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Phylogenetic Relationships of the Madagascar Pygmy Kingfisher (Ispidina Madagascariensis)

Posted on: Tuesday, 20 December 2005, 06:00 CST

By Marks, Ben D; Willard, David E

ABSTRACT.-

The avifauna of Madagascar presents a complicated taxonomic and biogeographic problem. Although Madagascar was once connected to Africa, the birds of the island are not all of African origin. The Madagascar Pygmy Kingfisher (Ispidina madagascariensis) is sometimes placed in the African genus Ispidina and sometimes in the Southeast Asian genus Ceyx. We sequenced 755 base pairs of mitochondrial DNA from a fragment of the NADH dehydrogenase subunit II (ND2) and from the complete NADH dehydrogenase subunit III (ND3). We used these data to construct phylogenetic hypotheses for the Alcedinidae. Using these phylogenies, we evaluate previous hypotheses of relationships of I. madagascariensis. Although we cannot reject the hypothesis that I. madagascariensis is indeed a member of Ispidina, tree- building analyses support a relationship not with Ispidina or Ceyx, but instead with members of the African genus Corythornis. These data suggest that certain behaviors and plumage types have evolved several times in the Alcedinidae. Received 22 March 2004, accepted 27 April 2005.

Key words: Alcedinidae, Ceyx, Ispidina, Madagascar, phylogeny.

Relations Phylogntiques de Ispidina madagascariensis

RSUM. -L'avifaune malgache prsente un problme taxonomique et biogographique assez compliqu. Bien qu'il soit reconnu que Madagascar tait jadis connect au reste du continent africain, il est aussi clair que tous les oiseaux de l'le n'ont pas une origine africaine. Ispidina madagascariensis est tantt plac dans le genre africain Ispidina, tantt dans le genre asiatique Ceyx. Nous avons ralis le squenage de 755 paires de bases d'ADN mitochondrial provenant d'un fragment de la sous-unit II de la dshydrognase NADH (ND2) et la totalit de la sous-unit III de la dshydrognase NADH (ND3). Ces donnes ont t utilises pour reconstruire les hypothses phylogntiques des Alcedinidae. Nous avons valu les hypothses prcdentes propos des affinits du martin-pcheur Ispidina madagascariensis en utilisant ces phylognies. Bien que nous ne soyons pas en mesure de rejeter l'hypothse selon laquelle Ispidina madagascariensis est en ralit membre du genre Ispidina, l'analyse des arbres phylogntiques appuie l'existence d'une affinit non pas avec Ispidina ou Ceyx, mais plutt avec des membres d'un autre genre africain Corythornis. Ces donnes suggrent que certains comportements et types de plumage ont volu plusieurs fois chez les Alcedinidae.

THE ISLAND OF Madagascar is well known for the high degree of endemism of its flora and fauna. Madagascar split off from Africa ~165 mya and from the Indian subcontinent ~88 mya (Krause 2003). It now sits ~400 km off of the coast of Africa and ~4,000 km from India (Krause 2003). Although the island is close to Africa, the prevailing winds travel from east to west (Donque 1972), a counter against "easy" dispersal of birds from the mainland to Madagascar. Because of its current proximity to Africa and its tectonic history, Madagascar is an especially interesting case study for the biogeographic origins of its biota.

