ORNITOLOGIA NEOTROPICAL 23: 187–206, 2012 © The Neotropical Ornithological Society

TOWARDS AN INTEGRATED HISTORICAL OF THE NEOTROPICAL LOWLAND AVIFAUNA: COMBINING DIVER- SIFICATION ANALYSIS AND LANDSCAPE EVOLUTION

Camila C. Ribas1, Marcos Maldonado-Coelho2,3, Brian Tilston Smith4, Gustavo S. Cabanne5, Fernando M. d’Horta3, Luciano N. Naka4,6

1Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Manaus, AM, Brasil. E-mail: [email protected] 2Department of , University of Missouri-St. Louis, 223 Research Building, One University Boulevard, St. Louis, USA. 3LGEMA, Departamento de Genética e Biologia Evolutiva, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 4Museum of Natural Science, Louisiana State University, 119 Foster Hall, Baton Rouge, LA, USA 5División de Ornitología, Museo Argentino de Ciencias Naturales ‘B. Rivadavia’, Ángel Gallardo 470, Buenos Aires, Argentina. 6Current address: Centro de Estudos da Biodiversidade, Universidade Federal de Roraima, Boa Vista, RR, Brazil.

Resumo. – Uma abordagem integrada da história biogeográfica da avifauna Neotropical de terras baixas: combinando padrões de diversificação e evolução da paisagem. – A importância da evolução da paisagem como agente causador da diversificacão biológica na região Neotropical é conhecida há tempo, mas mecanismos comuns até hoje não foram revelados. Sugerimos que três fatores principais contribuem para essa ausência de consenso: (i) pouco conhecimento da história da Terra, (ii) problemas com o teste de hipóteses de diversificação, e (iii) representação incompleta da diversidade pela taxonomia atual. Portanto, para estudar padrões de diversificacão alguns passos básicos têm que ser observados: (i) as unidades evo- lutivas têm que ser identificadas através de revisões taxonômicas, (ii) padrões de diversificacão precisam ser correlacionados a informações recentes sobre a história da Terra e (iii) hipóteses precisam ser avaliadas em relação a predições diretas e não ambíguas derivadas de cenários históricos alternativos. Neste artigo mostramos como estudos que amostram todas as unidades evolutivas e utilizam abordagens integrativas que combinam análise da diversificacão com dados detalhados sobre a história da Terra podem fornecer novas perspectivas sobre o papel dos fatores históricos na diversificação de organismos Neotropicais. Os resultados apresentados mostram que tanto mudanças paleoclimáticas quanto paleogeográficas podem ter sido importantes na diversificação de grupos de aves Neotropicais de terras baixas durante e antes do Pleistoceno.

Abstract – The importance of landscape evolution as driver of biotic diversification in the Neotropical low- lands has long been appreciated, but no clear common mechanisms have been revealed. We suggest that three main issues have collaborated to this: (i) poor understanding of earth history; (ii) problems with testing diversification hypotheses; and (iii) poor representation of diversity by current . Thus, in order to study diversification patterns, some basic steps need to be observed: (i) the units of biodiversity need to be properly recognized through taxonomic reviews, with good geographic sampling; (ii) diversification patterns need to be carefully confronted to new information on landscape history and (iii) hypotheses need to be evaluated against direct and unambiguous predictions from alternative historical scenarios. Here we show how studies that sample all evolutionary units and use integrative approaches that combine diversification analysis with detailed data on earth history can provide new insights on the role of historical factors on the

187 Ribas et al. diversification of Neotropical organisms. The results presented show that both paleogeographic and paleo- climatic processes may have had an important role in the diversification of lowland Neotropical avian groups during the and before. Key words: Neotropical, , phylogeography, diversification

INTRODUCTION due to the cyclical isolation of populations in forest refugia, mainly during the Pleistocene Evolutionary biologists have long struggled glacial eras. Many aspects of the refuge model to understand the causes of high have been challenged, including the timing diversity in the Neotropics, but have of speciation events and the existence of not reached a general consensus on the putative refugia (e.g. Lessa et al. 2003, Bush & mechanisms underlying observed patterns. In Oliveira 2006). A main criticism was that most the Neotropical lowlands, the importance of diversification events in Amazonia predate landscape evolution as driver of population the Pleistocene (Hackett & Rosenberg 1990; differentiation and speciation has long been Mustrangi & Patton 1997; Weir 2006; Hoorn appreciated (Chapman 1917, Haffer 1969). et al. 2010), triggering strong reactions against Although both palaeoclimatic and geological the refuge hypothesis and the Pleistocene history are thought to have influenced paradigm of speciation, and pointing towards a population dynamics, potentially leading to pre- origin of lowland Neotropical speciation across ecological and physical species (but see Rull 2011a). Some authors, barriers, many questions remain regarding their however, challenge this view, suggesting that roles on the processes of diversification. Here Pleistocene speciation events may have been we suggest that three main issues have hindered overlooked by under-representation of species a better understanding of the mode and tempo diversity (Bates & Demos 2001, Tobias et al. of speciation in the Neotropical lowlands: 2008, Rull 2011a,b). In fact recent studies (i) poor understanding of earth history (i.e. suggest that diversification rates have been paleogeographic and climatic processes); constant during both the Quaternary and the (ii) problems with testing diversification Neogene (Derryberry et al. 2011, Patel et al. hypotheses; and (iii) poor representation 2011, Rull 2006, 2011a,b), with no signal of of diversity by current taxonomy. These decrease in the Neotropical lowlands (Tobias issues have collaborated to create a false and et al. 2008, Patel et al. 2011, Ribas et al. 2012). unnecessary dichotomy between processes Based on these results, we suggest that in operating during the Pleistocene (i.e. climatic order to study diversification patterns, some oscillations) and before the Pleistocene (i.e. basic steps need to be observed: (i) the units geological evolution), and have eclipsed our of biodiversity (independent evolutionary views about the influence of the mechanisms units) need to be properly recognized through underlying diversification. taxonomic reviews, with good geographic In the Neotropics, the Pleistocene refugia sampling; (ii) diversification patterns need to hypothesis, originally proposed as a speciation be carefully confronted to new information on mechanism for Amazonian birds (Haffer landscape history and (iii) evaluated against direct 1969), rapidly became the dominant paradigm, and unambiguous predictions from alternative and remained as such for at least two decades. historical scenarios, in a mechanistic framework, The main prediction of this hypothesis was bridging the fields of , , that many forest dwelling species originated phylogeography and the biology of organisms.

