The Central American land bridge as an engine of diversification in New World doves

Aim The closure of the Central American land‐bridge connection between North and South America 3.5 million years ago was a major biogeographic event that allowed considerable interchange of the previously isolated faunas of these continents. However, the role that this connection may have had in diversification of North and South American faunas is less well understood. The goal of this study was to evaluate the potential role of the formation of this land connection in generating diversity, through repeated rare dispersal events followed by isolation. Location North and South America. Methods We evaluated the role of the Central American land‐bridge connection in avian diversification using a molecular phylogeny based on four gene regions for mid‐sized New World doves. Diversification events were dated using a Bayesian relaxed clock analysis and internal calibration points for endemic island taxa with known island ages. Results The reconstructed phylogenetic tree was well supported and recovered monophyly of the genera Leptotila and Zenaida, but the quail‐doves (Geotrygon) were paraphyletic, falling into three separate lineages. The phylogeny indicated at least nine dispersal‐driven divergence events between North and South America. There were also five dispersal events in the recent past that have not yet led to differentiation of taxa (polymorphic taxa). Main conclusions Most of these dispersal‐driven diversification events occurred at the time of or after the formation of the Central American land bridge, indicating that this land connection played a role in facilitating divergence via dispersal of doves between continents.     

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.     

Phylogeography and biogeography of the lower Central American Neotropics: diversification between two continents and between two seas

Lower Central America (LCA) provides a geologically complex and dynamic, richly biodiverse model for studying the recent assembly and diversification of a Neotropical biota. Here, we review the growing literature of LCA phylogeography studies and their contribution to understanding the origins, assembly, and diversification of the LCA biota against the backdrop of regional geologic and climatic history, and previous biogeographical inquiry. Studies to date reveal that phylogeographical signal within taxa of differing distributions reflects a diversity of patterns and processes rivalling the complexities of LCA landscapes themselves. Even so, phylogeography is providing novel insights into regional diversification (e.g. cryptic lineage divergences), and general evolutionary patterns are emerging. Congruent multi‐taxon phylogeographic breaks are found across the Nicaraguan depression, Chorotega volcanic front, western and central Panama, and the Darién isthmus, indicating that a potentially shared history of responses to regional‐scale (e.g. geological) processes has shaped the genetic diversity of LCA communities. By contrast, other species show unique demographic histories in response to overriding historical events, including no phylogeographic structure at all. These low‐structure or incongruent patterns provide some evidence for a role of local, ecological factors (e.g. long‐distance dispersal and gene flow in plants and bats) in shaping LCA communities. Temporally, comparative phylogeographical structuring reflects Pliocene–Pleistocene dispersal and vicariance events consistent with the timeline of emergence of the LCA isthmus and its major physiographic features, e.g. cordilleras. We emphasise the need to improve biogeographic inferences in LCA through in‐depth comparative phylogeography projects capitalising on the latest statistical phylogeographical methods. While meeting the challenges of reconstructing the biogeographical history of this complex region, phylogeographers should also take up the critical service to society of applying their work to the conservation of its fascinating biodiversity.     

Early and dynamic colonization of Central America drives speciation in Neotropical army ants

The emergence of the Isthmus of Panama is one of the most important events in recent geological history, yet its timing and role in fundamental evolutionary processes remain controversial. While the formation of the isthmus was complete around 3 million years ago (Ma), recent studies have suggested prior intercontinental biotic exchange. In particular, the possibility of early intermittent land bridges facilitating colonization constitutes a potential mechanism for speciation and colonization before full closure of the isthmus. To test this hypothesis, we employed genomic methods to study the biogeography of the army ant genus Eciton, a group of keystone arthropod predators in Neotropical rainforests. Army ant colonies are unable to disperse across water and are therefore ideally suited to study the biogeographic impact of land bridge formation. Using a reduced representation genome sequencing approach, we show that all strictly Central American lineages of Eciton diverged from their respective South American sister lineage between 4 and 7 Ma, significantly prior to the complete closure of the isthmus. Furthermore, three of the lineage pairs form extensive and coincident secondary contact zones in Costa Rica and Nicaragua, with no evidence of gene flow. Such a discrete and repeated biogeographic pattern indicates at least two waves of army ant dispersal into Central America that were separated by significant genetic divergence times. Thus, by integrating phylogenomic, population genomic and geographic evidence, we show that early colonization of Central America across the emerging Isthmus of Panamá drove parallel speciation in Eciton army ants.     