It has long been recognized that the Malagasy avifauna has relationships to the faunas of both Africa and Asia (Keith 1980). Malagasy birds span a spectrum, ranging from members of ancient endemic families (e.g. Cibois et al. 2001, Kirchman et al. 2001) whose closest relatives are yet to be determined, to species that move between Africa and Madagascar for breeding and wintering. Most nonendemic species of Malagasy birds are shared with Africa but not with Asia (e.g. Marsh Owl [Asia capensis], Namaqua Dove [Oena capensis], Madagascar Bee-eater [Merops superciliosus], and Wattled Starling [Creatophora cinerea]). Some endemic species, such as the Madagascar Malachite Kingfisher (Alcedo vintsioides), often treated as a subspecies of the African Malachite Kingfisher (A. cristata), also have clear connections to Africa. However, other species, such as the Madagascar Bulbul (Hypsipetes madagascariensis) and Madagascar Magpie-Robin (Copsychus albospecularis), are included in genera with Asian ranges. A full understanding of the biogeographic relationships of the Malagasy avifauna has been hampered by a lack of knowledge regarding the phylogenetic relationships of these species. For many genera that are shared among Africa, Asia, and Madagascar, no published studies have yet determined the closest relatives of the Malagasy form.

TABLE 1. Recent generic allocation of small African and Madagascar kingfishers.a

The Madagascar Pygmy Kingfisher (lspidina madagascariensis) is an example of a Madagascar endemic with uncertain affinities, and it has been treated taxonomically in a variety of ways over the past 50 years (Table 1). Delacour (1951) and Fry (1980) included it in the largely Asian genus Ceyx, along with the African Pygmy (I. picta) and Dwarf (Myioceyx lecontei) kingfishers, largely on the basis of bill shape and color. Traylor (1960) considered these characters convergent and placed I. madagascariensis in a broad African genus Corythornis, which included species otherwise treated in Alcedo, lspidina, and Myioceyx. Sibley and Monroe (1990) and Peters (1945) connected it to the small insectivorous African Pygmy Kingfisher (picta) in the genus lspidina, whereas Wolters (1976) placed it in a monotypic genus, Ceycoides.

Here, we investigate the phylogenetic relationships of the Madagascar Pygmy Kingfisher using sequences from the mitochondrial NADH dehydrogenase subunit II (ND2) and NADH dehydrogenase subunit III (ND3) genes. In the process, we hope to solve one piece of the much larger puzzle of Madagascar endemic bird relationships.

METHODS

Sibley and Monroe (1990) split the kingfishers into three families: Alcedinidae, Cerylidae, and Dacelonidae. We designed the taxon sampling here to allow us to investigate the generic placement of the Madagascar Pygmy Kingfisher as well as to assess generic limits of some other controversial groupings within the Alcedinidae. Following Sibley and Monroe (1990), we sampled 4 of the 11 species of Ceyx, 7 of 10 Alcedo species, and all 3 Ispidina species (including Myioceyx). Genera representing Cerylidae and Dacelonidae were included as outgroups to the Alcedinidae, as were several other Coraciiform species (Table 2).

We sequenced 755 base pairs (bp) of mitochondrial DNA (mtDNA) from two genes (complete ND3 and a fragment of ND2) from 1-6 individuals of each of the 28 study taxa using the primer sets L5215 and H5578 for ND2 (Hackett 1996) and L10755 and H11151 for ND3 (Chesser 1999). Sequences obtained using the ND2 primers were 362 bp long, and those obtained with the ND3 primers were 393 bp long. Total genomic DNA was extracted from muscle or toe pads using the reagents and protocols provided with the QIAamp Tissue Kit (Qiagen, Valencia, California). All polymerase chain reactions (PCR) followed the protocols outlined in Marks et al. (2002); automated sequencing protocols followed manufacturer recommendations (ABI Big Dye, version 2.0, Applied Biosystems, Foster, California) and were run on an ABI 377 automated DNA sequencer. We sequenced DNA in both directions and verified and aligned using SEQUENCHER (version 3.1.1, Gene Codes, Ann Arbor, Michigan). All of the mtDNA sequences collected for the study have been deposited in GenBank (accession numbers AY998882-AY998927 for ND2 sequences and AY998928-AY998974 for ND3 sequences).

TABLE 2. Taxon sampling and regional localities for specimens used in the study.

