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Illinois Natural History Survey Bulletin Illinois Natural History Survey Bulletin International • Peer-Reviewed • Open-Access Published continuously since 1876 A molecular phylogenetic analysis of the genera of fruit doves and their allies using dense taxonomic sampling Jennifer E. Nowak1†, Andrew D. Sweet1,2†, Jason D. Weckstein3,4, and Kevin P. Johnson1 1 Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, 1816 South Oak Street, Champaign, Illinois 61820, USA 2 Department of Entomology, Purdue University, 901 West State Street, West Lafayette, Indiana 47907, USA 3 Ornithology Department, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, USA 4 Department of Biodiversity, Earth, and Environmental Sciences, Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, USA † Authors contributed equally to the work Research Article Abstract Cite This Article: Fruit doves and their allies are a diverse group within the Nowak, J. E., A. D. Sweet, J. D. pigeon and dove family (Aves: Columbidae). Progress toward Weckstein, and K. P. Johnson. 2019. subfamilial classification of Columbidae relies on identifying A molecular phylogenetic analysis major groups and the phylogenetic relationships within these of the genera of fruit doves and groups. One such recently proposed group is the Raphinae, their allies using dense taxonomic based on previous evidence that the extinct dodo is potentially sampling. Illinois Natural History within what was formerly recognized as the Treroninae (fruit Survey Bulletin 42:2019001. doves and allies). Although several studies have explored the Author For Correspondence: phylogenetic relationships within Columbidae, most have focused Andrew D. Sweet either on broad-scale, familial-level relationships or finer-scale, email: [email protected] species-level relationships. Here we use mitochondrial and Data Accessibility Statement nuclear gene sequences from a diverse taxonomic sample to Sequence data are available identify relationships among the genera and species of fruit on GenBank under accession doves and their allies. In particular, our goal is to identify which numbers KT023313-KT023498 and of these genera should be included within Raphinae (the name KT029857-KT029914. Relevant that has taxonomic priority over Treroninae), focusing on an sequence alignment and phylo- inclusive, well-supported, monophyletic group. We also use genetic tree files are available dense taxon sampling to explore relationships among genera from the Illinois Data Bank (DOI: and species in this group, expanding on previous studies. In 10.13012/B2IDB-9797270_V1). addition, we use resulting phylogenetic hypotheses to recon- struct the ancestral evolutionary history of foraging mode and Keywords: biogeographic patterns of dispersal within the group. We use Raphinae, phylogeny, foraging, dispersal, biogeography, taxon two data sets for phylogenetic analysis: the first consisting sampling of novel sequences generated for this project and the second of additional, previously published sequences from the fruit- Received: dove genus (Ptilinopus). Our analyses found support for the 23 May 2019 monophyly of a clade that contains a large fraction of the Accepted: genera currently classified within Raphinae and also found 16 July 2019 several well-supported clades within this group of pigeons and Associate Editor: doves. Character reconstruction methods based on the resulting Auriel M. V. Fournier phylogeny recover multiple transitions from a terrestrial to an Editor in Chief: arboreal foraging mode and evidence for multiple dispersal Maximilian L. Allen events from Asia to Africa throughout the history of the clade. Copyright 2019 by the authors. Published by the Illinois Natural History Survey under the terms of the creative commons attribution license http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. ILLINOIS NATURAL HISTORY SURVEY BULLETIN 1 Introduction classification and instead included all proposed Pigeons and doves (Aves: Columbidae) are a high- Treroninae genera in an expanded subfamily Raph- ly successful and diverse group of birds that are inae. This classification corresponds to “Clade C” globally distributed and inhabit a variety of habi- from Pereira et al. (2007) and is expanded to in- tats (Goodwin 1983; Gibbs et al. 2001). However, clude the phabine genera and allies. However, the despite publication of several studies on phyloge- inclusion of the phabines in this group was quite netic relationships of Columbiformes, there are still unstable. Shapiro et al. (2002) first recoveredDre - many uncertainties about the diversification pat- panoptila and Alectroenas nested within Ptilinopus, terns within the order (Johnson and Clayton 