Biogeographical Signature of River Capture Events in Amazonian

Journal of Biogeography (J. Biogeogr.) (2015) ORIGINAL Biogeographical signature of river ARTICLE capture events in Amazonian lowlands Victor A. Tagliacollo1,2*, Fabio Fernandes Roxo1, Scott M. Duke-Sylvester2, Claudio Oliveira1 and James S. Albert2 1Instituto de Biociências de Botucatu, ABSTRACT Universidade Estadual Paulista – UNESP, Aim To investigate the effects of river capture on the biogeographical history Botucatu, SP 18618–970, Brazil, 2Biology of South American freshwater fishes. Department, University of Louisiana at Lafayette, Lafayette, LA 70504-2451, USA Location Western Amazon and La Plata basins, and adjacent river drainages. Methods We used a species-dense time-calibrated phylogeny of long- whiskered catfishes (Siluriformes, Pimelodidae) to calculate likelihoods for 16 biogeographical scenarios of river capture, each differing in details of (1) landscape evolution and/or (2) models of species range evolution. We designed eight alternative landscape evolution models (LEMs) to represent distinct palaeogeographical river capture histories between the Western Amazon and La Plata drainages during the formation of the Central Andean (Bolivian) orocline (43.0–15.0 Ma). The LEMs differed only in patterns of area-connectivity constraints through time, and otherwise had the same geographical areas, time durations and dispersal probabilities. We used the DEC and DECj models of species range evolution under these eight LEM constraints to calculate likelihood values for ancestral area estimates. Results Divergence time estimates indicated that crown-group pimelodids emerged during the Late Cretaceous or Palaeogene (c. 72.9 Æ 20 Ma) and model-selection recovered a best-fit palaeogeographical scenario with (1) a LEM with three river capture events, and (2) a DECj model of species range evolution. These results were quantitatively replicated using Lagrange and BayArea-like methods. Main conclusions The taxon–area chronogram of pimelodids exhibits the characteristic biogeographical signature of river capture; i.e. several non-monophyletic regional (basin-wide) species assemblages coupled with the presence of many species inhabiting more than one basin. These phylogenetic and biogeographical patterns are consistent with the effects of three large-scale river capture events during the formation of the Bolivian orocline. *Correspondence: Victor A. Tagliacollo, Keywords Universidade Estadual Paulista – UNESP, Amazonian biodiversity, geographical range evolution, historical biogeography, Instituto de Biociências de Botucatu, Botucatu, landscape evolution models, Neotropical fishes, parametric biogeography, SP 18618–970, Brazil. E-mail: [email protected] Pimelodidae, river capture barriers that separate geographical areas and divide ancestral INTRODUCTION population ranges (Humphries & Parenti, 1999), and (2) the Historical biogeography aims to understand how geomor- erosion of barriers that merge previously separated geograph- phological events and other landscape evolution processes ical areas and allow geographical range expansions among affect the geographical distributions of species, higher taxa these newly connected areas (Lieberman & Eldredge, 1996; and whole biotas. Two important geomorphological Lieberman, 2003a). Studies in vicariance biogeography exam- processes of landscape evolution are: (1) the emergence of ine the phylogenetic relationships of individual taxa, or ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12594 V. A. Tagliacollo et al. taxon–area relationships of multiple phylogenies, to docu- landscape evolution processes (Lieberman, 2003b; Pyron, ment the history of biotic range fragmentation among conti- 2014). A biogeographical signature implies that geomorpho- nents and other areas of endemism (Ronquist, 1997; Brooks logical events help to regulate species range evolution et al., 2001; Burridge et al., 2007; Sanmartın et al., 2008). (Rosen, 1978; Lieberman, 2005). The signature of river cap- Other studies document patterns of coordinated dispersal ture (Fig. 1) might sometimes be masked by stochastic between areas to understand how geographical merging events of long-distance dispersals (Cook & Crisp, 2005), events (i.e. geodispersal) contribute to the formation of regional or local extinctions (Lieberman, 2002), pseudocon- regional species assemblages (Lieberman & Eldredge, 1996; gruence in taxon–area relationships (Donoghue & Moore, Lieberman, 2003a). The goal of all these studies is to under- 2003), or uncertainties in phylogenetic or biogeographical stand the role of landscape evolution in the process of lin- reconstructions (Nylander et al., 2008; Ho & Phillips, 2009). eage diversification and formation of regional species With the development of molecular