Christine D. Bacon

Biological evidence supports an early and complex emergence of the Isthmus of Panama

Significance The formation of the Isthmus of Panama, which linked North and South America, is key to understanding the biodiversity, oceanography, atmosphere, and climate in the region. Despite its importance across multiple disciplines, the timing of formation and emergence of the Isthmus and the biological patterns it created have been controversial. Here, we analyze molecular and fossil data, including terrestrial and marine organisms, to show that biotic migrations across the Isthmus of Panama began several million years earlier than commonly assumed. An earlier evolution of the Isthmus has broad implications for the mechanisms driving global climate (e.g., Pleistocene glaciations, thermohaline circulation) as well as the rich biodiversity of the Americas. 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.

Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record

Summary Plants have a long evolutionary history, during which mass extinction events dramatically affected Earths ecosystems and its biodiversity. The fossil record can shed light on the diversification dynamics of plant life and reveal how changes in the origination–extinction balance have contributed to shaping the current flora. We use a novel Bayesian approach to estimate origination and extinction rates in plants throughout their history. We focus on the effect of the ‘Big Five’ mass extinctions and on estimating the timing of origin of vascular plants, seed plants and angiosperms. Our analyses show that plant diversification is characterized by several shifts in origination and extinction rates, often matching the most important geological boundaries. The estimated origin of major plant clades predates the oldest macrofossils when considering the uncertainties associated with the fossil record and the preservation process. Our findings show that the commonly recognized mass extinctions have affected each plant group differently and that phases of high extinction often coincided with major floral turnovers. For instance, after the Cretaceous–Paleogene boundary we infer negligible shifts in diversification of nonflowering seed plants, but find significantly decreased extinction in spore‐bearing plants and increased origination rates in angiosperms, contributing to their current ecological and evolutionary dominance.

An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics

Understanding the processes that have generated the latitudinal biodiversity gradient and the continental differences in tropical biodiversity remains a major goal of evolutionary biology. Here we estimate the timing and direction of range shifts of extant flowering plants (angiosperms) between tropical and non-tropical zones, and into and out of the major tropical regions of the world. We then calculate rates of speciation and extinction taking into account incomplete taxonomic sampling. We use a recently published fossil calibrated phylogeny and apply novel bioinformatic tools to code species into user-defined polygons. We reconstruct biogeographic history using stochastic character mapping to compute relative numbers of range shifts in proportion to the number of available lineages through time. Our results, based on the analysis of c. 22,600 species and c. 20 million geo-referenced occurrence records, show no significant differences between the speciation and extinction of tropical and non-tropical angiosperms. This suggests that at least in plants, the latitudinal biodiversity gradient primarily derives from other factors than differential rates of diversification. In contrast, the outstanding species richness found today in the American tropics (the Neotropics), as compared to tropical Africa and tropical Asia, is associated with significantly higher speciation and extinction rates. This suggests an exceedingly rapid evolutionary turnover, i.e., Neotropical species being formed and replaced by one another at unparalleled rates. In addition, tropical America stands out from other continents by having “pumped out” more species than it received through most of the last 66 million years. These results imply that the Neotropics have acted as an engine for global plant diversity.

Delimitation of the Segregate Genera of Maytenus s. l. (Celastraceae) Based on Morphological and Molecular Characters

Abstract Maytenus s. l. (including Gymnosporia) is a morphologically diverse genus of about 300 species that is widely distributed in the tropics and subtropics of both the Old and New Worlds. Its delimitation has been extensively debated and despite the segregation of Gymnosporia, Maytenus s. s. remains a heterogeneous, polyphyletic group. To delimit natural segregate genera we increased taxon sampling and generated sequences from two nuclear gene regions (ITS and 26S rDNA) and two plastid loci (matK and trnL-F) to analyze together with morphological characters. Both Moya and Tricerma were found to be nested within the New World Maytenus and are recognized as synonyms of Maytenus s. s.. In contrast, the three New World species of Gymnosporia are recognized as a new genus that is closely related to Gyminda. Haydenia is erected for these three species: H. gentryi, H. haberiana , and H. urbaniana . One or more previously proposed or novel genera are required to accommodate the systematically difficult African Maytenus. Putterlickia, and most likely Gloveria, are nested within Gymnosporia and should be synonymized with that genus. New binomials are required for four Chinese and one Rapan species of Gymnosporia that have been previously treated only as Maytenus: Gymnosporia austroyunnanensis, G. confertiflora, G. dongfangensis, G. guangxiensis , and G. pertinax . Austral-Pacific Maytenus are transferred to Denhamia, requiring eight new binomials: Denhamia bilocularis, D. cunninghamii, D. cupularis, D. disperma, D. fasciculiflora, D. ferdinandii, D. fournieri , and D. silvestris . Existing intrageneric classifications of Gymnosporia and Maytenus s. s. were not supported in their entirety. Gymnosporia is inferred to have had an African origin followed by dispersals to Madagascar, southeast Asia and the Austral-Pacific.