188 NEOTROPICAL LOWLAND DIVERSIFICATION

Here, we show how studies that sample number of good species are likely to neglect all evolutionary units and use integrative part of the diversity they aim to analyze. approaches that combine diversification Indeed, when taxonomic misrepresentation of analysis with detailed data on earth history diversity is fully accounted for by performing can provide new insights on the role of taxonomic reviews prior to phylogeographic/ historical factors on the diversification of phylogenetic analyses on widespread polytypic Neotropical organisms. More specifically, we species, it has been shown that many species suggest that new geological and molecular originated within the Pleistocene (Tobias et al. data indicate that both paleogeographic 2008, Ribas et al. 2011). and paleoclimatic processes may have had an important role in the diversification of Evolution of South American and lowland Neotropical avian groups during the diversification of forest birds. Climate, Pleistocene and before. A complete review of particularly the amount and seasonality current diversification hypotheses is beyond of rainfall, is one of the most important the scope of this study and we only refer to factors determining spatial patterns of forest benchmark studies to highlight the increasing distribution. In the tropical lowlands, including importance of phylogeographic approaches in South America, rainforests grow on almost understanding mechanisms of diversification any soil, but only develop where annual rainfall in the Neotropical lowlands. is well distributed throughout the year and is greater than ;1800 mm (Corlett & Primack Underestimation of diversity by 2011). Therefore, changes in these variables, current taxonomy – Several authors have associated with climate cycles during the highlighted the perils of taxonomic artifacts Pleistocene, may have affected the distribution in biogeographical interpretations (Bates of lowland forests. Based on this assumption, & Demos 2001, Tobias et al. 2008, Pattel et and on the scarce geomorphological and al. 2011). In fact, regardless of the species palynological data available at the time, concept of choice, taxonomic reviews Haffer (1969) proposed the so-called “refuge applying modern conceptual frameworks hypothesis”. are crucial to document speciation patterns Available data consistently indicates that in lowland organisms. Recent studies have millennial-scale climate changes in South shown that many widespread polytypic species America were primarily forced by Milankovitch actually contain a number of evolutionary cycles (Vonhof & Kaandorp 2010). Also, independent lineages that deserve species significant glacial-interglacial variation is status (Tobias et al. 2008, Ribas et al. 2011). registered in several of the longer Quaternary For example, whereas Weir (2006) suggested records (e.g. Hooghiemstra et al. 1993, Cruz that Pleistocene climatic fluctuations where et al. 2005). Therefore, it is expected that more pervasive on Neotropical mountains changes in lowland forests distribution have than in the lowlands, it remains unclear occurred cyclically and, at least, throughout whether this is an artifact of taxonomic bias the Quaternary. Current data also suggest (Tobias et al. 2008). Similarly, taxonomic that the intensity of climatic oscillations in uncertainty has led to the idea that species are South America differed among regions. For younger in the Andes than in the lowlands example, lowlands and Andean highlands (i.e. the museum hypothesis; Fjeldså 1995). have shown different patterns of rainfall Studies of the Amazonian biota that assume response during LGM (Vizy & Cook 2007). that polytypic species do not encompass a Even among lowland forest regions is also

189 Ribas et al. observed a decoupling of climate patterns. that drainage evolution could be regarded as a For example, Cruz et al. (2009) observed that potential driver of biotic diversification mainly climate in the eastern Amazon swung between during the Miocene, and has collaborated to interglacial wet and glacial arid conditions, the dichotomy between old (rivers/Miocene) while western Amazon remained generally and young (refugia/Pleistocene) drivers of humid throughout the last 250 ka (Cheng et diversification in Amazonia. al. unpublished). Similarly, different regions of However, analyses of sediments from Atlantic forest seem to have experienced not central Amazonia and Peru have led other only different intensities of changes (Carnaval authors (Rossetti et al. 2005, Campbell et & Moritz 2008), but also opposite responses al. 2006, Latrubesse et al. 2010, Silveira & - with forest expansion in the south and Nogueira 2011) to suggest an alternative retraction in the north at the same time (Cruz interpretation, in which drainage evolution et al. 2005, 2009; Wang et al. 2004, 2006), and was a long process that started during the these patterns are supported by biological data Miocene, and lasted until the Pleistocene, with (e.g. Cabanne et al. 2008, d’Horta et al. 2011). the current drainage system being established Therefore, it seems that the spatial behavior during the Plio-Pleistocene. This alternative of during the Quaternary was model implies that the Purus arch (Wanderli- much more complex than previously thought, Filho et al. 2010) was an important barrier generating different expectations regarding for drainage evolution, and that the Amazon the impact of these climate cycles on forest basin was divided by it until the Pliocene, distribution among South American regions. with the transcontinental Amazon drainage Although there isn’t an integrated system being established only after that time regional climate history, a great amount of (Latrubesse et al. 2010, Silveira & Nogueira paleoenvironmental data has become available 2011). Further supporting the dynamic nature since the proposition of the Refuge hypothesis of Amazonian drainage, studies employing (e.g. Auler et al. 2006; Wang et al. 2006; Cruz SRTM data and termoluminescense dating et al. 2009; Ledru et al. 2009). These new of sediments at riverine terraces have shown data will necessarily improve our knowledge that some of the large Amazonian rivers of climate evolution in South America, and have recent histories, influenced by sediment allow for a better assessment of the role of accumulation and neotectonics (Almeida- Quaternary climate changes in the origin of Filho & Miranda 2007, Soares et al. 2010). the biogeographic patterns observed in the The evolutionary scenario derived from continent. this alternative interpretation brings the time frame of drainage evolution to overlap with the Geological evolution of the Amazon beginning of the Pleistocene glacial era (last 2.6 Basin: new data and debates. Based on Myr). As the dating of diversification events stratigraphic records from Colombia and in several Amazonian avian groups indicates eastern Amazonia, several authors (Hoorn that current species originated during the Plio- 1994, Hoorn et al. 1995, Figueiredo et al. Pleistocene (Aleixo 2004, Patel et al. 2011, 2009, Hoorn & Wesselingh, 2010, Hoorn et al. Ribas et al. 2012, Ribas et al. unpublished), this 2010) have developed the currently accepted scenario implies a temporal correlation between paleoenvironmental history of northern South drainage evolution and biotic diversification. America, in which the Amazonian drainage Thus, the possibility that drainage evolution system was established during the Middle to has influenced the diversification of organisms Late Miocene (~15 to 7 mya). This implies in Amazonia during the Plio-Pleistocene needs