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.     

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.     

Multiple transisthmian divergences,extensive cryptic diversity,occasional long‐distance dispersal,and biogeographic patterns in a marine coastal isopod with an amphi‐American distribution

Excirolana braziliensis is a coastal intertidal isopod with a broad distribution spanning the Atlantic and Pacific tropical and temperate coasts of the American continent. Two separate regional studies (one in Panama and one in Chile) revealed the presence of highly genetically divergent lineages, implying that this taxon constitutes a cryptic species complex. The relationships among the lineages found in these two different regions and in the rest of the distribution, however, remain unknown. To better understand the phylogeographic patterns of E. braziliensis, we conducted phylogenetic analyses of specimens from much of its entire range. We obtained DNA sequences for fragments of four mitochondrial genes (16S rDNA, 12S rDNA, COI, and Cytb) and also used publicly available sequences. We conducted maximum likelihood and Bayesian phylogenetic reconstruction methods. Phylogeographic patterns revealed the following: (1) new highly divergent lineages of E. braziliensis; (2) three instances of Atlantic–Pacific divergences, some of which appear to predate the closure of the Isthmus of Panama; (3) the distributional limit of highly divergent lineages found in Brazil coincides with the boundary between two major marine coastal provinces; (4) evidence of recent long‐distance dispersal in the Caribbean; and (5) populations in the Gulf of California have closer affinities with lineages further south in the Pacific, which contrasts with the closer affinity with the Caribbean reported for other intertidal organisms. The high levels of cryptic diversity detected also bring about challenges for the conservation of this isopod and its fragile environment, the sandy shores. Our findings underscore the importance of comprehensive geographic sampling for phylogeographic and taxonomical studies of broadly distributed putative species harboring extensive cryptic diversity.     

Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record

Marine organisms exhibit a wide range of egg sizes, even among closely related taxa, and egg size is widely considered to be one of the most important components of the life histories of marine species. The nature of the trade-off between egg size and number and the consequences of variation in egg size for offspring growth and survivorship have been extensively modeled. Yet, there is little empirical evidence that supports the relative importance of particular environmental parameters in engendering the tremendous variation in egg size seen in marine organisms. This study compares egg sizes between six geminate species pairs of bivalves in the family Arcidae to determine whether egg size differs in predictable directions between geminate species in the two oceans separated by the Central American isthmus, and whether the direction and timing of egg size evolution among geminates in this family is correlated with both modern and paleoceanographic patterns of oceanic productivity. In all modern members of six geminate pairs, egg size was larger in the species in the western Atlantic than in its sister species the eastern Pacific. This pattern supports the hypothesis that optimal egg size differs in the two oceans due to the low productivity and poor larval feeding environment in the western Atlantic relative to the eastern Pacific. The fossil record of one geminate pair shows that egg size has remained consistently large in the western Atlantic from the Miocene to the Recent, while egg size in the eastern Pacific has decreased to the current small size in less than 2 million years; this suggests that modern-day differences between egg sizes in the western Atlantic and eastern Pacific are due to either an increase in productivity in the eastern Pacific and subsequent selection for smaller eggs in that ocean, or differential patterns of extinction that occurred well after the rise of the isthmus. These results agree with ancestral character state reconstruction using linear parsimony, but differ from squared-change parsimony reconstructions.     

Evaluating the role of contracting and expanding rainforest in initiating cycles of speciation across the Isthmus of Panama

Climatic and geological changes across time are presumed to have shaped the rich biodiversity of tropical regions. However, the impact climatic drying and subsequent tropical rainforest contraction had on speciation has been controversial because of inconsistent palaeoecological and genetic data. Despite the strong interest in examining the role of climatic change on speciation in the Neotropics there has been few comparative studies, particularly, those that include non-rainforest taxa. We used bird species that inhabit humid or dry habitats that dispersed across the Panamanian Isthmus to characterize temporal and spatial patterns of speciation across this barrier. Here, we show that these two assemblages of birds exhibit temporally different speciation time patterns that supports multiple cycles of speciation. Evidence for these cycles is further corroborated by the finding that both assemblages consist of 'young' and 'old' species, despite dry habitat species pairs being geographically more distant than pairs of humid habitat species. The matrix of humid and dry habitats in the tropics not only allows for the maintenance of high species richness, but additionally this study suggests that these environments may have promoted speciation. We conclude that differentially expanding and contracting distributions of dry and humid habitats was probably an important contributor to speciation in the tropics.     

Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra

Echinometra is a pantropical sea urchin made famous through studies of phylogeny, speciation, and genetic structure of the Indo-West Pacific (IWP) species. We sequenced 630 bp of the cytochrome oxidase I (COI) mitochondrial gene to provide comparable information on the eastern Pacific and Atlantic species, using divergence between those separated by closure of the Isthmus of Panama 3.1 million years ago (Ma) to estimate dates for cladogenic events. Most recently (1.27-1. 62 Ma), the Atlantic species E. lucunter and E. viridis diverged from each other, at a time in the Pleistocene that sea levels fell and Caribbean coral speciation and extinction rates were high. An earlier split, assumed to have been coincident with the completion of the Isthmus of Panama, separated the eastern Pacific E. vanbrunti from the Atlantic common ancestor. Transisthmian COI divergence similar to that in the sea urchin genus Eucidaris supports this assumption. The most ancient split in Echinometra occurred between the IWP and the neotropical clades, due to cessation of larval exchange around South Africa or across the Eastern Pacific Barrier. Gene flow within species is generally high; however, there are restrictions to genetic exchange between E. lucunter populations from the Caribbean and those from the rest of the Atlantic. Correlation between cladogenic and vicariant events supports E. Mayr's contention that marine species, despite their high dispersal potential, form by means of geographical separation. That sympatric, nonhybridizing E. lucunter and E. viridis were split so recently suggests, however, that perfection of reproductive barriers between marine species with large populations can occur in less than 1.6 million years (Myr).     

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.     

Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans

To understand how allopatric speciation proceeds, we need information on barriers to gene flow, their antiquity, and their efficacy. For marine organisms with planktonic larvae, much of this information can only be obtained through the determination of divergence between populations. We evaluated the importance of ocean barriers by studying the mitochondrial DNA phylogeography of Tripneustes, a pantropical genus of shallow water sea urchin. A region of cytochrome oxidase I (COI) was sequenced in 187 individuals from locations around the globe. The COI phylogeny agreed with a previously published phylogeny of bindin that barriers important to the evolution of Tripneustes are: (1) the cold water upwelling close to the tip of South Africa, (2) the Isthmus of Panama, (3) the long stretch of deep water separating the eastern from the western Atlantic, and (4) the freshwater plume of the Orinoco and the Amazon rivers between the Caribbean and the coast of Brazil. These barriers have previously been shown to be important in at least a subset of the shallow water marine organisms in which phylogeography has been studied. In contrast, the Eastern Pacific Barrier, 5000 km of deep water between the central and the eastern Pacific that has caused the deepest splits in other genera of sea urchins, is remarkably unimportant as a cause of genetic subdivision in Tripneustes. There is also no discernible subdivision between the Pacific and Indian Ocean populations of this genus. The most common COI haplotype is found in the eastern, central, and western Pacific as well as the Indian Ocean. Morphology, COI, and bindin data agree that T. depressus from the eastern Pacific and T. gratilla from the western Pacific are, in fact, the same species. The distribution of haplotype differences in the Indo-Pacific exhibits characteristics expected from a sea urchin genus with ephemeral local populations, but with high fecundity, dispersal, and growth: there is little phylogenetic structure, and mismatch distributions conform to models of recent population expansion on a nearly global scale. Yet, comparisons between local populations produce large and significant F(ST) values, indicating nonrandom haplotype distribution. This apparent local differentiation is only weakly reflected in regional divergence, and there is no evidence of isolation by distance in correlations between F(ST) values and either geographical or current distance. Thus, Tripneustes in the Indo-Pacific (but not in the Atlantic) seems to be one large metapopulation spanning two oceans and containing chaotic, nonequilibrium local variation, produced by the haphazard arrival of larvae or by unpredictable local extinction.     

