The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon

The 'Great American Interchange' (GAI) is recognized as having had a dramatic effect on biodiversity throughout the Neotropics. However, investigation of patterns in Neotropical avian biodiversity has generally been focused on South American taxa in the Amazon Basin, leaving the contribution of Central American taxa under-studied. More rigorous studies of lineages distributed across the entire Neotropics are needed to uncover phylogeographical patterns throughout the area, offering insights into mechanisms that contribute to overall Neotropical biodiversity. Here we use mitochondrial DNA sequence data and intensive geographical sampling from the widespread Neotropical avian genus Trogon to investigate the role of the GAI in shaping its phylogeographical history. Our results show that genetic diversity in Trogon exceeds the perceived biodiversity, and that the GAI resulted in lineage diversification within the genus. Despite greater diversity in South America, a Central American centre of origin with multiple and independent dispersals into South America is indicated. These dispersals were followed by the evolution of divergent lineages associated with the Andes Mountains and other South American geographical features. According to our phylogenetic reconstructions, several species, which were originally defined by morphological characters, are nonmonophyletic. In sum, our results elucidate the evolutionary history of Trogon , reveal patterns obscured by extant biodiversity, and serve as a biogeographical model to consider in future studies.     

The extraordinary journey of Peperomia subgenus Tildenia (Piperaceae): insights into diversification and colonization patterns from its cradle in Peru to the Trans‐Mexican Volcanic Belt

Aim Peperomia subgenus Tildenia consists of c. 60 species growing in seasonal habitats of Neotropical mountain areas from Mexico to Argentina. The subgenus can be split geographically, with almost equal diversity in the Northern Hemisphere (centred in Mexico and Guatemala) and in the Southern Hemisphere (centred in Peru and Bolivia). Only a few species are known from a limited number of localities between these two hotspots. As such, Tildenia is an ideal candidate with which to test time, direction and mode of migration of high mountain taxa against the background of the ‘Great American Biotic Interchange’. Location The Andes with focus on the Central Andes, and the Mexican mountain chains, especially the Trans‐Mexican Volcanic Belt. Methods To elucidate the spatio‐temporal origin, subsequent colonization and radiation of Tildenia, we combine Bayesian phylogenetics based on the chloroplast trnK–matK–psbA region, georeferenced distribution data, and fossil calibrated molecular dating approaches using both penalized likelihood and relaxed phylogenetics. Reconstruction of the ancestral distribution area was performed using dispersal–vicariance analysis and dispersal–extinction–cladogenesis. Results Peperomia subgenus Tildenia is subdivided into six Andean clades and one Mexican and Central American clade originating from a north/central Peruvian ancestor. Molecular dating approaches converge on a stem age of c. 38 Ma for Tildenia and a mostly Miocene diversification and colonization. Main conclusions We detect a strong correlation between diversification of Tildenia and orogenetic events in the respective distribution centres. In the Andes, distribution was influenced by the Altiplano–Eastern Cordillera System as well as the Amotape‐Huancabamba Zone, where the latter serves as both migration barrier and migration bridge for different clades. In contrast to most studies of high‐elevation taxa, we provide support for a south–north colonization towards Central America and Mexico, and provide additional, independent evidence for the latest view on the timing of the Great American Biotic Interchange. In Mexico, the Trans‐Mexican Volcanic Belt has played a major role in more recent radiations together with climatic oscillation and the formation of refugia.     

Environmental change drove macroevolution in cupuladriid bryozoans

Most macroevolutionary events are correlated with changes in the environment, but more rigorous evidence of cause and effect has been elusive. We compiled a 10 Myr record of origination and extinction, changes in mode of reproduction, morphologies and abundances of cupuladriid bryozoan species, spanning the time when primary productivity collapsed in the southwestern Caribbean as the Isthmus of Panama closed. The dominant mode of reproduction shifted dramatically from clonal to aclonal, due in part to a pulse of origination followed by extinction that was strongly selective in favour of aclonal species. Modern-day studies predict reduced clonality in increasingly oligotrophic conditions, thereby providing a mechanistic explanation supporting the hypothesis that the collapse in primary productivity was the cause of turnover. However, whereas originations were synchronous with changing environments, extinctions lagged 1–2 Myr. Extinct species failed to become more robust and reduce their rate of cloning when the new environmental conditions arose, and subsequently saw progressive reductions in abundance towards their delayed demise. Environmental change is therefore established as the root cause of macroevolutionary turnover despite the lag between origination and extinction.     