Quaternary glaciation and the Great American Biotic Interchange

Recent geological studies demonstrate that the Isthmus of Panama emerged some 10 m.y. earlier than previously assumed. Although absent today in Panama, Central American savanna environments likely developed in connection with the onset of Northern Hemisphere glaciations. As is widely recognized, most of the mammals crossing the isthmus since 2.5 Ma lived in savannas. Could climate-induced vegetational changes across Panama explain the delayed migration of mammals, rather than terrestrial connectivity? We investigate the congruence between cross-continental mammal migration and climate change through analysis of fossil data and molecular phylogenies. Evidence from fossil findings shows that the vast majority of mammals crossed between South and North America after ca. 3 Ma. By contrast, dated mammal phylogenies suggest that migration events started somewhat earlier, ca. 4–3 Ma, but allowing for biases toward greater ages of molecular than geologic dating and uncertainties in the former, we consider this age range not to be significantly earlier than 3 Ma. We conclude that savanna-like environments developed in response to the vast Laurentide ice sheet at the first Quaternary glaciation triggered the initiation of the Great American Biotic Interchange in mammals.

Reply to Lessios and Marko et al.: Early and progressive migration across the Isthmus of Panama is robust to missing data and biases

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.

Fossil biogeography: a new model to infer dispersal, extinction and sampling from palaeontological data.

Methods in historical biogeography have revolutionized our ability to infer the evolution of ancestral geographical ranges from phylogenies of extant taxa, the rates of dispersals, and biotic connectivity among areas. However, extant taxa are likely to provide limited and potentially biased information about past biogeographic processes, due to extinction, asymmetrical dispersals and variable connectivity among areas. Fossil data hold considerable information about past distribution of lineages, but suffer from largely incomplete sampling. Here we present a new dispersal–extinction–sampling (DES) model, which estimates biogeographic parameters using fossil occurrences instead of phylogenetic trees. The model estimates dispersal and extinction rates while explicitly accounting for the incompleteness of the fossil record. Rates can vary between areas and through time, thus providing the opportunity to assess complex scenarios of biogeographic evolution. We implement the DES model in a Bayesian framework and demonstrate through simulations that it can accurately infer all the relevant parameters. We demonstrate the use of our model by analysing the Cenozoic fossil record of land plants and inferring dispersal and extinction rates across Eurasia and North America. Our results show that biogeographic range evolution is not a time-homogeneous process, as assumed in most phylogenetic analyses, but varies through time and between areas. In our empirical assessment, this is shown by the striking predominance of plant dispersals from Eurasia into North America during the Eocene climatic cooling, followed by a shift in the opposite direction, and finally, a balance in biotic interchange since the middle Miocene. We conclude by discussing the potential of fossil-based analyses to test biogeographic hypotheses and improve phylogenetic methods in historical biogeography.

Phylogeny of Celastraceae Subfamilies Cassinoideae and Tripterygioideae Inferred from Morphological Characters and Nuclear and Plastid Loci

Abstract The phylogeny of Celastraceae subfamilies Cassinoideae (120 species in 17 genera in both the Old and New World tropics and subtropics) and Tripterygioideae (39 species in seven genera) was inferred using plastid (matK, trnL-F) and nuclear (ITS and 26S rDNA) loci together with morphological characters. Subfamily Cassinoideae include those Celastraceae genera with drupes, berries, or nuts that have one to five locules and one to two seeds per locule, while Tripterygioideae include those genera with one to two seeded samaras that lack arillate seeds. We infer that both subfamilies are grossly polyphyletic groups, with Cassinoideae consisting of ≥ eight separate lineages and Tripterygioideae consisting of ≥ six separate lineages. Crossopetalum, from tropical America, is part of an early derived lineage sister to a taxonomically diverse Austral-Pacific clade. Myginda is not distinct from Crossopetalum. Gyminda + Orthosphenia + Rzedowskia + Schaefferia are a clade that is only distantly related to Crossopetalum. The monotypic Hartogiopsis is in a clade with other Madagascan genera and sister to the more widely distributed Pleurostylia. Fraunhofera and Plenckia are a clade nested within New World Maytenus; taxonomic changes are required for ≥ one of these genera. Platypterocarpus is part of a primarily African clade and is only distantly related to Tripterygium and Wimmeria.

Comment (1) on “Formation of the Isthmus of Panama” by O’Dea et al.

The conclusions of O’Dea et al. on the formation of the Isthmus of Panama are not supported by analysis of the data. A review and reanalysis of geological, molecular, and paleontological data led O’Dea et al. (1) to propose (i) that reports by Montes et al. (2) and Bacon et al. (3) regarding a middle Miocene closure of the Central American Seaway (CAS) are unsupported, and (ii) a new age of the formation of the Isthmus at 2.8 million years ago (Ma). Here, we reject both of these conclusions.

Toward a Self-Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa

&NA; Rapidly growing biological data—including molecular sequences and fossils—hold an unprecedented potential to reveal how evolutionary processes generate and maintain biodiversity. However, researchers often have to develop their own idiosyncratic workflows to integrate and analyze these data for reconstructing time‐calibrated phylogenies. In addition, divergence times estimated under different methods and assumptions, and based on data of various quality and reliability, should not be combined without proper correction. Here we introduce a modular framework termed SUPERSMART (Self‐Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa), and provide a proof of concept for dealing with the moving targets of evolutionary and biogeographical research. This framework assembles comprehensive data sets of molecular and fossil data for any taxa and infers dated phylogenies using robust species tree methods, also allowing for the inclusion of genomic data produced through next‐generation sequencing techniques. We exemplify the application of our method by presenting phylogenetic and dating analyses for the mammal order Primates and for the plant family Arecaceae (palms). We believe that this framework will provide a valuable tool for a wide range of hypothesis‐driven research questions in systematics, biogeography, and evolution. SUPERSMART will also accelerate the inference of a “Dated Tree of Life” where all node ages are directly comparable.