Biogeographical,ecological and morphological structure in a phylogenetic analysis of Ateleia (Swartzieae,Fabaceae) derived from combined molecular,morphological and chemical data

A phylogenetic analysis of combined morphological, chemical and ITS/5.8S sequence data reveals that species of Ateleia are often more genetically than morphologically divergent, and that species thought to be most closely related morphologically are distant relatives within the genus. Ateleia shows niche conservatism, with most species confined to seasonally dry tropical forest in Central America and the Caribbean, and fewer species in the same biome in South America. Four independent transitions to wet forests may have occurred in the genus. The estimated ages of Ateleia lineages spanning Central and South America are either older or younger than the estimated age of closure of the Isthmus of Panama. The older dates clearly suggest that over‐water dispersal is responsible for the distribution of Ateleia that includes the Caribbean Islands. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 162 , 39–53.     

Speciation in protists: Spatial and ecological divergence processes cause rapid species diversification in a freshwater chrysophyte

Although eukaryotic microorganisms are extremely numerous, diverse and essential to global ecosystem functioning, they are largely understudied by evolutionary biologists compared to multicellular macroscopic organisms. In particular, very little is known about the speciation mechanisms which may give rise to the diversity of microscopic eukaryotes. It was postulated that the enormous population sizes and ubiquitous distribution of these organisms could lead to a lack of population differentiation and therefore very low speciation rates. However, such assumptions have traditionally been based on morphospecies, which may not accurately reflect the true diversity, missing cryptic taxa. In this study, we aim to articulate the major diversification mechanisms leading to the contemporary molecular diversity by using a colonial freshwater flagellate, Synura sphagnicola, as an example. Phylogenetic analysis of five sequenced loci showed that S. sphagnicola differentiated into two morphologically distinct lineages approximately 15.4 million years ago, which further diverged into several evolutionarily recent haplotypes during the late Pleistocene. The most recent haplotypes are ecologically and biogeographically much more differentiated than the old lineages, presumably because of their persistent differentiation after the allopatric speciation events. Our study shows that in microbial eukaryotes, species diversification via the colonization of new geographical regions or ecological resources occurs much more readily than was previously thought. Consequently, divergence times of microorganisms in some lineages may be equivalent to the estimated times of speciation in plants and animals.     

Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species

Evolutionary biologists have often suggested that ecology is important in speciation, in that natural selection may drive adaptive divergence between lineages that inhabit different environments. I suggest that it is the tendency of lineages to maintain their ancestral ecological niche (phylogenetic niche conservatism) and their failure to adapt to new environments which frequently isolates incipient species and begins the process of speciation. Niche conservatism may be an important and widespread component of allopatric speciation but is largely unstudied. The perspective outlined here suggests roles for key microevolutionary processes (i.e., natural selection, adaptation) that are strikingly different from those proposed in previous literature on ecology and speciation. Yet, this perspective is complementary to the traditional view because it focuses on a different temporal stage of the speciation process.     

Evolutionary history of the reef fish Anisotremus interruptus (Perciformes: Haemulidae) throughout the Tropical Eastern Pacific

The Tropical Eastern Pacific (TEP) is a dynamic coastal environment characterized by a complex system of oceanic processes and discontinuous rocky habitats. These features, in conjunction with the ecological and physiological characteristics of Anisotremus interruptus, might limit gene flow and shape the evolutionary history of the species. In this study, we investigate the evolutionary history of the reef fish A. interruptus (and its Atlantic sister species A. surinamensis) throughout its range in the TEP, using two mitochondrial (cox1 and cytb) and two nuclear markers (S7 and RAG1). We found three genetic groups of A. interruptus with recent divergence times from the Galapagos Archipelago, Revillagigedo Archipelago, the continental TEP, and A. surinamensis the sister specie from the Atlantic. The haplotype mtDNA networks show A. surinamensis in a central position with respect to Pacific genetic haplogroups, whereas nDNA networks show mixed haplotypes between the four genetic groups. In the species tree, A. surinamensis appears as the sister species of all the Pacific samples and the Galapagos Archipelago population emerges as a genetically distinctive group. The samples from the Revillagigedo Archipelago also constitute a genetic distinctive group, closely related to the continental samples. Continental individuals do not show significant genetic structure and exhibit a population expansion during the Pleistocene. The sandy gaps of the TEP not appear to act as barriers isolating populations of A. interruptus, whereas the open sea gap between the oceanic islands and the continental coast do.