Phylogenetic analyses were conducted with PAUP* (version 4.0b4a; Swofford 2000) and MRBAYES (version 2.1; Huelsenbeck and Ronquist 2001). Prior to phylogenetic analysis, we used PAUP* to evaluate base composition of the ND2 and ND3 sequences for variability among taxa and among codon positions using a chi-square analysis of base frequencies across taxa, examining each codon position separately. We performed partition homogeneity tests (ILD statistic of Farris et al. 1994, 1995) to determine whether the two gene fragments could be combined in tree searches. All ILD tests were run excluding uninformative characters (Cunningham 1997), using a heuristic search with 10 random-addition replicates and tree bisection-reconnection (TBR) branch-swapping with 100 null-distribution replicates, and equal weights among characters. Barker and Lutzoni (2002) suggested that the ILD test can be misleading, resulting in false rejection of homogeneity across partitions and lacking power to detect certain types of heterogeneity. Therefore, we further assessed combinability of the two gene fragments by analyzing each fragment separately under a parsimony framework, looking for conflict between topologies at wellsupported nodes. Each individual gene analysis was run using the heuristic search option with 10 random-addition replicates and TBR branchswapping. Nodal support was assessed by nonparametric bootstrapping (100 pseudoreplicates, each with 10 random-addition replicates and TBR branch-swapping). After data exploration, parsimony tree searches with the combined data were run as described above.

Hierarchical likelihood ratio tests were run using MODELTEST (version 3.06; Posada and Crandall 1998) to choose the appropriate m\odel of evolution for maximum-likelihood (ML) and Bayesian analyses. Maximum-likelihood searches were performed using the heuristic search option with 10 random-addition replicates and TBR branch-swapping. We estimated support for nodes on the likelihood tree using Bayesian posterior probabilities derived from MRBAYES (Huelsenbeck and Ronquist 2001). Bayesian analysis was performed with the following settings. The ML model employed six substitution types, with base frequencies set to the empirically observed values. Rate variation across sites was modeled using a gamma distribution. The Markov chain Monte Carlo search was run with four chains for 3 10^sup 6^ generations, with trees being sampled every 1,000 generations (the first 500 trees were discarded as "burnin"). Posterior probabilities for individual clades were based on a 50% majority rule consensus tree of the remaining 2,500 trees (Fig. 2).

Alternative tree topologies were developed using MACCLADE (version 4.0; Maddison and Maddison 2000) and evaluated with the Shimodaira and Hasegawa (SH) test (Shimodaira and Hasegawa 1999). The SH test was used because of its conservative nature in comparison with the similar SOWH test that has been shown to be misleading at times (Buckley 2002). The SH tests were run with full approximation, 1,000 bootstrap replicates, and model of evolution identified by MODELTEST.

RESULTS

An alignment of 755 bp of partial ND2 (362 bp) and complete ND3 sequences (393 bp, including tRNA and spacers) was obtained for all taxa. Levels of uncorrected sequence divergence (P distance) were generally low within the taxa represented by multiple individuals (0- 0.6%), with the exception of /. madagascariensis. In this species, levels of divergence ranged from 0% to 1.4% between island localities. Homogeneity of base frequencies across taxa and codon positions could not be rejected for any comparison. All ILD tests failed to reject the null hypothesis of homogeneity between genes and codon partitions within genes, and there were no well-resolved nodes in conflict between separate analyses of the gene fragments.

Parsimony analysis of the combined data set resulted in 30 equally parsimonious trees (length 1,695, consistency index [CI] = 0.406, retention index [RI] = 0.652). Figure 1 shows the strict consensus of these trees with bootstrap support values from 100 replicates above the nodes. The Alcedinidae are supported as a monophyletic group. Within this clade, the species traditionally treated as Alcedo are not monophyletic. Alcedo cyanopecta is within the Ceyx clade, with a highly supported sister relationship to C. lepidus. The African A. quadribrachys, Eurasian A. atthis, and Southeast Asian A. meninting form a separate clade from the African leucogaster and cristata and the Malagasy vintsioides. Although weakly supported by bootstrap resampling, the Madagascar Pygmy Kingfisher is sister to these latter three species and not to Ceyx or Ispidina.