190 NEOTROPICAL LOWLAND BIRD DIVERSIFICATION to be further investigated by including all the & Moritz 2008), which can be used to derive available geological information into plausible explicit spatio-temporal predictions to be diversification scenarios and adopting contrasted with pattern of genetic variation sampling schemes designed specifically to test (Maldonado-Coelho 2012). A conceptual the competing hypotheses. framework combining phylogeography and information on paleoenvironmental data Hypotheses testing: integrating was recently used to disentangle the effects phylogeographic analyses and landscape of drainage evolution and glaciations as evolution. The importance of classical engines of speciation in a widely distributed hypotheses in explaining diversification of Amazonian avian group (Ribas et al. 2012). Neotropical organisms has been historically As detailed information on earth history is contentious; the main criticisms stem from becoming widely available for many lowland the fact that similar biogeographic patterns regions, the emergent field of statistical can be equally well explained by more than phylogeography also offers the possibility one hypothesis (Endler 1982). In fact few of testing multiple plausible diversification contrasting predictions are currently available, models derived directly from these external or can be derived from alternative hypotheses sources of data (Knowles 2009, Hickerson et al. of speciation (Moritz et al. 2000). One way 2010). In some cases, however, the competing to overcome such hurdles is through the hypotheses predict similar temporal and spatial application of integrative approaches that patterns of population differentiation, and combine information on earth history and more explicit and detailed spatial-temporal landscape evolution with population genetics frameworks would be useful. For example, and coalescent theory analytical methods, one would need to use sampling schemes which can allow the falsification of hypotheses designed to test specific hypotheses, as did the in a more comprehensive way (e.g. Cabanne et classical study of Patton and co-workers along al. 2011, Maldonado-Coelho 2012, Ribas et al. the Juruá River (Patton et al. 1994), to derive 2012). unambiguous predictions capable of clarifying The test of competing hypotheses of the roles of relatively young paleodrainage diversification among and within biogeographic evolution (i.e. Pleistocene- boundary; regions is greatly strengthened when available Rossetti & Valeriano 2007) versus Pleistocene information on paleoenvironmental evolution glaciations on population divergence. Different is incorporated (Carnaval & Bates 2008, Ribas approaches used to test competing hypotheses et al. 2012). This type of approach can generate will vary case by case and will depend on unambiguous predictions that can provide clues available information on earth history and on on how and when populations were affected the creativity of individual researches. by earth history such as drainage evolution, glaciations, orogeny, and changes in biome RESULTS PRESENTED IN THE distribution. Paleoenvironmental data may SYMPOSIUM come from palynological (Ledru et al. 2006), geological (Campbell et al. 2006, Latrubesse et Idiosyncrasies in Atlantic Forest al. 2010, Hoorn et al. 2011), and paleo-climatic diversification patterns: the case of data (Wang et al. 2004, Raymo et al. 2006). In the Greenish (Schiffornis addition to raw paleoenvironmental data, it is virescens, Tytiridae). Studies of Atlantic also possible to generate refugia hypotheses Forest organisms suggest that the historical based on historical climatic modeling (Carnaval distribution of the forest cover generated

