler et al., 2004; McGuire et al., 2007). We restricted the outgroup to 4 genera: Adelomyia and Metallura from the coquettes group, and Aglaeactis and Urosticte from the brilliants group. Coquettes and brilliants form the sister clade to a group that comprises Patagona, emeralds, mountain gems, and bees (see Fig. 3 in McGuire et al., 2007).

DNA amplification and sequencing. We extracted DNA from tissue samples using the Qiagen DNeasy extraction kit, following the manufacturer's protocols. We amplified 3 DNA fragments of similar size of different regions and characteristics: the full length of a non coding intron (intron 5 of Adenylate kinase, or AK5), and partial sequences of 2 protein coding genes, 1 nuclear (proto-oncogen c-mos, intronless codes for a kinase) and 1 mitochondrial (NADH dehydrogenase subunit 2, or ND2). The 3 amplified fragments have comparable lengths: for ND2 we amplified and sequenced a fragment 537 base pairs (bp) long using the primers L5215 and H5766 (Sorenson et al., 1999); the intron, AK5, is 580 bp and was amplified using different combinations of the primers reported by Shapiro and Dumbacher (2001); and the nuclear coding gene c-mos has a length of 572 bp, and was amplified following the conditions reported by Cooper and Penny (1997). Nuclear fragments were only amplified and sequenced for a subset of samples that included H. leucotis and H. xantusii and related genera. Amplified products were cleaned by gel filtration using Sephadex G50 columns (Sigma), and sequenced using dye-labelled terminators (BigDye chemistry, Applied Biosystems). Sequencing reaction products were cleaned by gel filtration in the same way as PCR products, and resolved with an ABI 377 automated sequencer. All sequences generated for this study have been deposited in Genbank under accesion numbers from KM389474 to KM389529 (Table 1). Sequences were aligned and proofread using SeAl v. 2.0a11 (Rambaut, 2003) and ClustalX (Thompson et al., 1997). We corroborated the origin of all our sequences by combining at least 2 of the following methods: amplifying overlapping gene segments, amplifying or sequencing 1 region with different primer sets, sequencing both DNA strands for all amplified fragments, or using multiple individuals of a single species. We found no evidence of numt contamination of our mtDNA sequences (Bensasson et al., 2001; Sorenson and Quinn, 1998; Zhang and Hewitt, 1996), and we obtained congruent sequences of our nuclear genes that aligned well with sequences of other avian species –particularly with hummingbirds when available.

Data analyses. We conducted phylogenetic analysis using maximum parsimony (MP) and maximum likelihood (ML), with combined nuclear sequences (c-mos+AK5), separate genes (c-mos, AK5, ND2) and the 3 concatenate genes (c-mos+AK5+ND2). There is disagreement on whether the best approach for phylogenetic analyses is the combination of all existing information (total evidence) or the congruence between independent sets. We used both approaches by performing analyses of our individual gene fragments (independent sets) as well as a combination of all sequences. Moreover, because the taxon sampling varied somewhat between the different gene fragments, it was important to ensure through the analyses of each individual gene fragment that this taxon sampling did not bias our main conclusions. MP and ML analysis were performed using PAUP* (Swofford, 2002) unless otherwise stated. MP analyses used a heuristic search using a TBR branch-swapping option and with all positions equally weighted, support for each node was obtained by 1 000 bootstrap replicates (Felsenstein, 1985). We used jModeltest v. 0.1.1 (Posada, 2008) to evaluate the model parameters for the ML searches. The best fitting models for our combined sequences and for each gene were: c-mos+AK5, HKY+I+G; c-mos, TrN+I+G; AK5, HKY+G, and ND2, GTR+I+G. The ML analyses were performed using heuristic searches and nodal support was estimated via 1000 bootstrap replicates, with the gaps defined as missing data.

We performed Bayesian Inference (BI) on the combined nuclear sequences (AK5 and c-mos), the separate genes, and the 3 concatenate gene fragments. When using more than 1 fragment at a time we defined partitions corresponding to each fragment, and allowed for different evolutionary rates in each partition.. We used the model of evolution that best explained our data as estimated with jModeltest (see above). BI analyses were conducted using MrBayes 3.0 (Huelsenbeck and Ronquist, 2002). Each analysis consisted of 4 Markov chains, random starting trees, and uniform prior distribution of parameters. The chains were run for 10 million generations, sampling trees every 250th generation. The asymptote was determined visually, the first 1 000 trees were discarded as burn-in, and the remaining trees from the plateau phase were then used to estimate Bayesian posterior probabilities. We considered that clades were strongly supported if they were present in at least 95% of the sample trees (Huelsenbeck and Ronquist, 2002; Wilcox et al., 2002).

All trees obtained were rooted with the same species as outgroup (Adelomyia and Metallura from the coquettes group, and Aglaeactis and Urosticte from the brilliants group) as suggested by previous results (Bleiweiss, 1998a; Altshuler et al., 2004; García-Moreno et al., 2006; McGuire et al., 2007).

Results

Analysis of mitochondrial sequences using 3 different search strategies, maximun parsimony, maximun likelihood and bayesian inference, in all cases identified a well supported (≥ 95%) monophyletic clade integrated by H. leucotis and H. xantusii (Fig. 1a) distinct from other Hylocharis species which appear several nodes away, always nested within Amazilia. The clade formed by Hylocharis leucotis and H. xantusii is more closely related to the Cynanthus and Chlorostilbon clade, which in turn is the sister group of a large clade containing the rest of the emeralds and including the other Hylocharis species (Fig. 1a).