phylogenetic methods to assemblages (Aleixo & de Fatima Rossetti, 2007; Cowling estimate absolute clade ages (Lepage et al., 2007), and et al., 2009; Hoorn et al., 2010b; Badgley et al., 2014). model-based methodologies in biogeography to estimate spe- Vicariance and geodispersal are geomorphological pro- cies range evolution (Ree & Smith, 2008; Landis et al., 2013; cesses that affect range evolution by separating or connecting Matzke, 2014), these confounding contingencies can be mini- populations and biotas (Lieberman, 2003a; Wiens & Dono- mized (Ree & Sanmartın, 2009; Chacon & Renner, 2014). ghue, 2004; Buerki et al., 2011). These two processes usually One strategy is to evaluate the likelihood for alternative his- have opposite effects on marine and terrestrial taxa. For torical scenarios of species range evolution in the context of instance, the Plio-Pleistocene rise of the Panamanian isthmus alternative hypotheses of landscape evolution. separated some marine groups into populations in the Wes- In South America, biogeographical studies of river capture tern Atlantic and Eastern Pacific (Lessios, 2008), while simul- have mostly been conducted in geologically stable areas (e.g. taneously allowing range expansions of terrestrial organisms shields), where erosion is slow and the geophysical signals of between Central and South America (Marshall et al., 1982). palaeogeographical events are geologically persistent (Ribeiro, Similarly, the Late Cretaceous separation of South America 2006; Lujan et al., 2011; Roxo et al., 2014). On the other and Africa isolated terrestrial groups on either side of the hand, historical studies in lowland Amazonian river systems, emerging South Atlantic (Cracraft, 2001), while allowing including the Western Amazon and other portions of the range expansions of marine organisms between the Northern sub-Andean foreland, have received less attention (but and Southern Atlantic basins (Marshall et al., 1982). In both see Albert et al., 2006; Albert & Carvalho, 2011). The sub- these examples, some clades display a vicariant signature of Andean foreland is a retroarc depression located along the range splitting, while other clades display a geodispersal sig- eastern margin of the Andean Cordillera (Horton & DeCelles, nature of synchronized range expansions. 1997). Over the last 50 million years, the sub-Andean system River capture is a special case of landscape evolution that has been fragmented into semi-isolated sub-basins by a series results in both the formation and removal of barriers of geomorphic uplifts that reshaped the watershed bound- between portions of adjacent river drainages. River capture is aries (Lundberg et al., 1998; Hoorn et al., 2010a). The for- especially interesting from a biogeographical perspective mation of the Bolivian orocline during the late Eocene to because, by moving the physical location of watershed middle Miocene (43.0–15.0 Ma) contributed to the fragmen- boundaries, different portions of adjacent river basins tation of the sub-Andean foreland and resulted in large-scale become isolated and merged (Albert & Crampton, 2010). river capture events in the area of the headwaters of what is This predictable barrier displacement produces complex and today the Upper Madeira and Upper Paraguay basins (Lund- reticulated, but also predicable, patterns of taxon–area rela- berg et al., 1998; Albert & Reis, 2011). This area tionships (Albert & Carvalho, 2011; Roxo et al., 2014). River (~1,050,000 km2) is located in the department of Santa Cruz, capture can have great consequences for the geographical Bolivia, and it has a complex history of watershed move- range evolution and diversification of obligate aquatic taxa ments between the Western Amazon and La Plata basins. (e.g. freshwater fishes, some amphibians), and taxa special- Here, we investigate the effects of river capture on the bio- ized to riparian and floodplain habitats (e.g. some plants and geographical history of pimelodid catfishes (Ostariophysi, Sil- birds) in which dispersal is constrained by the geometry of uriformes) inhabiting the sub-Andean foreland basin, river drainage networks (Waters et al., 2000; Aleixo & de especially at the margins of the modern Western Amazon Fatima Rossetti, 2007; Grant et al., 2007; Albert et al., 2011). and La Plata basins. Pimelodids are mainly riverine fishes In the absence of confounding historical contingencies, that inhabit virtually all portions of the sub-Andean foreland river capture imprints a characteristic biogeographical basins, and which represent an interesting case to understand signature on taxon–area relationships: the presence of non- the effects of river capture on the spatial distribution of monophyletic regional (basin-wide) species

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