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Biogeography and Diversification of Rhegmatorhina (Aves: Thamnophilidae): Implications for the Evolution of Amazonian Landscapes During the Quaternary

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Biogeography and Diversification of Rhegmatorhina (Aves: Thamnophilidae): Implications for the Evolution of Amazonian Landscapes During the Quaternary DOI: 10.1111/jbi.13169 ORIGINAL ARTICLE Biogeography and diversification of Rhegmatorhina (Aves: Thamnophilidae): Implications for the evolution of Amazonian landscapes during the Quaternary Camila C. Ribas1,2 | Alexandre Aleixo3 | Chrysoula Gubili4 | Fernando M. d’Horta4 | Robb T. Brumfield5 | Joel Cracraft2 1Coord. de Biodiversidade, Instituto Nacional de Pesquisas da Amazonia,^ Abstract Manaus, AM, Brazil Aim: To test the importance of alternative diversification drivers and biogeographi- 2Department of Ornithology, American cal processes for the evolution of Amazonian upland forest birds through a densely Museum of Natural History, New York, NY, USA sampled analysis of diversification of the endemic Amazonian genus Rhegmatorhina 3Coord. de Zoologia, Museu Paraense at multiple taxonomic and temporal scales. Emılio Goeldi, Belem, PA, Brazil Location: Amazonia. 4Graduate Program in Genetics, Conservation and Evolutionary Biology, Taxon: Antbirds (Thamnophilidae). INPA, Manaus, AM, Brazil Methods: We sequenced four mtDNA and nuclear gene regions of 120 individuals 5Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA from 50 localities representing all recognized species and subspecies of the genus. We performed molecular phylogenetic analyses using both gene tree and species Correspondence Camila C. Ribas, Coord. de Biodiversidade, tree methods, molecular dating analysis and estimated population demographic his- Instituto Nacional de Pesquisas da tory and gene flow. Amazonia,^ Manaus, AM, Brazil. Email: [email protected] Results: Dense sampling throughout the distribution of Rhegmatorhina revealed that the main Amazonian rivers delimit the geographic distribution of taxa as inferred Present addresses from mtDNA lineages. Molecular phylogenetic analyses resulted in a strongly sup- Chrysoula Gubili, Hellenic Agricultural Organization, Fisheries Research Institute, ported phylogenetic hypothesis for the genus, with two main clades currently sepa- Nea Peramos, Kavala, Macedonia, Greece. rated by the Madeira River. Molecular dating analysis indicated diversification Funding information during the Quaternary. Reconstruction of recent demographic history of populations Fundacßao~ de Amparo a Pesquisa do Estado revealed a trend for population expansion in eastern Amazonia and stability in the do Amazonas, Grant/Award Number: 929/ 2011; Fundacß~ao de Amparo a Pesquisa do west. Estimates of gene flow corroborate the possibility that migration after diver- Estado de Sao~ Paulo, Grant/Award Number: gence had some influence on the current patterns of diversity. 2007/07637-3, 2012/50260-6; Conselho Nacional de Desenvolvimento Cientıfico e Main Conclusions: Based on broad-scale sampling, a clarification of taxonomic Tecnologico, Grant/Award Number: boundaries, and strongly supported phylogenetic relationships, we confirm that, first, 308927/2016-8, 310880/2012-2, 470610/ 2008-5; United States Agency for mitochondrial lineages within this upland forest Amazonian bird genus agree with International Development, Grant/Award spatial patterns known for decades based on phenotypes, and second, that most lin- Number: PEER Cycle 5,AID-OAA-A-11- 00012; Coordenacß~ao de Aperfeicßoamento de eages are geographically delimited by the large Amazonian rivers. The association Pessoal de Nıvel Superior, Grant/Award between past demographic changes related to palaeoclimatic cycles and the histori- Number: 23038.001963/2012-41; Directorate for Biological Sciences, Grant/ cally varying strength and size of rivers as barriers to dispersal may be the path to Award Number: 1146423, 1241066; F.M. the answer to the long-standing question of identifying the main drivers of Amazo- Chapman Fund/AMNH; NSF, Grant/Award Number: 1241066, 1146423; NASA nian diversification. Editor: Miles Silman | Journal of Biogeography. 2018;45:917–928. wileyonlinelibrary.com/journal/jbi © 2018 John Wiley & Sons Ltd 917 918 | RIBAS ET AL. KEYWORDS Amazonia, Antbirds, diversification, molecular systematics, Neotropic, phylogeny, phylogeography, taxonomy 1 | INTRODUCTION Recent, more detailed phylogenetic and phylogeographic studies, associated systematic revisions and temporal diversification analyses Amazonian diversity and its distribution are still poorly known, even of extant Amazonian taxa show constant diversification rates in well-studied groups such as birds (Whitney & Cohn-Haft, 2013). throughout the Neogene/Quaternary (Brumfield, 2012; d’Horta, Numerous regions of this vast forest lack modern biotic inventories, Cuervo, Ribas, Brumfield, & Miyaki, 2013; Patel, Weckstein, Patane, and