Analyses of both separated and concatenated sequences of the nuclear fragments also retrieved the H. leucotis - H. xantusii clade (Figs. 1b-d). The nuclear sequences do not resolve completely the relationships within the emeralds clade, nor the relationships between the bees and mountains gems groups. Nevertheless, the nuclear sequences also suggest that the H. leucotis-H. xantusii pair is not closely related to other Hylocharis species, as these always appeared nested within a clade that included the Amazilia species included in this study.

Besides the Basilinna clade, we recovered a well resolved relationship between Hylocharis species and different Amazilia species (Figs. 1a-d) (García-Moreno et al., 2006; McGuire et al., 2007).

The position of the H. leucotis-H. xantusii clade within the phylogeny is still unresolved. The pair came out as sister to a clade containing Cynanthus, Chlorostilbon and Chlorestes species in our analyses with ND2 sequences, but without sufficient support (< 95%). In the analyses with the AK5 intron the H. leucotis-H. xantusii clade is part of a polytomy between several well supported clades, whereas Chlorostilbon and Chlorestes are nested with some support (though not unambiguously) within a large complex that includes Campylopterus-Klais clade and a larger Elvira-Hylocharis-Amazilia. No sequences of Chlorostylbon or Campylopterus were available for an analysis with c-mos.

Discussion

Our results strongly suggest that the genus Hylocharis as currently understood is a paraphyletic group, as already suggested in the broad study of McGuire et al. (2007). We found this result using 3 genetic markers with different characteristics (an intron, AK5; a proto-oncogen, c-mos; and a mitochondrial protein coding gene, ND2), 3 different inference methods (maximum parsimony, maximum likelihood, and bayesian inference), and 6 of the 8 species that
the AOU recognizes in the genus (Remsen et al 2013).

Based on the results presented here and in García-Moreno et al. (2006), we suggest that the genus Basilinna be brought back into use. The use of the genus Basilinna has been supported recently by some authors (Howell and Webb, 1995; Schuchmann, 1999), but had never been properly defined from a phylogenetic perspective. In a study focused on the Mountain Gems of the genus Lampornis that included nuclear and mitochondrial DNA sequences, García-Moreno et al. (2006 –their Fig. 2) already found Basilinna as a well supported clade that fell within the Emerald group close to Chlorostilbon, while the other Hylocharis species included in that study, H. cyanus, also appeared deep within the Emerald clade and separated from H. leucotis and H. xantusii by several genera, a result that we are confirming in this more focused study.

Our results do not support Schuchmann's (1999) proposal, based in the shared presence of a broad white postocular stripe, that Basilinna is closely related to Lampornis. This character, however, can also be seen in Adelomyia melanogenys, a genus from the Coquettes clade and clearly different from Lampornis and Basilinna (McGuire et al., 2007). None of our results suggest a particularly close relationship between Lampornis and Basilinna. Analyses based on individual fragments did not have the power to resolve the deeper relationships between the different clades. Nevertheless, whereas the H. leucotis - H. xantusii group was unresolved with respect to other clades, in most analyses Lampornis came out close to Heliomaster, Eugenes, and Lamprolaima. We never recovered a topography implying a sister relationship between Lampornis and H. leucotis - H. xantusii. It is worth mentioning that although we were unable to amplify the same set of species for each gene fragment, this does not seem to affect the main conclusions of this work, namely the paraphyly of Amazilia and Hylocharis, the existence of a Basilinna clade, and the lack of a close relationship between Basilinna and Lampornis (Figs. 1, 2). Our total-evidence analysis, using the concatenated sequences of the 3 amplified DNA fragments, suggests a closer relationship of H. leucotis - H. xantusii with the Emeralds than with Lampornis. Ridgway (1911) provides a good description of the morphology and color patterns of the genus Basilinna and its 2 species, emphasizing differences with Hylocharis. In particular, the broad white postocular stripe present in H. leucotis and H. xantusii, but not in other members of Hylocharis, was one of the main characters leading Boie (1831) and Ridgway (1911) to propose the existence of Basilinna.

As for the other Hylocharis species, they appear in different places within the Emerald clade. Our hypothesis using all the available sequence information results in only 2 species forming part of the same clade, H. grayi and H. cyanus, which also includes Amazilia versicolor; whereas H. sapphirina and H. eliciae form 2 separate clades with other Amazilia species, namely and Amazilia chionogaster and A. candida respectively (Fig. 2). Although comparisons are not straightforward because the taxon sampling differs between the studies, in their more comprehensive phylogenetic study of hummingbirds McGuire et al. (2007) also found its 4 Hylocharis species – the same ones included in this study – interspersed within a clade rich in Amazilia species, with only 2 Hylocharis forming part of the same clade (H. eliciae and H. cyanus). Our results, together with those of other authors, indicate that a thorough revision of the genera Amazilia and Hylocharis, including other related genera (e.g., Chrysuronia, Lepidopyga), is necessary.

In conclusion, our results support the existence of a clearly defined clade formed by the 2 species of hummingbirds currently known as H. leucotis and H. xantusii, which other authors in the past have recognized as a genus on its own. We therefore propose the recognition of the genus Basilinna (Boie, 1831) encompassing 2 species: B. leucotis, distributed along the highlands of Mexico and Central America down to Nicaragua, and B. xantussi, restricted to the Baja California Peninsula in northwest Mexico. The results presented here also suggest that Hylocharis and Amazilia are currently paraphyletic groups
in need of a thorough revision (McGuire et al., 2007).

Acknowledgments

We thank Alejandro Gordillo Martínez, Fabiola Ramírez Corona and Raúl Iván Martínez Becerril for technical support. The manuscript was improved by the comments of C. Cordero. This research was supported by PAPIIT-Universidad Nacional Autónoma de México (IN-202509, IN225611) and Conacyt 00090774. The writing of this paper began when BEHB was on a sabbatical year at the American Museum of Natural History (New York) supported by Conacyt (grant 93731).

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