| Abstract: | The linking of North and South America by the Isthmus of Panama had major impacts on global climate, oceanic and atmospheric currents, and biodiversity, yet the timing of this critical event remains contentious. The Isthmus is traditionally understood to have fully closed by ca. 3.5 million years ago (Ma), and this date has been used as a benchmark for oceanographic, climatic, and evolutionary research, but recent evidence suggests a more complex geological formation. Here, we analyze both molecular and fossil data to evaluate the tempo of biotic exchange across the Americas in light of geological evidence. We demonstrate significant waves of dispersal of terrestrial organisms at approximately ca. 20 and 6 Ma and corresponding events separating marine organisms in the Atlantic and Pacific oceans at ca. 23 and 7 Ma. The direction of dispersal and their rates were symmetrical until the last ca. 6 Ma, when northern migration of South American lineages increased significantly. Variability among taxa in their timing of dispersal or vicariance across the Isthmus is not explained by the ecological factors tested in these analyses, including biome type, dispersal ability, and elevation preference. Migration was therefore not generally regulated by intrinsic traits but more likely reflects the presence of emergent terrain several millions of years earlier than commonly assumed. These results indicate that the dramatic biotic turnover associated with the Great American Biotic Interchange was a long and complex process that began as early as the Oligocene–Miocene transition.The Isthmus of Panama is the narrow strip of land that connects North and South America and divides the Atlantic and Pacific oceans. The emergence of the Isthmus initiated one of the largest episodes of biological migration between previously disconnected landmasses, the Great American Biotic Interchange (GABI) (1–5), one of the best natural experiments on invasive species. The closure of the Central American Seaway (CAS, the oceanic pathway along the tectonic boundary between South America and the Panama Block) and rise of the Isthmus have been linked to the onset of both thermohaline oceanic circulation and northern hemisphere glaciation (6–8). Despite its broad importance, the formation of the Isthmus and its impact on the rich biodiversity of the Americas remains contentious (9). Therefore, a better understanding of when the formation of the Isthmus of Panama occurred has important implications in several scientific fields across multiple disciplines.The timing of Isthmus formation has been assessed through different proxies. Previous studies have long suggested full closure by 3.5 Ma (7, 8, 10–16). More recent geological work has suggested a longer and more complex formation, where the initial collision between South America and the Panama Block occurred between 25 and 23 Ma (17). By 20 Ma the Panama Block is suggested to have been connected to North America (18–21) and the width of the CAS to be 200 km (19, 20). Full closure of the CAS occurred by 10 Ma, ending the exchange of deep and intermediate waters between the Caribbean and the Pacific (11, 19, 20, 22–24). However, the exchange of shallow waters between these oceans likely continued along pathways other than the CAS for many millions of years (7, 8, 10–16, 25).Over the past two decades, hundreds of studies have assumed the Isthmus of Panama to have closed at 3.5 Ma (SI Appendix), causing the separation of widespread marine populations into distinct Pacific and Caribbean groups (vicariance) and the first possible dispersals between North and South America (with the exception of stochastic long-distance dispersals). Here, we address the following questions: Given the complexities and the recent evidence of a much older geological history of the Isthmus of Panama, is 3.5 Ma an adequate age for those events? Were the suggested water corridors across the Isthmus—even if shallow and narrow—indeed effective barriers against both dispersal of terrestrial organisms and conduits of marine ones until a full closure at 3.5 Ma? We address these questions using comprehensive biological data from living and fossil organisms, where the assumption is that any well-developed terrestrial corridor would lead to both more frequent biotic dispersal between North and South America as well as a division of widespread marine organisms into distinct Caribbean and Pacific lineages (26). Biological data provide a powerful tool for this purpose compared with geological evidence, which cannot inform on the subtle differences between exposed land and shallow waters that can be crucial to the dispersal of organisms.Recent attempts to synthesize dispersal patterns across the Isthmus of Panama are based on dated phylogenies (27–29) that have included data that used a 3.5 Ma Isthmus closure as a calibration point (e.g., in calculating mutation rate). These assumptions lead to circularity if the goal is to examine timing of dispersal or vicariance across the Isthmus. Our molecular analyses differ from previous studies both qualitatively (by the elimination of the timing of the emergence of the Isthmus of Panama and the contrast between patterns in marine and terrestrial taxa) and quantitatively (735% more data points than a previous cross-taxonomic analysis) (27) and serve as a comparison with a comprehensive fossil dataset.Another crucial aspect of the formation of the Isthmus of Panama and its impact on biological diversity entails the direction of terrestrial dispersal (e.g., north to south) and the ecology of dispersing organisms. In his seminal work on the GABI, Simpson (1) used the mammal fossil record to suggest that North American taxa had a competitive advantage over the South American fauna in that more North American taxa dispersed, survived, and diversified in southern ranges. Recent studies have suggested that ecological barriers to dispersal, such as dry savanna-like environments (30) or reduced rain forest cover (31), also prevented tropical South American taxa from migrating successfully to the north.To explicitly address the timing of the formation of the Isthmus of Panama and its effect on geographical distributions of biota, we develop a Migration Rates Through Time (MRTT) model. Using this approach, in which migration is defined as dispersal and vicariance events collectively, we conduct an analysis of over 400 data points (SI Appendix, 1.2) of molecular divergence dates conferring dispersal events between North and South America or vicariance between the eastern Pacific and the Caribbean Sea. We compare results from extant data with over 23,000 records of American fossil mammals. Our results corroborate recent geological evidence that rather than a Pliocene, time-limited, single event, the formation of the Isthmus of Panama and the GABI were long and complex processes that began as early as the Oligocene–Miocene transition. We also show incongruent patterns in the direction of migration when comparing the molecular and fossil data, possibly reflecting differential diversification rates following dispersal. None of the ecological factors measured in the analyses can explain the statistical differences in the timing of migration across the Isthmus region among different taxa, and together with the MRTT results, this suggests that rather than intrinsic (biological) traits, extrinsic factors such as the presence of emergent land likely drove these patterns. |