191 Ribas et al. demographically stable populations in its lineages, hence to the observed lack of a central region and unstable populations in strong phylogeographic pattern and low the southern and northern regions (Carnaval genetic diversity. & Moritz 2008; Carnaval et al. 2009). The Even though the results of this study are southern range of the Atlantic Forest was not fully compatible with the demographic apparently the most affected by forest predictions derived from Carnaval and Moritz retraction and formation of refuges during the (2008) and Carnaval et al. (2009), which Pleistocene glaciations (Carnaval et al. 2009). were accepted in other AF taxa (Cabanne This observation led some authors to state that et al. 2007; Cabanne et al. 2008; Mustrangi & refuge formation might have been important Patton 1997; d’Horta et al. 2011; Carnaval et to explain diversification of Atlantic Forest al. 2009; Maldonado-Coelho 2012), they still taxa (i.e. Cabanne et al. 2007, Carnaval et al. are in accordance with hypotheses of the AF 2009, Maldonado-Coelho 2012). history during the Pleistocene. The fact that S. Cabanne et al. (unpubl) studied the virescens is a relatively young species and is also mitochondrial phylogeographic structure of associated with southern AF might explain why the Greenish Schiffornis Schiffornis virescens the pattern found differs from other studied (Tytyridae), a endemic to the AF groups. Independent of the origin of the and inhabitant of the forest understory, and phylogeographic structure of S. virescens, our evaluated questions and predictions related to results suggest that some AF taxa like S. virescens the aforementioned hypothesis. The specific have had all their populations affected by the questions were: i) does the species present recent history of the biome, contrary to what a strong phylogeographic structure, with ii) has been revealed by other phylogeographic demographic stability in the northern regions studies that indicated different demographic and iii) demographic expansion in the southern histories between central and southern AF populations? populations (Cabanne et al. 2008; d’Horta et The authors analyzed cytochrome b and al. 2011; Carnaval et al. 2009; Batalha-Filho et control region sequences of the mitochondrial al. 2009, Maldonado-Coelho 2012). Therefore, genome by traditional phylogenetic and organisms may have idiosyncratic responses to population genetic methods based on historical processes, and predictions about the summary statistics. In addition, they used history of the biome should take into account coalescent simulations to evaluate specific ecological characteristics and distribution of models of evolution of the populations of each organism. Schiffornis virescens. The results did not support phylo- Rivers and Refuges in Atlantic Forest geographic partitions of the genetic variability and Amazonian taxa: phylogeographic of S. virescens. The time to the most recent patterns. Surveys conducted in distinct regions common ancestor was 0.4 MY (95%CI 0.2- containing a suite of environmental conditions 0.6 Myr), which indicates that the species is constitute ideal scenarios to assess the role of relatively young. The overall Fst was= 0.32 both climatic and geological history as drivers and gene flow between regions was moderate of diversification. Maldonado-Coelho et al. to high. The analysis suggested that the whole carried out a densely sampled study to elucidate population of S. virescens suffered a bottleneck the importance of paleoclimatic and geological followed by a demographic expansion in the factors as engines of diversification on the late Pleistocene. The bottleneck might have lowland representatives of South American contributed to the of intraspecific fire-eye ( Pyriglena). The authors

192 NEOTROPICAL LOWLAND BIRD DIVERSIFICATION used mitochondrial and nuclear sequence data 2011). Also, they have important implications to examine the phylogeographic structure of for a better understanding of the importance fire-eye populations along the southeastern of large Amazonian rivers in vertebrate Amazon Basin and Atlantic Forest, and diversification in the Neotropics and agree confronted the predictions of the river and with recent geological (Rosseti et al. 2005, Pleistocene refuge hypotheses against the Campbell et al., 2006; contra Hoorn et al., 2010) patterns of genetic variation observed in these and molecular studies (Patel et al. 2011, Ribas et populations. A number of phylogeographic al. 2011) that have suggested that the modern and population genetics analytical approaches Amazonian drainage system originated during were employed to address these questions the Pleistocene (see above). Fire-eyes seemed (Maldonado-Coelho 2010). to have a complex evolutionary history, The phylogenetic/phyogeographic recon- involving large-scale geological and climatic structions and Bayesian dating estimates processes acting over regional and continental suggest that the origin of the three major scales during the last 2.5 Myr. clades trace back to the formation of the A similar pattern for Amazonian birds modern course of the Amazon, Tapajós, is revealed by the results presented by Ribas Xingu and São Francisco Rivers, with et al. Both the genus Psophia (Gruiformes; subsequent diversification fostered by more Psophiidae) and the genus Rhegmatorhina recent events, such as the origin of the modern (Passeriformes; Thamnophilidae) have current Tocantins River course and by Pleistocene species distributions delimited by large climatic oscillations creating opportunities Amazonian rivers, and both genera diversified for range expansion and geographic isolation during the last 3 Ma. Psophia occurs throughout in the Atlantic Forest. More specifically, the the Amazon Basin and Ribas et al. (2012) showed role of large rivers as barriers to population that the genus comprises eight, rather than the differentiation in fire-eyes is apparently three species previously recognized. Each of stronger in Amazonia than in the Atlantic these eight species occurs in a different area of Forest. A detailed analysis along the Tocantins endemism, and the sequence of diversification River valley provides no support for the events in the genus suggests a sequence for hypothesis that populations were isolated drainage evolution in the basin, with a first split in glacial forest refuges. Instead, the data related to the lower Amazon River, subsequent provide strong support for a key prediction splits related to the upper Negro and Madeira of the river hypothesis and shows that this Rivers, and more recent splits occurring river has likely been the historical mechanism between adjacent interfluvia at the Brazilian underlying population divergence in fire-eyes shield. The first split within Rhegmatorhina, (Maldonado-Coelho et al. submitted). On which does not occur in the Guiana shield, the other hand, climatic oscillations seemed corresponds to the Madeira River. In both less important in creating opportunities for genera there is higher genetic structure within geographic differentiation within the Amazon the Madeira - Tapajós interfluvium (Rondonia in comparison to the Atlantic Forest. area of endemism) when compared to other These results add to mounting evidence Amazonian regions. Signal of recent (last 10.000 that climatic oscillations seem to have played a to 20.000 years) demographic expansion was substantial role in shaping the phylogeographic found for the Psophia species that occur at the structure and possibly the diversification of Guiana and Inambari areas of endemism, while many taxa in the Atlantic Forest (e.g. Cabanne demographic stability was suggested for the et al. 2008; Carnaval et al. 2009, d’Horta et al. Rondonia area of endemism. In Rhegmatorhina,

