Climatic dynamics and topography control genetic variation in Atlantic Forest montane birds.

Montane organisms responded to Quaternary climate change by tracking suitable habitat along elevational gradients. However, it is unclear whether these past climatic dynamics generated predictable patterns of genetic diversity in co-occurring montane taxa. To test if the genetic variation is associated with historical changes in the elevational distribution of montane habitats, we integrated paleoclimatic data and a model selection approach for testing the demographic history of five co-distributed bird species occurring in the southern Atlantic Forest sky islands. We found that changes in historical population sizes and current genetic diversity are attributable to habitat dynamics among time periods and the current elevational distribution of populations. Taxa with populations restricted to the more climatically dynamic southern mountain block (SMB) had, on average, a six-fold demographic expansion, whereas the populations from the northern mountain block (NMB) remained constant. In the current configuration of the southern Atlantic Forest montane habitats, populations in the SMB have more widespread elevational distributions, occur at lower elevations, and harbor higher levels of genetic diversity than NMB populations. Despite the apparent coupling of demographic and climatic oscillations, our data rejected simultaneous population structuring due to historical habitat fragmentation. Demographic modeling indicated that the species had different modes of differentiation, and varied in the timing of divergence and the degree of gene flow across mountain blocks. Our results suggest that the heterogeneous distribution of genetic variation in birds of the Atlantic Forest sky islands is associated with the interplay between topography and climate of distinct mountains, leading to predictable patterns of genetic diversity.

Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds.

The role of historical factors in establishing patterns of diversity in tropical mountains is of interest to understand the buildup of megadiverse biotas. In these regions, the historical processes of range fragmentation and contraction followed by dispersal are thought to be mediated by the interplay between rugged relief (complex topography) and climate fluctuations and likely explain most of the dynamics of diversification in plants and animals. Although empirical studies addressing the interaction between climate and topography have provided invaluable insights into population divergence and speciation patterns in tropical montane organisms, a more detailed and robust test of such processes in an explicit spatio-temporal framework is still lacking. Consequently, our ability to gain insights into historical range shifts over time and the genomic footprint left by them is limited. Here, we used niche modeling and subgenomic population-level datasets to explore the evolution of two species of warbling finches (genus Microspingus) disjunctly distributed across the Montane Atlantic Forest, a Neotropical region with complex geological and environmental histories. Population structure inferences suggest a scenario of three genetically differentiated populations, which are congruent with both geography and phenotypic variation. Demographic simulations support asynchronous isolation of these populations as recently as ∼40,000 years ago, relatively stable population sizes over recent time, and past gene flow subsequent to divergence. Throughout the last 800,000 years, niche models predicted extensive expansion into lowland areas with increasing overlap of species distributions during glacial periods, with prominent retractions and isolation into higher altitudes during interglacials, which are in line with signs of introgression of currently isolated populations. These results support a dual role of cyclical climatic changes: population divergence and persistence in mountain tops during warm periods followed by periods of expansion and admixture in lower elevations during cold periods. Our results underscore the role of the interplay between landscape and climate as an important mechanism in the evolution of the Neotropical montane biota.