FIG. 1. Strict consensus tree of 30 equally parsimonious trees (length 1,695, CI = 0.406, RI = 0.652). Numbers above nodes are percentage of bootstrap replicates (H = 100) in which that branch was recovered. Branches with bootstrap percentages ≤70 are indicated by a thicker line.

The ML tree is topologically identical to the most probable Bayesian tree (Fig. 2). This tree defines many of the same clades as the parsimony tree, with the major topological difference being the placement of the clade containing A. quadribrachys, A, atthis, and A. meninting. In the Bayesian tree, this clade is sister to the Ceyx clade with weak Bayesian support; whereas in the maximum parsimony tree, it has unresolved sister relationships. Both trees support a sister relationship between I. madagascariensis and A. leucogaster, A. cristata, and A. vintsioides.

We compared the Bayesian topology with two alternate topologies using the SH test; one with madagascariensis sister to Ceyx, and another with madagascariensis united with Ispidina. The phylogenetic hypothesis uniting madagascariensis with Ceyx was rejected (P = 0.01; Table 3). However, although nearly significant, we could not reject the hypothesis uniting madagascariensis with Ispidina (P = 0.06).

DISCUSSION

Phylogenetic analysis of the ND2 and ND3 sequences suggests that the Madagascar Pygmy Kingfisher is most closely related to the African species A. leucogaster and A. cristata and the Malagasy A. vintsioides, and not to species within Ceyx or Ispidina. These three species (leucogaster, cristata, and vintsioides) have been placed in the genus Corythornis by some authors (Table 1), or as a subgenus within Alcedo (Peters 1945). Traylor (1960) suggested that madagascariensis be placed in Corythornis, but recommended that /. picta and /. (Myioceyx) lecontei be included as well. Although he was less certain about including the latter two species in Corythornis, he was convinced, correctly, that none of these taxa should be lumped with either Ceyx or Alcedo. Our data support some of Traylor's (1960) conclusions. Although the SH test fails to reject the hypothesis uniting madagascariensis with Ispidina, Bayesian analysis strongly indicated a sister relationship between madagascariensis and A. leucogaster, A. cristata, and A. vintsioides (Fig. 2) and that the two Ispidina species are more distantly related to this group.

TABLE 3. Results from SH test of alternate tree topologies.

These data can be applied to some other taxonomic problems within the Alcedinidae, many of whose relationships remain obscure. Most authors recognize the genera Ceyx and Alcedo, but there is little agreement on their boundaries. Our data suggest that the Asian taxa C. erithacus, C. rufidorsum, C. lepidus, and C. melanurus belong in Ceyx and that cyanopecius, which Sib ley and Monroe (1990) moved to Alcedo, also should be included in Ceyx. Alcedo meninting, A. atthis, and A. quadribrachys should remain in Alcedo. Alcedo cristata, A. vintsioides, and A. leucogaster should be removed from Alcedo and placed in Corythornis; and madagascariensis, the sister taxon to these three, could either be included in Corythornis or placed in the resurrected monotypic genus Ceycoides as Wolters (1976) suggested.

The Madagascar Pygmy Kingfisher shares the rufous coloration of its upper parts with only two other Alcedinidae, both clearly members of Ceyx (rufidorsum and melanurus). Whereas the other members of Corythornis are all associated with water and feed primarily on aquatic life, madagascariensis is a forest bird, more like lspidina. Our results suggest that these plumage types and behaviors have evolved several times within the Alcedinidae.