193 Ribas et al. recent population expansion is suggested for evaluate the role of Amazonian rivers in the all Brazilian shield clades, including the three generation and maintenance of avian species distinct clades found within the Rondonia area diversity, the authors used pairs of parapatric of endemism. Recent population expansion was taxa divided by the Rio Negro. In the Guiana also detected at the Inambari area of endemism. Shield, nearly a third (78 species) of all In both genera there are taxa of similar ages terra-firme forest birds have phenotypically (1.0-1.5 mya) endemic of the lower Negro – differentiated taxa on opposite sides of the lower Solimões – Japurá interfluvium, a region lower Rio Negro (Naka et al. 2012). This suggested as a new area of endemism (Borges pattern of parapatric replacement across et al. 2007, Borges & Silva 2011), and probably the river occurs across a taxonomically and influenced by the evolutionary dynamics of the ecologically diverse array of taxa, representing lower Negro river (Ribas et al. 2012). 22 different avian families and 63 different The results obtained for Psophia and genera, and includes groups as diverse as Rhegmatorhina, combined to recent studies parrots, toucans, woodpeckers, jacamars, and of other avian clades (Armenta et al. 2005; almost every family of passerine birds (Naka Eberhard & Bermingham 2005; Ribas et 2011, Naka et al. 2012). In some cases, these al. 2005; Aleixo et al. 2009; Patel et al. 2011; morphologically distinct populations are d’Horta et al. in press; Aleixo et al. in prep.) considered different species (i.e. Monasa atra show a strong spatial correlation between and Monasa morphoeus), whereas in others, pairs lineage distributions and large Amazonian are regarded as different subspecies of more rivers. Also, molecular dating in all these widespread polytypic taxa (i.e. Ramphastos groups indicates a relatively recent origin (from tucanus tucanus and R. t. couvieri). Despite the about 6.0 to 0.5 Ma) for these Amazonian current taxonomic treatment, which in many species. It is becoming clear that these patterns cases is due to a subjective assessment of are only revealed when taxonomic reviews the amount of phenotypic differentiation are made prior to biogeographic analysis, observed, pairs of taxa are geographical and when sampling is complete (i.e. includes replacements that in general do not occur all basal evolutionary lineages). These results together, thus providing useful pairs to study also indicate that species origins predate the the role of rivers in dividing their populations. strongest glacial cycles (upper Pleistocene), In a recent study, Naka and co-authors (2012) but that these cycles may have influenced provided evidence showing that the phenotypic species distributions, as there are evidences of variation found in pairs of populations across population expansions in several forest taxa the Rio Negro is generally accompanied by during this period. It is important to consider marked genetic differentiation. These results the possibility that the Amazonian drainage has suggest that by inhibiting gene flow, large been very dynamic during the Plio-Pleistocene Amazonian rivers prevent potential species and has played an important role on the origin introgression and, as a result, are important for of current species. maintaining current levels of species diversity. It is less clear, however, whether rivers were The role of rivers in the diversification important in originating current patterns of of birds in the Guiana Shield. Taking a diversity (Haffer 1992, 1997; Colwell 2000; somewhat different approach, Naka et al. Gascon et al. 2000). evaluated distribution patterns and phenotypic Part of the answer may be found in bird or phylogeographic breaks of an entire avian species distributions. Using a comparative community (Naka 2011, Naka et al. 2012). To phylogeographic approach and extensive

194 NEOTROPICAL LOWLAND BIRD DIVERSIFICATION distributional and molecular datasets from Rio Branco are important barriers for many the Guiana Shield, Naka et al. (2012) showed species/subspecies of birds, their role in that only a fourth (21) of the 78 pairs of the diversification process might have been avian taxa divided by the lower Rio Negro quite different. This study supports the idea remain isolated by the upper sections of the that some rivers may have been important as river, implying that the upper Negro may not primary barriers, as suggested by Sick (1967), represent such an overwhelming barrier for Capparella (1988 and 1991), Ayres and Clutter- avian populations. Quite interestingly, most of Brock (1992), and Ribas et al. (2012), whereas those pairs divided by the lower, but not the others possibly represent barriers to secondary upper Negro, are bounded by a second river, contact, as suggested by Haffer along the years the poorly known Rio Branco, which has been (1992, 1997, 2002). shown to divide the distributions of 42 pairs of closely related avian taxa (Naka et al. 2006, Faunal Interchange between Amazonian/ Naka 2011, Naka et al. 2012). Together, these Andean and Atlantic forests. The main two rivers (the Branco and the Negro) are South American forest disjunction, which responsible for dividing the populations of 63 isolates the Andean and Amazonian forests pairs of avian taxa in the Guiana Shield, and from the Atlantic forest, is formed by the offer an ideal setting to better understand the Chaco, Cerrado and Caatinga (Oliveira-Filho & role of rivers in the origin and maintenance of Ratter 1995). This region, known as the “open species diversity. Furthermore, because they diagonal” (Vanzolini 1963), is covered mainly represent very different rivers, in terms of by savannas, woodlands, and dry forests, which size, , color (a proxy for the amount are unsuitable habitats for most lowland forest of sediments), , extent of species. associated flooded forests, and history, they Dispersal or vicariance can be evoked to provide independent examples to test the explain the origin of the current distribution of riverine barrier hypothesis. sister-species (or even populations of the same Using a sample of 60 avian populations species) that occupy Amazonian, Andean and with phenotypic differentiation across the Atlantic forests. In some cases dispersal has lower Rio Negro and the Rio Branco, Naka been considered a valid mechanism to explain et al. (2012) revealed that these pairs present these disjunct distribution patterns (e.g. small disparate levels of genetic divergences (ranging mammals, Costa 2003), as many forest taxa are from 0.5 to 13% of corrected mitochondrial able to use forests at the open diagonal (gallery distance), and their origins probably spanned and dry forest in the Cerrado) as corridors. several geological Periods, from the late However, the high humid forest dependence Miocene to the Pleistocene. Consistent with exhibited by other taxa makes it unlikely that these observations, preliminary results using divergence has occurred by any processes Approximate Bayesian Computation analyses other than vicariance associated with changes do not support a scenario of simultaneous in humid forest distribution. divergence among all pairs of taxa divided by The contact between Atlantic and the lower Rio Negro or the Rio Branco (Naka Amazonian/Andean forests has been analyzed et al. in prep). On the other hand, when only from spatial (Willis 1992, Nores 1992, 1994, pairs divided by the upper Rio Negro are Silva 1994, Cabanne et al. 2008, Costa 2003) used, a scenario of common diversification and temporal perspectives (Ribas & Myiaki cannot be rejected. These results suggest 2007, Cabanne et al. 2008, Costa 2003, d’Horta that whereas both the Rio Negro and the et al. unpublished). Based on distribution

