The drivers of tropical speciation

Since the recognition that allopatric speciation can be induced by large-scale reconfigurations of the landscape that isolate formerly continuous populations, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers, landscape change has been viewed as a primary driver of biological diversification. This process is referred to in biogeography as vicariance. In the most species-rich region of the world, the Neotropics, the sundering of populations associated with the Andean uplift is ascribed this principal role in speciation. An alternative model posits that rather than being directly linked to landscape change, allopatric speciation is initiated to a greater extent by dispersal events, with the principal drivers of speciation being organism-specific abilities to persist and disperse in the landscape. Landscape change is not a necessity for speciation in this model. Here we show that spatial and temporal patterns of genetic differentiation in Neotropical birds are highly discordant across lineages and are not reconcilable with a model linking speciation solely to landscape change. Instead, the strongest predictors of speciation are the amount of time a lineage has persisted in the landscape and the ability of birds to move through the landscape matrix. These results, augmented by the observation that most species-level diversity originated after episodes of major Andean uplift in the Neogene period, suggest that dispersal and differentiation on a matrix previously shaped by large-scale landscape events was a major driver of avian speciation in lowland Neotropical rainforests. In the species-rich Neotropics, the origins of biodiversity are usually linked to changes to the Earth’s landscape over geological time. Palaeogeographic studies indicate that Andean mountain building during the Neogene catalysed tumultuous changes in the lowlands, including formation of the Amazon River system, closure of the Isthmus of Panama, and the isolation of humid lowland forests east and west of the Andes by montane habitats and the aridification of the Caribbean lowlands in northern South America. These large-scale landscape changes are hypothesized to have driven speciation by fragmenting species distributions that were formerly continuous, a process that can generate congruent spatial and temporal patterns of genetic differentiation in co-distributed lineages, especially for lineages with similar ecological characteristics. Bolstering support for the importance of landscape change driving isolation in this region, time-calibrated phylogenies of a taxonomically diverse group of organisms encompassing a broad range of ecologies and dispersal abilities indicate that many modern Neotropical lineages originated during time periods associated with major reconfigurations of the landscape, presumably signifying a shared response to landscape history. An alternative hypothesis is that the principal effect of Andean mountain building in the Neogene on speciation was the formation of a geographically structured landscape matrix upon which subsequent diversification occurred. Within the humid lowland forests of the Neotropics the landscape contains mountains and rivers that restrict the movement of individuals across them (we use the term dispersal for these movements). Under this model, lineages with a longer occupation of the landscape have a higher likelihood of dispersing across geographical barriers and diversifying. In addition, lineages with lower dispersal ability are expected to accrue genetic differentiation between populations at a relatively higher rate than more dispersive lineages, leading to a higher rate of speciation. In this model, lineage-specific attributes are predicted to be the primary determinants of species diversity within lineages. These two models of diversification in the Neotropics have been difficult to evaluate empirically because: (1) large-scale comparative data are needed from multiple co-distributed lineages; (2) each lineage needs to be sampled densely across its range to identify phylogeographic breaks and to estimate within-lineage species diversity; (3) the sampled lineages must encompass a range of quantifiable dispersal abilities and ecological guilds in order to test how these variables affect speciation; and (4) the phylogenetic position of each lineage must be known to approximate lineage age. We assessed the relative support for these two models in explaining standing species-level variation by characterizing recent large-scale diversification using a comparative phylogeography data set containing over 2,500 individuals from 27 widespread bird lineages in the speciesrich Neotropics (Supplementary Table 17 and Figs 1 and 2). Biological species often represent an inaccurate estimate of the true diversity in avian rainforest communities because the alpha taxonomies of most groups still require formal revision using modern methods. To minimize biases associated with species limits based on current taxonomy, we defined each lineage as all populations of a given taxon that represent, on the basis of available evidence, a monophyletic group, regardless of whether the lineage is currently treated as a single species or as a species complex that includes several closely related species. By examining relatively recent diversification at the phylogeographic scale, where extinction is less likely to have occurred, we minimized the confounding effects of extinction. Extinction is difficult to account for analytically and typically increases with time. The Andes, the Isthmus of Panama and large rivers of the Amazon Basin (the Amazon, Madeira and Negro rivers) are prominent features of the Neotropical landscape that interrupt the distributions of the 27 focal lineages to varying degrees (Fig. 1 and Supplementary Figs 1–27). The effect of the landscape on diversification is evident taxonomically, with distinct taxa usually located on opposite banks of Amazonian rivers, the Isthmus of Panama and the Andes. Biogeographers often treat regions delimited by these dispersal barriers as areas of endemism because of the accumulation within them of distinct taxa having common distributional ranges (Extended Data Fig. 1). The exact time of origin of the dispersal barriers separating these areas is debated, but most data