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Significance The biological interchange between North and South America associated with the formation of the Isthmus of Panama is key to defining current gradients of species diversity. A major gap in our understanding of the interchange is its asymmetry, where mammals of North American origin attained higher diversity in South America than vice versa. The prevailing view is that this asymmetry resulted from higher origination of immigrant mammals in South America. In contrast, we find that asymmetry results from high extinction of native mammals in South America, which reduced the diversity of native mammals available to disperse northwards. These results shed light on the legacy of the biotic interchange to understand the current patterns of species diversity across the Americas., The interchange between the previously disconnected faunas of North and South America was a massive experiment in biological invasion. A major gap in our understanding of this invasion is why there was a drastic increase in the proportion of mammals of North American origin found in South America. Four nonmutually exclusive mechanisms may explain this asymmetry: 1) Higher dispersal rate of North American mammals toward the south, 2) higher origination of North American immigrants in South America, 3) higher extinction of mammals with South American origin, and 4) similar dispersal rate but a larger pool of native taxa in North versus South America. We test among these mechanisms by analyzing ∼20,000 fossil occurrences with Bayesian methods to infer dispersal and diversification rates and taxonomic selectivity of immigrants. We find no differences in the dispersal and origination rates of immigrants. In contrast, native South American mammals show higher extinction. We also find that two clades with North American origin (Carnivora and Artiodactyla) had significantly more immigrants in South America than other clades. Altogether, the asymmetry of the interchange was not due to higher origination of immigrants in South America as previously suggested, but resulted from higher extinction of native taxa in southern South America. These results from one of the greatest biological invasions highlight how biogeographic processes and biotic interactions can shape continental diversity.

Patterns of molecular coevolution can reveal structural and functional constraints within or among organic molecules. These patterns are better understood when considering the underlying evolutionary process, which enables us to disentangle the signal of the dependent evolution of sites (coevolution) from the effects of shared ancestry of genes. Conversely, disregarding the dependent evolution of sites when studying the history of genes negatively impacts the accuracy of the inferred phylogenetic trees. Although molecular coevolution and phylogenetic history are interdependent, analyses of the two processes are conducted separately, a choice dictated by computational convenience, but at the expense of accuracy. We present a Bayesian method and associated software to infer how many and which sites of an alignment evolve according to an independent or a pairwise dependent evolutionary process, and to simultaneously estimate the phylogenetic relationships among sequences. We validate our method on synthetic datasets and challenge our predictions of coevolution on the 16S rRNA molecule by comparing them with its known molecular structure. Finally, we assess the accuracy of phylogenetic trees inferred under the assumption of independence among sites using synthetic datasets, the 16S rRNA molecule and 10 additional alignments of protein-coding genes of eukaryotes. Our results demonstrate that inferring phylogenetic trees while accounting for dependent site evolution significantly impacts the estimates of the phylogeny and the evolutionary process.

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 emergence of the Isthmus of Panama left a major imprint on the biodiversity of the Americas. The connection between South and North America facilitated dispersal of terrestrial and freshwater organisms, while separating marine species between the eastern Pacific and Caribbean seas. Recent geological data have questioned the long-standing view of a Pliocene emergence of the Isthmus (1) and show that the Central American Seaway, defined as the deep oceanic seaway along the tectonic boundary of the South American plate and Panama arc, was already closed by 15–13 Ma (2). Caribbean–Pacific shallow water exchange probably continued, albeit intermittently, until a full closure at 3.5 Ma (1–3). Recently Bacon et al. (3) used molecular and fossil data to evaluate the timing, tempo, and directionality of biotic exchange and vicariance across the Isthmus, and tested whether biological data are congruent with recent geological evidence. Significant increases in terrestrial dispersals were found at ca. 20 and 6 Ma, and increases in marine vicariance at ca. 23 and 7 Ma. Similar patterns prevailed despite intrinsic differences among the taxonomic groups surveyed. This led Bacon et al. (3) to reject the assumption of a single closure of the Isthmus at ca. 3.5 Ma in favor of an older, more complex model of land emergence and biotic interchange.