2000a a relationship that has remained consistent in more and 2000b; Johnson et al. 2001; Pereira et al. 2007; recent studies (Cibois et al. 2014). This study had an Gibb and Penny 2010; Johnson et al. 2010; Johnson extensive representation of the diverse Ptilinopus ge- and Weckstein 2011; Cibois et al. 2014; Sweet and nus but did not focus on other related genera. Given Johnson 2015). One group that remains ambiguous the recent instability in these classification schemes, is the fruit pigeons and doves (“fruit doves” here- it is important to sample genera and species more after) and allied genera (Ptilinopus, Ducula, Gym- densely to identify stable phylogenetic patterns. nophaps, Lopholaimus, Hemiphaga, Phapitreron, The phylogenetic and taxonomic statuses of these Goura, Caloenas, Otidiphaps, Trugon, Turtur, Oena, lineages has important implications for the evolu- , and ), which had previously Chalcophaps Treron tion of Columbiformes, because this group could been considered to be members of a subfamily, the encompass a geographically and ecologically di- Treroninae (del Hoyo et al. 1997). However, a more verse subset of taxa (Goodwin 1983; Gibbs et al. recent classification (del Hoyo et al. 2014) places 2001; del Hoyo et al. 2014). The most species-rich ge- all of these genera within an expanded group, the nus within this group, Ptilinopus, is found primarily Raphinae, upon the discovery that the extinct dodo in forest canopies of Southeast Asia and Oceania. (Raphus cucullatus) is phylogenetically embedded Species in Ptilinopus vary in size but are all pri- within Treroninae (Shapiro et al. 2002; Pereira et al. marily frugivorous. Species from two other diverse 2007), and with Raphinae being the oldest available genera, Ducula and Treron, are also primarily found name for this group, as discussed by Cracraft in in forest canopies and forage on fruit. However, Dickinson and Remsen (2013). Pereira et al. (2007) has a broad geographic range, with repre- identified the monophyly and composition of this Treron group, but the result was somewhat unstable across sentatives in Asia and Africa. Additional arboreal analyses and included only limited taxon sampling. and frugivorous groups with phylogenetic affinities likely include the long-tailed pigeons from Austral- In addition to the more typical and large genera of asia (Gymnophaps, Lophalamius, and Hemiphaga), fruit doves (Ptilinopus, Ducula, and Treron), several Phapitreron from the Philippines, Drepanoptila and less diverse genera are associated with the fruit Cryptophaps from Oceania, and Alectroenas from doves and allies. Del Hoyo et al. (1997) defined islands in the western Indian Ocean. Other allied Treroninae as including the green pigeons (Treron), genera are terrestrial and primarily granivorous. The long-tailed pigeons (Gymnophaps, Cryptophaps, large ground pigeons are terrestrial and found in Lopholaimus, and Hemiphaga), fruit doves (Ducu- rainforest habitats in Oceania. Shapiro et al. (2002) la, Alectroenas, Drepanoptila, and Ptilinopus), and place the terrestrial Caloenas nicobarica (Nicobar brown pigeons (Phapitreron). The molecular phy- pigeon) as the closest living relative to the extinct logeny of Pereira et al. (2007) also included wood dodo (Raphus cucullatus). The small-bodied wood doves (Turtur, Oena, and Chalcophaps), ground pi- doves also forage on the ground and are distrib- geons (Otidiphaps, Trugon, Didunculus, Microgou- uted in Africa and Australasia. Thus, understanding ra, Goura, and Caloenas), cloven-feathered doves the transitions between terrestrial and arboreal for- (Drepanoptila), and blue pigeons (Alectroenas) in aging requires more-detailed understanding of the a clade with the Treroninae genera of del Hoyo et phylogenetic relationships among these genera. al. (1997). However, Gibbs et al. (2001) considered the wood doves (Chalcophaps, in particular) to be Some studies have indicated that increased taxon more closely related to bronzewings (Henicophaps) sampling can help resolve phylogenetic relation- in the phabine clade (Phaps, Geophaps, Ocyphaps, ships (Pollock et al. 2002; Hedtek et al. 2006; Prum Petrophassa, Geopelia, and Leucosarcia). Goodwin et al. 2015), so here we include dense sampling to (1983) likewise considered Chalcophaps, along improve the ability to resolve the phylogenetic re- with Oena and Turtur, to be closely related to the lationships within the fruit doves and their allies, phabines. He also included green pigeons, long- focusing in particular on species from many of tailed pigeons, fruit doves, blue pigeons, and the the genera mentioned. The taxa included in such cloven-feathered doves as a clade. Recently, del a clade would
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