Among the terrestrial vertebrates of Madagascar, biogeographic origins remain an interesting and, in many cases, unresolved issue. One family of frogs appears to have African relationships, a second is likely sister to an Asian family, and the third may not be monophyletic (Glaw and Vences 2003). Raxworthy (2003) states that no Malagasy reptile group has a well-supported phylogeny supporting sister relationships with any Asian group, but questions of over- water dispersal versus Gondwanan breakup relics have yet to be answered. Among mammals, the carnivores (Yoder et al. 2003), primates (Yoder et al. 1996), and tenrecs (Oison and Goodman 2003) all have fairly well-established African connections, but endemic rodent origins (Jansa et al. 1999, Jansa and Carleton 2003) remain unresolved.

FIG. 2. Results of Bayesian analysis of the complete data set. Shown is the 50% majority rule consensus of 2,500 trees. Nodes with Bayesian support of <0.95 are indicated by a thicker line.

Our results show that the Madagascar Pygmy Kingfisher is most closely related to African taxa. Unfortunately, because there have been so few studies directed at determining the origins of the Madagascar avifauna, it is far too early to make generalizations about the avifauna as a whole. Prum (1993) concluded that the endemic family of asities and sunbird-asities (Philepittidae) is embedded in the broadbill family (Eurylaimidae) and sister to the African genus Pseudocalyptomena. The Madagascar Swamp Warbler (Acrocephalus newtoni) has been shown to have African relationships (Leisler et al. 1997, Helbig and Seibold 1999). The Madagascar Wagtail (Motacilla flaviventris) is sister to the African M. clara and M. capensis (Voelker 2002). The foudies (ιaudio) appear to be closest to the African genera Euplectes and Quelea (Craig 1999). On the other hand, Payne (1997) suggested that the endemic cuckoo genus Coua is closest to Asian cuckoos in the subfamily Phaenicophaeinae. Craig (1999) leaves open the possibility of an Asian origin for Malagasy Ploceus. Three species, the bulbul Hypsipetes madagascariensis, the thrush Copsychus albospecularis, and the starling Hartlaubius auratus (often included in Saroglossa) are all in Asian genera, but as Schulenberg (2003) points out, their relationships "should be confirmed rather than assumed." The origins of the two impressive radiations of Malagasy passerines, the Malagasy warblers and the Vangidae, while showing some indications of African origin, are still unresolved pending more complete taxon sampling (Cibois et al. 2001, Yamagishi et al. 2001, Fuchs et al. 2004). Beyond these, there is a litany of Malagasy species, some in endemic genera and some in genera shared with both Africa and Asia, whose closest relatives are yet to be determined. These include (not exhaustively) species in the genera Alectroenas, Streptopelia, Coracopsis, Centropus, Otus, Caprimulgus, Mirafra, Coradna, Monticola, Nesillas, Randia, Cisticola, Terpsiphone, Nectarinia, Zosterops, Lonchura, and Dicrurus. With the recent explosion of interest in Madagascar, we are aware of ongoing studies addressing phylogenies of many of these taxa, and as these studies are finished, we expect a more complete picture to emerge.

ACKNOWLEDGMENTS

We greatly a\ppreciate the field efforts of S. Goodman and M. J. Raherilalao, who collected many of the samples used in this study. We thank the Ministere des Eaux et Forets in Madagascar, the Ghana Wildlife Division, and the Uganda Wildlife Authority and Forestry Department for permission to collect and export the specimens. M. Traylor provided the inspiration for this study. We thank F. Sheldon and D. Dittmann for allowing access to samples in the Genetic Resources collection at the LSUMNS. We are grateful to C. Kahindo for providing the translation of the abstract, as well as to R. Moyle, M. Cohn-Haft, J. Weckstein, S. Hackett, J. Bates, T. Schulenberg, and F. Sheldon for their helpful comments on the manuscript.

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Associate Editor: R. C. Fleischer

BEN D. MARKS1,3 AND DAVID E. WILLARD2

1 Musenm of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA: and

2 Bird Division, The Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA

3 E-mail: bmarks5@lsu.edu

Copyright American Ornithologists' Union Oct 2005

Source: Auk, The

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