Robust Estimates of Divergence Times and Selection with a Poisson Random Field Model: A Case Study of Comparative Phylogeographic Data

Mutation frequencies can be modeled as a Poisson random field (PRF) to estimate speciation times and the degree of selection on newly arisen mutations. This approach provides a quantitative theory for comparing intraspecific polymorphism with interspecific divergence in the presence of selection and can be used to estimate population genetic parameters. Although the original PRF model has been extended to more general biological settings to make statistical inference about selection and divergence among model organisms, it has not been incorporated into phylogeographic studies that focus on estimating population genetic parameters for nonmodel organisms. Here, we modified a recently developed time-dependent PRF model to independently estimate genetic parameters from a nuclear and mitochondrial DNA data set of 22 sister pairs of birds that have diverged across a biogeographic barrier. We found that species that inhabit humid habitats had more recent divergence times and larger effective population sizes than those that inhabit drier habitats, and divergence time estimated from the PRF model were similar to estimates from a coalescent species-tree approach. Selection coefficients were higher in sister pairs that inhabited drier habitats than in those in humid habitats, but overall the mitochondrial DNA was under weak selection. Our study indicates that PRF models are useful for estimating various population genetic parameters and serve as a framework for incorporating estimates of selection into comparative phylogeographic studies.     

Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution

Among shallow water sea urchin genera, Arbacia is the only genus that contains species found in both high and low latitudes. In order to determine the geographical origin of the genus and its history of speciation events, we constructed phylogenies based on cytochrome oxidase I and sperm bindin from all its species. Both the mitochondrial and the nuclear gene genealogies show that Arbacia originated in the temperate zone of the Southern Hemisphere and gave rise to three species in the eastern Pacific, which were then isolated from the Atlantic by the Isthmus of Panama. The mid-Atlantic barrier separated two additional species. The bindin data suggest that selection against hybridization is not important in the evolution of this molecule in this genus. Metz et al. in a previous publication found no evidence of selection on bindin of Arbacia and suggested that this might be due to allopatry between species, which obviated the need for species recognition. This suggestion formed the basis of the conclusion, widely spread in the literature, that the source of selection on sea urchin bindin (where it does occur) was reinforcement. However, the range of Arbacia spatuligera overlaps with that of two other species of Arbacia, and our data show that it is hybridizing with one of them. We found that even in the species that overlap geographically, there are no deviations from selective neutrality in the evolution of bindin.     

Out of sight, out of mind: high cryptic diversity obscures the identities and histories of geminate species in the marine bivalve subgenus Acar

Aim The rise of the Isthmus of Panama and the formation of ‘geminate’ species pairs serves as an important model of allopatric speciation. However, to function as a model system, hypothesized geminates must first be shown to be each other’s closest living relatives. If the presence of cryptic taxa obscures true relationships, the biogeographical histories of transisthmian taxa are likely to be misinterpreted. We have therefore completed a phylogeographic survey of the transisthmian bivalve subgenus Acar in the genus Barbatia to characterize patterns of tropical American diversity and to place transisthmian taxa in a regional phylogeographic context. Location Tropical America. Methods Mitochondrial cytochrome c oxidase I (COI) and nuclear internal transcribed spacer (ITS) sequences were obtained from 233 specimens of Acar. Sequences were analysed using cladistic and Bayesian methods. Divergence times between species were inferred from net nucleotide divergences and a coalescence‐based method. Results The survey revealed 22 COI clades that were also monophyletic at ITS, indicating that the taxonomy of Acar is potentially greater than a fivefold diversity underestimate. The lone previously recognized geminate [Barbatia (Acar) gradata and Barbatia (Acar) domingensis] is composed of 15 clades. Among the four transisthmian lineages identified, two diverged more than 14 Ma; the two other geminates split just prior to the time of final seaway closure. In addition to a fourfold increase in the number of known geminates, our data show that within‐basin diversification has been more impressive, with one geminate splitting into five monophyletic clades in the Western Atlantic alone since seaway closure. Electron microscopy of the larval shells of specimens indicates that the transisthmian lineage with the greatest rate of post‐Isthmian diversification possesses non‐planktonic larvae, a life‐history feature linked to high speciation rates. Main conclusions Our analyses revealed that the identities of geminate pairs split by the Isthmus of Panama were obscured by extremely high tropical American cryptic diversity. Although we have identified four geminates, only two appear to have been split by the Isthmus. Our uncovering of extensive post‐Isthmian diversification is consistent with the palaeontological perspective that the final closure of the Central American Seaway was followed by high rates of subgeneric diversification, particularly in the tropical Western Atlantic.