195 Ribas et al. patterns of intra and extra-Atlantic Forest and Atlantic forests. There is a clear pattern avian species, Willis (1992) evaluated five of evolutionary relationships linking lineages possible connection routes between these from southern Atlantic forest with Andean/ domains. Nores (1992, 1994) and Silva (1994), western Amazonia, and northern Atlantic based on the distribution of avian species, forest with eastern Amazonia. Second, the evaluated possible connections throughout scenario of multiple contacts between the the region currently occupied by the Chaco two largest forest blocks of South America and Cerrado. Finally, Costa (2003), analyzing is also supported by the great differences in phylogeographic patterns of small non-volant divergence times estimated between lineages mammals, pointed to potential historical/ associated to these forests (e.g. Cabanne et al. current connections between the Atlantic and 2008; Ribas et al. 2005, 2006, 2007; Derryberry other forests of northern South America. et al. 2011; d’Horta et al. unpublished). Finally, Recent palaeoclimate data shed new the asynchrony of the pulses of increased/ light over this discussion. Cheng et al. (in decreased of precipitation evidenced prep.), analyzing records from western between western and eastern corridors is also Amazonia and available data from eastern corroborated by the historical demography of Amazonia and Atlantic forest regions (e.g. populations associated to these corridors (eg. Cruz et al. 2005, 2009; Wang et al. 2004, 2006), Cabanne et al. 2008, d’Horta et al. 2011). described an east-west dipole-like pattern of Despite the poor attention that faunal precipitation (west dry / east wet and vice interchange among South American forests versa) in cis-Andean South America. This has received so far, the understanding of this climatic pattern suggests the existence of two process is essential to reconstruct the origin preferential corridors between Amazonian/ of the current biodiversity patterns of South Andean and Atlantic forests through which American rainforest birds. past biotic interchanges may have occurred: one connecting eastern Amazonia with the Seasonally deciduous dry forests and northeastern Atlantic Forest (eastern corridor), Neotropical arid biomes. Phylogeographic and the other connecting western Amazonia studies on lowland Neotropical birds have with the southwestern Atlantic Forest (western been heavily focused on species that inhabit corridor). Additionally, the cycles of climate humid forests. While humid forests are very change over the last 250 ky associated to these interesting these environments only represent corridors seem to have been asynchronous one component of the diverse (Cruz et al 2009, Cheng et al in prep.), with found in the lowlands. The lowlands are highly the pulses of increasing/decreasing of rainfall heterogeneous environments often consisting registered to eastern and western corridors of multiple habitats types that can turnover occurring in alternate periods. across small geographic distances (Stotz et al. d’Horta et al. based on available phylogenetic 1996). For example, a matrix of often highly and distributional data of rainforest birds disjunct arid habitats, known as seasonally conducted a preliminary evaluation of the deciduous dry forest (Prado 2000), occurs from predictions derived from the model described Mexico through Argentina. Understanding above. Results indicated that, first, the spatial speciation patterns and the tempo of patterns of distribution of sister species, or diversification in taxa distributed across these populations from the same species, strongly regions and other non-rainforest habitats will support the past existence of these two provide critical insight into the evolution and preferential corridors connecting Amazonian assembly of Neotropical avifaunas. Currently,

196 NEOTROPICAL LOWLAND BIRD DIVERSIFICATION we do not know whether dry taxa evolved in to the user’s delimitation of biodiversity. response to the same mechanisms as humid Analyses that used biological species as forest taxa or alternatively, whether dry taxa biodiversity units supported a model of were impacted by different historical processes. declining rates of diversification over time. It can be predicted that when climatic Alternatively, analyses that used subspecies conditions became drier during glacial cycles or phylogenetic species supported a model of and the ranges of humid taxa contracted, arid constant diversification over time. Overall, biota taxa should have expanded their ranges. these findings suggest that thorough range- Constant phases of expansion and contraction wide sampling of taxa is important for should have left distinct patterns of genetic inferring models of speciation and that structure across the landscape. the current species designations poorly To assess evolutionary patterns in the more describe the extant diversity. Moreover, this arid regions of the Neotropical lowlands, Smith preliminary evidence indicates that humid and et al. presented findings on spatial and temporal dry taxa both exhibit similar patterns of deep patterns of diversification in Forpus parrotlets genetic structure across the landscape and this a group that largely inhabits dry forests and structure appears to have been generated at more-open habitats. An objective of the study a constant rate over time. Future comparative was to compare diversification rates estimated phylogeographic studies will need to assess from multilocus data from estimates using whether these analogous patterns in humid only mitochondrial DNA. Smith et al. found and dry taxa have occurred during the same that in Forpus, multilocus and mitochondrial time periods or in contrast, whether these taxa DNA estimates of diversification rates were evolved in response to different mechanisms. similar and that the best-fit model suggested a constant diversification rate across time. This NEW METHODS AND pattern of constant diversification in Forpus PERSPECTIVES is similar to the mode of speciation shown in other Neotropical birds, such as ovenbirds Research on the evolution of the Neotropical (Derryberry et al. 2011) and toucans (Patel et avifauna has its roots in natural history, al. 2011). These findings are contrary to the which has since expanded into a highly hypothesis that speciation rates are predicted integrative field utilizing population genetics, to decline over time as niche space fills-up computational biology, and . (Rabosky 2008, Phillimore & Price 2008). The The molecular age has provided researchers striking disparities between these findings are with an unprecedented toolkit for inferring not yet clear; however; sampling biases have aspects such as historical demography and the been shown to impact diversification rate timing and patterns of speciation events. Over estimates (Cusimano & Renner 2010). the last ten years phylogeographic studies Smith et al. assessed the role taxonomic have been transitioning from single locus units and sampling may have on the estimation mitochondrial DNA studies to multilocus of diversification rates. Diversification rate studies, and now are expanding into genomics analyses rely on sampling the extant diversity using next-generation sequencing. Next- of a group, but the scale at which diversity generation sequencing has already shown great should be sampled is not apparent. Should promise in avian systematics and has been we include biological species, subspecies, or used to evaluate deep (Faircloth et al. 2012) and phylogenetic species? Smith et al. found that shallow (McCormack et al. 2012) evolutionary diversification rate analyses may be sensitive questions in the avian Tree of Life.

