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Three New Species of Stiphrornis \(Aves: Muscicapidae\) from the Afro

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Three New Species of Stiphrornis \(Aves: Muscicapidae\) from the Afro Systematics and Biodiversity (2017), 15(2): 87–104 Research Article Three new species of Stiphrornis (Aves: Muscicapidae) from the Afro- tropics, with a molecular phylogenetic assessment of the genus GARY VOELKER1, MICHAEL TOBLER2, HEATHER L. PRESTRIDGE1, ELZA DUIJM3, DICK GROENENBERG3, MARK R. HUTCHINSON1, ALYSSA D. MARTIN1, ALINE NIEMAN3, CEES S. ROSELAAR4 & JERRY W. HUNTLEY1 1Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843, USA 2Division of Biology, Kansas State University, Manhattan, KS 66506, USA 3Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, the Netherlands 4Naturalis Biodiversity Center, Vertebrate Department, PO Box 9517, 2300 RA Leiden, the Netherlands (Received 22 April 2016; accepted 7 August 2016; published online 28 September 2016) We describe three new species of forest robin in the genus Stiphrornis; two from West Africa and one from the Congo Basin. Each species represents a distinct phylogenetic lineage based on genetic analysis. In addition to genetic differentiation, each new species is diagnosable from other Stiphrornis lineages by morphology, and by plumage. One of the new species appears to be restricted to the Central and Brong-Ahafo Regions of Ghana, and another is restricted to Benin and the Central Region of Ghana. In Ghana, these two new species presumably come into contact with Stiphrornis erythrothorax (Western Region of Ghana and westward), and there is evidence that one of the new species has a distinguishably different song from erythrothorax. The distribution of the third new species is primarily on the south bank of the Congo River, near the city of Kisangani. Recognition of these species provides additional evidence that Afrotropical forests are harbouring substantial cryptic diversity, and that our knowledge of the drivers of this diversity remains poorly documented across the region. http://www.zoobank.org/urn:lsid:zoobank.org:pub:BF2A0BE6-1140-4EFF-9035-380D61AB03AE Key words: Africa, cryptic species, speciation, systematics, tropical forests Introduction Congo Basin are relatively old (1970s and earlier) and lack associated tissue samples (but see Beresford & Cra- The Afrotropical lowland forests of West Africa and the craft, 1999; Schmidt, Foster, Angehr, Durrant, & Congo Basin harbour a substantial and diverse avifauna Fleischer, 2008). (see Sinclair & Ryan, 2010). Many species that comprise The general lack of collecting in Afrotropical lowland this avifauna have minimal, or lack completely, intra-spe- forests is likely inhibiting the potential discovery of new cific plumage variation (Mayr & O’Hara, 1986). As such, species, although several have been described in recent there has been comparatively little research done to deter- years. For example, there have been two Forest Robin mine whether a given lowland forest species harbours (Stiphrornis) species discovered in the last 15 years (Beres- genetic variation or exhibits phylogeographic patterns. ford & Cracraft, 1999; Schmidt et al., 2008). While the This dearth of genetic analyses (as compared to the better- five described Forest Robin species (erythrothorax, gabo- studied avifauna of the Eastern Arc Mountains of Africa) nensis, pyrrholaemus, sanghensis, xanthogaster)arepheno- has been exacerbated by a general lack of well-preserved typically rather similar, even the recently described taxa DNA for genetic analysis. While work in Liberia, Sierra should not be considered cryptic, as all taxa show clear dif- Leone and Ghana in the last few decades has produced a ferences in genetics, song and plumage colour. This suggests limited number of voucher specimens with associated pre- that a lack of sampling in the region, rather than a lack of served tissue samples, most avian collections from the obvious variation alone, is a contributing issue in fully docu- menting avian biodiversity in lowland forests. Correspondence to: Gary Voelker. E-mail: [email protected] ISSN 1477-2000 print / 1478-0933 online This article was originally published with errors. Please see Corrigendum ( http://dx.doi.org/10.1080/14772000.2016.1246134) Ó The Trustees of the Natural History Museum, London 2016. All Rights Reserved. http://dx.doi.org/10.1080/14772000.2016.1226978 88 G. Voelker et al. Additionally, and despite a lack of obvious variations in Materials and methods plumage in many species distributed in them, it is becom- Phylogenetic relationships and lineage dating ing clear that the Afrotropical forests may indeed harbour substantial genetic variation that may warrant the recogni- In our analyses, we included representatives from all five tion of conservation units or new species. For example, the currently