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Rapid Laurasian Diversification of a Pantropical Bird Family During The Ibis (2020), 162, 137–152 doi: 10.1111/ibi.12707 Rapid Laurasian diversification of a pantropical bird family during the Oligocene–Miocene transition CARL H. OLIVEROS,1,2* MICHAEL J. ANDERSEN,3 PETER A. HOSNER,4,7 WILLIAM M. MAUCK III,5,6 FREDERICK H. SHELDON,2 JOEL CRACRAFT5 & ROBERT G. MOYLE1 1Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Lawrence, KS, USA 2Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA 3Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM, USA 4Division of Birds, Department of Vertebrate Zoology, National Museum of Natural History, Washington, DC, USA 5Department of Ornithology, American Museum of Natural History, New York, NY, USA 6New York Genome Center, New York, NY, USA 7Natural History Museum of Denmark and Center for Macroecology, Evolution, and Climate; University of Copenhagen, Copenhagen, Denmark Disjunct, pantropical distributions are a common pattern among avian lineages, but dis- entangling multiple scenarios that can produce them requires accurate estimates of his- torical relationships and timescales. Here, we clarify the biogeographical history of the pantropical avian family of trogons (Trogonidae) by re-examining their phylogenetic rela- tionships and divergence times with genome-scale data. We estimated trogon phylogeny by analysing thousands of ultraconserved element (UCE) loci from all extant trogon gen- era with concatenation and coalescent approaches. We then estimated a time frame for trogon diversification using MCMCTree and fossil calibrations, after which we performed ancestral area estimation using BioGeoBEARS. We recovered the first well-resolved hypothesis of relationships among trogon genera. Trogons comprise three clades, each confined to one of three biogeographical regions: Africa, Asia and the Neotropics, with the African clade sister to the others. These clades diverged rapidly during the Oligo- cene-Miocene transition. Our biogeographical analyses identify a Eurasian origin for stem trogons and a crown clade arising from ancestors broadly distributed across Laurasia and Africa. The pantropical ranges of trogons are relicts of a broader Afro-Laurasian distribu- tion that was fragmented across Africa, Asia and the New World in near coincident fash- ion during the Oligocene‐Miocene transition by global cooling and changing habitats along the Beringian land bridge and North Africa. Keywords: Beringian land bridge, historical biogeography, pantropical distribution, Trogonidae, ultraconserved elements. The occurrence of the disjunct pantropical biota disjunct distributions across the Old and New has been of wide interest to ornithologists. The Worlds. This hypothesis ascribes disjunct distribu- Boreotropics hypothesis (Wolfe 1975, Tiffney tions to a Laurasian origin in the early/middle 1985), which was borne out by studies of plant Palaeocene, during which lineages attained a broad taxa and their fossils but has since been invoked in distribution under favourable tropical and sub-tro- animal groups (e.g. Sanmartın et al. 2001), repre- pical climatic conditions and suitable land connec- sented a major advance in our understanding of tions across Laurasia before subsequently becoming isolated by high-latitude climatic deteri- oration and the severing of continental land *Corresponding author. Email: [email protected] bridges. The Boreotropics hypothesis provides a Twitter: @carlholiveros framework that describes the divergence of plant © 2019 British Ornithologists’ Union 138 C. H. Oliveros et al. and animal lineages across the North Atlantic Reconstructing the early biogeographical history (Lavin & Luckow 1993, Sanmartın et al. 2001) of the trogons has been a major challenge, even and Beringia (Beard 1998, Donoghue et al. 2001, with DNA sequence data. The trogons, in the Beard et al. 2016) and has even been invoked to family Trogonidae, consist of 43 species in seven explain an Africa–South America disjunction of an genera distributed throughout much of the Old angiosperm clade (Davis et al. 2002). Although World and New World tropics (Dickinson & Rem- the large-scale geographical and climatic events sen 2013; Fig. 1). Diversity is greatest in the New driving diversification are the same for all groups, World (29 species), followed by Asia (12 species) the pattern and timing of divergence in individual and Africa (three species). Trogons are generally lineages vary; thus, an accurate estimate of phy- considered poor long-distance dispersers, although logeny and divergence times for each lineage is some species exhibit seasonal movements and one essential for deciphering various patterns and indi- species has colonized the oceanic Philippine vidual