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The number of analytical procedures and of spatially explicit demographic simulations software packages available to researchers has (DIM SUM, Brown et al. 2009) can be used greatly increased the questions phylogeographic to generate expected diversification patterns studies are able to test. The APE (Paradis et al. across heterogeneous landscapes. 2004), LASER (Rabosky 2006), and GEIGER One challenge faced in phylogeographic (Harmon et al. 2008) software packages in studies is how to perform comparative analyses the R language allow researchers to estimate on complex datasets. Often phylogeographic diversifications rates and test different models studies focus on taxa with widespread of speciation. Reconstructing ancestral areas distributions that exhibit considerable genetic continues to be an important biogeographic structure. This complexity often does not fit question and range evolution programs have the assumptions of the available analytical become more complex allowing researchers methods. Many of the existing coalescent to incorporate speciation and extinction programs, such as, msBayes are designed rates (LAGRANGE; Ree & Smith 2008), to estimate parameters within unstructured phylogenetic uncertainty (S-DIVA; Yu et populations. Further difficulty occurs when al. 2010), and hypothesis testing of spatial the diversification of lineages encompasses patterns of dispersal (PHYLOMAPPER, multiple temporal scales. Deeper Miocene- Lemmon & Lemmon 2008). The BEAST Pliocene divergences are often best analyzed software package offers an array of different using phylogenetic approaches. In contrast, analyses including divergence time estimation Pleistocene divergences are better suited (Dummond & Rambaut 2007), species tree for coalescent methods that can account for estimation (Heled & Drummond 2010), lineage sorting, gene flow and population demographic history (Drummond et al. 2005), size changes. Phylogeographers have been and spatial diffusion models (Lemey et al. 2009). provided a powerful statistical toolkit, but are For population genetic studies, structured challenged to decide the most appropriate coalescent models have been expanded approach given their data and the assumptions and can be used to simultaneously estimate of the existing software packages. multiple population genetic parameters (IMa, Hey & Neilsen 2007; LAMARC, Kuhner 2006; FUTURE DIRECTIONS MIGRATE, Beerli & Felsenstein 2001) across multiple populations. The development of A central goal of Neotropical phylogeographers programs to simulate genealogies assuming has been to understand how Earth history specific population models of evolution, such has shaped biotic diversification. Studies on as SIMCOAL2 (Laval & Excoffier 2004) and diversification and Earth history range from SERIAL SIMCOAL (Anderson et al. 2005), climatic changes (Cabanne et al. 2008, Horta and of the approximate Bayesian Computation et al. 2011), divergence across forest-savanna (ABC) approaches offers researchers the ecotones (Cabanne et al. 2011), Andean uplift potential to test a range of diversification (Brumfield & Capparella 1996, Ribas et al. 2007), scenarios and complex demographic histories. the closure of the Panamanian land bridge The ABC packages msBAYES (Hickerson (Smith & Klicka 2010), and formation of the et al. 2007) and ABCTOOLBOX (Wegmann Amazon drainage basin (Ribas et al. 2012). et al. 2010) have quickly become a popular However, phylogeographic structure and genetic toolkit for testing for simultaneous divergence diversity patterns are not only shaped by these in multiple co-distributed taxa (i.e. Barber & deep historical factors, but also by contemporary Klicka 2010). Finally, the recent development (Smith et al. 2011) and stochastic processes