described Stiphrornis lineages (erythrothorax, monomorphic Green Hylia (Hylia prasina) is comprised of gabonensis, pyrrholaemus, sanghensis,andxanthogaster); five highly divergent phylogroups distributed across Afro- these lineages are varyingly recognized as races of erythro- tropical areas of endemism (Marks, 2010). Similar exam- thorax (e.g., Collar, 2005; Sinclair & Ryan, 2010)oras ples of genetic variation are evident in Red-tailed Bristle- species (e.g., Beresford & Cracraft, 1999;Boano,Vinals, bill (Bleda syndactyla), Fire-crested Alethe (Alethe casta- Durante, & Pavia, 2015; Schmidt et al., 2008). Whole nea), Pale-breasted Illadopsis (Illadopsis rufipennis)and genomic DNA was extracted from tissue using the DNeasy Eastern Forest Robins (Stiphrornis xanthogaster), where tissue extraction kit (Qiagen), from a total of 70 Stiphror- each presumptively monotypic species shows significant nis. We used polymerase chain reactions (PCR) to amplify genetic variation between sampling points distributed the mitochondrial cytochrome-b (cyt-b) and NADH dehy- across the Congo River (Voelker et al., 2013). drogenase subunit 2 (ND2) genes for all 70 samples using As part of our on-going efforts to explore the genetic previously published primers and protocols (Outlaw, and geographic variation of African birds we had the Voelker, & Outlaw, 2007). For a limited subset of samples D opportunity to conduct museum-based scientific collecting (n 38) which included representatives of all species, we in both Benin and the Democratic Republic of the Congo. also sequenced the nuclear FGB intron-5 (Fib 5) gene fol- In 2010, G.V. and J.W.H., along with T.J. Hibbitts, con- lowing published protocols (Schmidt et al., 2008). Auto- ducted collections-based fieldwork in Benin. This survey mated sequencing was performed with BigDye v3.1 included several days in the Lama Forest, a 16,250 ha (Applied Biosystems) and products were run out on an patch of semi-evergreen Guineo-Congolian (lowland) rain ABI PRISM 3730x sequencer. We used SEQUENCHER, forest (White, 1983) surrounded by exotic forests (e.g., version4.7(GeneCodes)toalignupto1025basepairs Eucalyptus) and agriculture, c. 80 km north of Cotonou. (bp) of cyt-b, 1018 bp of ND2 and 541 bp of FIB5. Importantly, this forest sits in the Dahomey gap, an area Sequence data are deposited in GenBank, and relevant of low rainfall that separates the otherwise broadly distrib- accession numbers are presented in Table S1 (see online uted western and eastern expanses of Guineo-Congolian supplemental material, which is available from the article’s forests (Salzmann & Hoelzmann, 2005; White, 1983). In Taylor & Francis Online page at http://dx.doi.org/10.1080/ 2009 and 2010, B.D. Marks, C. Kahindo and colleagues 14772000.2016.1226978). had the opportunity to conduct collections-based fieldwork We used our cyt-b data in conjunction with cyt-b data near Kisangani in the Democratic Republic of the Congo published for sanghensis and pyrrholaemus to determine (DRC). The primary goal of this survey work was to assess that we did in fact have those species represented in our genetic variation in avian species, and their ectoparasites, analyses (Beresford & Cracraft, 1999; Schmidt et al., distributed on both sides of the Congo River and several 2008). Subsequently, sequence data were analysed as a of its tributaries (see Light, Nessner, Gustafsson, Wise, & three gene concatenated dataset or a mitochondrial only Voelker, 2016;Voelkeretal.,2013). dataset. In both analyses, mitochondrial codon positions During our Benin survey, five specimens of Stiphrornis were unlinked (separate partitions). We used MrModelT- that are attributable to erythrothorax based on geography est (Nylander, 2004) to determine appropriate models of (Collar, 2005) were collected. During the DRC surveys, nucleotide substitution and to choose best-fit model of 10 Stiphrornis specimens attributable to xanthogaster sequence evolution for each partition. We used Sheppar- based on geography (Collar, 2005) were collected. All 15 dia aequatorialis as an outgroup (Voelker, Outlaw, & specimens (voucher skins and associated tissues) were Bowie, 2010). deposited in the Biodiversity Research and Teaching Col- For each dataset, we used MrBayes (Huelsenbeck & lections (formerly Texas Cooperative Wildlife Collec- Ronquist, 2001) to initiate two runs of four Markov-chain tions; TCWC remains the acronym) at Texas A&M Monte Carlo (MCMC) chains of 5,000,000 generations University. Tissue samples from these 15 specimens were each from a random starting tree, sampling every 100 gen- then included in a larger study of Stiphrornis systematics erations. Each run resulted in 50,000 trees and converged which included samples from all five currently recognized on the same topology. The first 5,000 trees from each taxa. While our initial goal was
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