causes of their spatial history (Donoghue islands. Multiple, conflicting biogeographical histo- et al. 2001, Sanmartın et al. 2001), and ultimately ries have been proffered for the group because of for understanding the development of modern differences in phylogenetic estimates (Espinosa de pantropical biota. los Monteros 1998, Johansson & Ericson 2005, Independent of the Boreotropics hypothesis, Moyle 2005, Ornelas et al. 2009, Hosner et al. many tropical avian lineages are considered relicts 2010). For instance, some studies recovered dis- of ancestors with broader distributions in Laurasia tinct clades of African, Asian and Neotropical taxa in the Palaeocene (Olson 1985, Blondel & Mourer- (Espinosa de los Monteros 1998, Johansson & Eric- Chauvire 1998, Feduccia 2003). These relicts son 2005, Ornelas et al. 2009), whereas others include: mousebirds (Coliiformes); the cuckoo suggested paraphyly of the Neotropical taxa roller (Leptosomiformes); hornbills (Buceroti- (Moyle 2005, Hosner et al. 2010). These conflicts formes); rollers and allies (Coraciiformes); wood- probably resulted from the use of a few, different peckers and allies (Piciformes); and trogons molecular markers, each supporting different (Trogoniformes). All of these bird groups have been topologies or providing little or no branch resolu- traditionally considered members of the ‘higher tion. Support for intergeneric relationships was non-passerines’ (Sibley & Alqhuist 1972) and have low in all the studies except one (Ornelas et al. recently been found to constitute a major clade of 2009), in which Bayesian posterior probabilities land birds, the Coraciimorphae (Jarvis et al. 2014, were high (100%) but maximum likelihood boot- Prum et al. 2015). Coliiformes and Leptosomi- strap values were < 50%. Moreover, with the formes, groups currently confined to Africa and exception of Hosner et al. (2010), previous work Madagascar, respectively, had much wider distribu- did not include the distinctive Asian genus Apal- tions in North America and Europe during the harpactes, whose placement with other Asian tro- Eocene based on the fossil record (Weidig 2006, gons was equivocal. Ksepka & Clarke 2009). Bucerotiformes at present The difficulty in resolving trogon phylogeny occur in the Old World tropics, but hornbill fossils stems from two factors. First, the base of the tro- are known from the Eocene and Miocene of Europe. gon tree is characterized by short successive Coraciiformes, Piciformes (including barbets) and internodes, indicating a rapid initial burst of lin- Trogoniformes, each of which has a contemporary eage formation. Phylogenies with such a structure pantropical distribution, had broader distributions are difficult to resolve with limited data, as in all in the Cenozoic. Eocene/Oligocene coraciiform fos- previous studies of trogons, because of the low sils are known from Europe; piciforms are known probability of informative substitutions occurring from the Eocene of North America and the Mio- along these short internodes (Lanyon 1988) and cene of Europe (Brodkorb 1971); and trogoniform the high probability of gene tree discordance fossils are known from the Palaeogene of Europe (Degnan & Rosenberg 2006). Secondly, trogons (Kristoffersen 2002, Mayr 2005, 2009). Among have no close, living sister-group to break up the these groups, trogons have been the subject of espe- long branch leading to their rapid radiation cially intense phylogenetic and biogeographical (Johansson & Ericson 2005, Moyle 2005, Hackett study (Espinosa de los Monteros 1998, Johansson & et al. 2008, Prum et al. 2015). This long branch, Ericson 2005, Moyle 2005, DaCosta & Klicka 2008, combined with subsequent short internodes at the Ornelas et al. 2009, Hosner et al. 2010). base of the trogon clade, obfuscates the root of © 2019 British Ornithologists’ Union Laurasian diversification of trogons 139 Otus elegans Colius striatus Leptosomus discolor Ceyx argentatus Upupa epops 100/-/97/80 Berenicornis comatus 100/-/100/100 Apaloderma aequatoriale ca i r f Apaloderma vittatum Africa A Apalharpactes mackloti Trogoniformes 78/81/65/86 Harpactes oreskios Harpactes ardens Asia 100/100/99/97 Harpactes erythrocephalus Euptilotis neoxenus Pharomachrus antisianus s c i Priotelus temnurus p o r t Priotelus roseigaster o e Trogon personatus N Neotropics Trogon violaceus Cret. Paleocene0.6 Eocene Oligocene0.3 0.2 Miocene 0.1 Pli. Pl. 70 60 50 40 30 20 10 0 Ma Beringian Land Bridge N. Atlantic Land Bridge Africa-Eurasia Land Bridge 25 20 15 (Temperature °C) (Temperature 10 70 60 50 40 30 20 10 0 Ma Figure 1. Estimate of phylogenetic relationships of trogons based on concatenated and coalescent approaches. Nodes with dots correspond to 100% bootstrap support
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