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(Miller et al. 2010). One factor that may play an current landscapes bias our interpretations. important role in understanding diversification Future phylogeographic studies will have to patterns is species ecology. Foraging strata has distinguish between the role of landscape been shown to have a significant impact on evolution in generating biodiversity from the degree of genetic differentiation across the role of landscape features in maintaining biogeographic barriers (Burney & Brumfield genetic differentiation between taxa. 2009). Species that inhabit the understory Finally, how robust are inferences of humid forests have been shown to have of speciation history to changes in our higher genetic distances across the Andes, and understanding of Earth history? Geology is Amazon and Madeira Rivers than do species a dynamic and changing field. As an example, that inhabit the canopy (Burney & Brumfield new evidence has suggested that the closure 2009). Moreover, dispersal across biogeographic of the Panamanian land bridge and the uplift barriers may be facilitated by changing climatic of the northern Andes may be older than conditions allowing environmental conditions previously understood (Farris et al. 2011, to become more favorable for certain species Montes et al. 2012). Speciation inferences (Smith et al. submitted). involving these geologic events are often As more data becomes available, it is constructed around a Late Pliocene timeframe. becoming apparent that there is wide degree Phylogeographers need to be careful to not of variance in speciation patterns and timing force the timing of speciation events into of diversification across the Neotropical an “expected” time period (i.e. Rheindt et al. lowlands. For example, results presented in 2009) because molecular clocks are often this symposium indicate that some understory calibrated from the same historical events birds such as S. virescens might present no we study. Ideally, phylogeographers need to phylogeographic structure, contrarily to what assess the robustness of speciation scenarios is expected from other studies on ecologically using independent evidence. Going forward, similar forest birds (Burney & Brumfield 2009, Neotropical phylogeographers will be faced Nyari 2007, Cabanne et al. 2008). This variance with the challenge of disentangling the role of likely indicates that Earth history and species Earth history, species ecology, and stochasticity ecology are not the only important factors. to understand evolutionary patterns in one of Stochasticity and extinction likely have left a the most species rich areas on Earth. strong signature in speciation patterns and pose serious challenges for reconstructing a shared ACKNOWLEDGMENTS history among co-distributed species (Haydon et al. 1994). Additionally, new data has shown All authors would like to thank the IX NOC Neotropical speciation is much more complex Scientific Program Committee for their than the traditional models have proposed. organizing efforts. CCR thanks FAPESP, New large-scale analyzes on Amazonian birds FAPEAM, CNPq, CAPES, Frank Chapman M. are changing our interpretations on the role of Fund (AMNH) for funding, and all collectors rivers as barriers to gene flow (Nakaet al. 2012). and collections that have obtained, organized, These new findings suggest that Amazonian kept, made available, and loaned samples to the rivers can be a spatially dynamic barrier and projects that originated the results presented the strength of a river as a barrier changes in this symposium. MMC is thankful to J. G. from the lower reaches to the headwaters Blake, R. E. Ricklefs, B. Loiselle, J. Bates and (Naka et al. 2012). Given that landscapes are C. Miyaki for guidance throughout his PhD ephemeral and ever changing it is unclear how and Pos-Doctorate projects, and to FAPESP,

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CNPq (overseas doctoral fellowship), National phylogeographic perspective on the role Science Foundation (Doctoral Dissertation of different hypotheses of Amazonian Improvement Grant OISE-0555482), diversification.Evolution , 58: 1303-1317. Whitney R. Harris World Ecology Center Aleixo, A., Burlamaqui, T., Schneider, M.P.C., (Parker-Gentry Fellowship) at University of Gonçalves, E.C. 2009. Molecular systematics Missouri-St. Louis, and the AMNH (Frank and plumage evolution in the monotypic Chapman Memorial Fund) for funding. BTS obligate army-ant-following genus Skutchia would like to acknowledge R. T. Brumfield, J. (Thamnophilidae). The Condor 111(2):382–387. Klicka, A. Cuervo and B. Hernandez-Baños. Almeida-Filho R, Miranda FP (2007) Mega capture GSC is thankful to CAPES, Consejo Nacional of the Rio Negro and formation of the de Investigaciones Científicas y Técnicas, Anavilhanas Archipelago, Central Amazônia, FAPEMIG, FAPESP and WWF for financial Brazil: Evidences in an SRTM digital elevation support, and to C. Miyaki for guidance during model. Remote Sens Environ 110:387–392. his PhD. Also, GSC is grateful to E. Sari., Anderson CNK, Ramakrishnan U, Chan YL, Hadly D Meyer, F. Santos and C. Miyaki for their EA. 2005 Serial SimCoal: A population genetics participation in the study of Schiffornis virescens model for data from multiple populations and presented in this symposium. FMH is grateful points in time. Bioinformatics 21 (8):1733-1734. to F. W. Cruz, who provided insightful ideas, Armenta J.K., Weckstein J.D., Lane D.F. 2005. C. Miyaki, D. Meyer and P. E. Vanzolini for Geographic variation in mitochondrial DNA their guidance during his PhD project, CAPES sequences of an Amazonian nonpasserine: the and FAPESP for financial support. LNN is Black-spotted Barbet complex. Condor 107: 527- grateful to R. T. Brumfield and J. V. Remsen for 536 comments and guidance throughout his PhD Auler, A.S., Piló, L.B., Smart, P.L., Wang, X., project. LNN was supported by a doctoral Hoffmann, D., Richards, D.A., Edwards, R.L., international scholarship from the Instituto Neves, W.A., Cheng, H. 2006. U-series dating Internacional de Educação do Brasil (IEB; and taphonomy of Quaternary vertebrates from Programa BECA) and an overseas doctoral Brazilian caves. , Palaeoclimatology, fellowship from CNPq (202131/2006-8). Palaeoecology, 240: 508-522. Funding was provided by NSF (Doctoral Ayres, J.M. & T.H. Clutton-Brock. 1992. River Dissertation Improvement Grant 1011512, boundaries and species range size in Amazonian and grants 0400797 and 0841729 to R.T. primates. American Naturalist 140: 531-537. Brumfield), AMNH (Frank Chapman Barber, B. & J. Klicka. 2010. Two pulses of Memorial Fund), AOU, IdeaWild, LSU, Sigma diversification across the Isthmus of Xi, and CNPq (grants 486253/2006-6 to L.M.P. Tehuantepec in a montane Mexican bird fauna. Henriques and 484219/2011-1). LNN would Proc R Soc 277:2675-2681. like to thank the financial support provided by Batalha-Filho H, Waldschmidt AM, Campos the editorial board of The Condor and the LAO, Tavares MG, Fernandes-Salomão Cooper Ornithological Society, particularly TM. 2010. Phylogeography and historical M. Patten and B. Smith-Patten, who made demography of the Neotropical stingless bee possible his participation in the IX NOC. Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and REFERENCES mitochondrial DNA. Apidologie 41(5). Bates, J. M & T. C. Demos. 2001. Do we need to Aleixo, A. 2004. Historical diversification of devalue Amazonia and other large tropical fo- a Terra-firme forest bird superspecies: a rests? Divers. Distrib. 7: 249–255.

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