many taxa remain to be described (Barrowclough, Cracraft, Bates, & Aleixo, 2011). Detailed taxonomic sampling and phyloge- Klicka, & Zink, 2016; Hopkins, 2007). Despite gaps in our taxonomic netic analysis have also shown a Plio–Pleistocene origin of species of and distributional knowledge, Amazonia harbours the highest species the genus Psophia, whose ranges are clearly delimited today by the diversity of any biome on Earth (de Groot et al., 2012). However, large Amazonian rivers (Ribas et al., 2012), indicating that the our understanding of its evolutionary origins remains unclear dynamic history of the Amazonian drainage system may be an because an answer relies on fundamental knowledge about the important driver of diversification during this period (Nogueira et al., region’s constituent taxa, their distributions and their interrelation- 2013). Population-level sampling of Psophia species also shows dis- ships, for which there are still many gaps. Multiple studies have tinct demographic signatures for populations from different Amazo- shown that currently recognized species significantly underestimate nian areas of endemism, suggesting differential effects of climatic the number of evolutionary taxa that are relevant for analyses of cycles on forest bird populations (Cheng et al., 2013; Ribas et al., diversification and biogeography (e.g. Fernandes, Wink, & Aleixo, 2012; Wang et al., 2017). Additional studies of other groups of Ama- 2012; Harvey & Brumfield, 2015; Ribas, Aleixo, Nogueira, Miyaki, & zonian birds corroborate these findings, supporting both drainage Cracraft, 2012; Ribas, Joseph, & Miyaki, 2006; Thom & Aleixo, evolution and climatic-driven changes on vegetation cover as impor- 2015). Thus, how we think about species-level taxa and how well tant drivers of diversification during the Plio–Pleistocene (d’Horta each group is geographically sampled and taxonomically known is et al., 2013; Fernandes, Wink, Sardelli, & Aleixo, 2014; Fernandes central to solving the question of the evolutionary drivers of Amazo- et al., 2012; Ferreira, Aleixo, Ribas, & Santos, 2017; Schultz et al., nian diversity. 2017; Thom & Aleixo, 2015). However, incongruent patterns (Smith An important uncertainty is how the origin of this high diversity et al., 2014) suggest a complex history and a combination of biogeo- relates to landscape history, which has been the subject of consider- graphic processes (including dispersal and vicariance) acting across able debate over many decades (Haffer, 1969; Hoorn et al., 2010; multiple time scales. Ribas et al., 2012; Smith et al., 2014). Our growing knowledge of The genus Rhegmatorhina includes taxa specialized for army-ant the geological and palaeoclimatological history of Amazonia (Cheng following in the understory of tall upland Terra Firme Amazonian for- et al., 2013; Hoorn et al., 2010; Latrubesse et al., 2010; Nogueira, est (Willis, 1969). There are five recognized species—R. gymnops, Silveira, & Guimar~aes, 2013; Wang et al., 2017) is now allowing us R. hoffmannsi, R. berlepschi, R. melanosticta and R. cristata (Zimmer & to ask specific questions about patterns of biotic history (Baker Isler, 2003). Large rivers define the majority of ranges for these spe- et al., 2014). In particular, how past climate variation may have cies, which occur in five Amazonian areas of endemism (sensu affected the demography and connectivity of forest-adapted popula- Borges & Silva, 2011; Cracraft, 1985; Silva et al. 2005): Tapajos, tions, and how landscape reorganization relating to drainage evolu- Rondonia,^ Inambari, Napo and Jau. The genus is absent from the tion may have contributed to the origin of upland forest species. three easternmost areas: Guiana, Xingu and Belem. Two species Traditionally, these candidate palaeoenvironmental drivers are sup- (R. hoffmannsi and R. berlepschi) occupy the Rondonia^ area, and one posed to have operated at different time frames: glacial cycles species (R. melanosticta) occupies two areas (Inambari and Napo). occurred mostly during the Quaternary (Haffer, 1969), whereas the Although species distributions within the genus are delimited by current configuration of the Amazonian drainage system has been major Amazonian rivers, hybridization has been documented largely assumed to date to the Miocene (Hoorn et al., 2010), despite between R. gymnops and R. hoffmannsi in the headwaters of the evidence pointing to more recent times (Latrubesse et al., 2010; Tapajos River, which is the limit between the Tapajos and Rondonia^ Nogueira et al., 2013). Due to this temporal difference, the two dri- areas (Weir, Faccio, Pulido-Santacruz, Barrera-Guzman, & Aleixo, vers are rarely integrated. Therefore, studies have assumed that spe- 2015). Here, we present combined phylogeographic and phyloge- cies may be old, with their origin related to Miocene drainage netic multilocus analyses for the genus to test the importance of evolution
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