Biogeography of Greater Antillean freshwater fishes, with a review of competing hypotheses.

In biogeography, vicariance and long-distance dispersal are often characterised as competing scenarios. However, they are related concepts, both relying on collective geological, ecological, and phylogenetic evidence. This is illustrated by freshwater fishes, which may immigrate to islands either when freshwater connections are temporarily present and later severed (vicariance), or by unusual means when ocean gaps are crossed (long-distance dispersal). Marine barriers have a strong filtering effect on freshwater fishes, limiting immigrants to those most capable of oceanic dispersal. The roles of vicariance and dispersal are debated for freshwater fishes of the Greater Antilles. We review three active hypotheses [Cretaceous vicariance, Greater Antilles-Aves Ridge (GAARlandia), long-distance dispersal] and propose long-distance dispersal to be an appropriate model due to limited support for freshwater fish use of landspans. Greater Antillean freshwater fishes have six potential source bioregions (defined from faunal similarity): Northern Gulf of México, Western Gulf of México, Maya Terrane, Chortís Block, Eastern Panamá, and Northern South America. Faunas of the Greater Antilles are composed of taxa immigrating from many of these bioregions, but there is strong compositional disharmony between island and mainland fish faunas (>90% of Antillean species are cyprinodontiforms, compared to <10% in Northern Gulf of México and Northern South America, and ≤50% elsewhere), consistent with a hypothesis of long-distance dispersal. Ancestral-area reconstruction analysis indicates there were 16 or 17 immigration events over the last 51 million years, 14 or 15 of these by cyprinodontiforms. Published divergence estimates and evidence available for each immigration event suggests they occurred at different times and by different pathways, possibly with rafts of vegetation discharged from rivers or washed to sea during storms. If so, ocean currents likely provide critical pathways for immigration when flowing from one landmass to another. On the other hand, currents create dispersal barriers when flowing perpendicularly between landmasses. In addition to high salinity tolerance, cyprinodontiforms collectively display a variety of adaptations that could enhance their ability to live with rafts (small body size, viviparity, low metabolism, amphibiousness, diapause, self-fertilisation). These adaptations likely also helped immigrants establish island populations after arrival and to persist long term thereafter. Cichlids may have used a pseudo bridge (Nicaragua Rise) to reach the Greater Antilles. Gars (Lepisosteidae) may have crossed the Straits of Florida to Cuba, a relatively short crossing that is not a barrier to gene flow for several cyprinodontiform immigrants. Indeed, widespread distributions of Quaternary migrants (Cyprinodon, Gambusia, Kryptolebias), within the Greater Antilles and among neighbouring bioregions, imply that long-distance dispersal is not necessarily inhibitory for well-adapted species, even though it appears to be virtually impossible for all other freshwater fishes.

Macroevolutionary trends of the Neotropical genus Ameroglossum (Linderniaceae) in rocky outcrop environments.

Ameroglossum is a rare plant genus endemic to northeastern of Brazil, initially monospecific (A. pernambucense) and recently expanded by the description of eight new species and two related genera. The genus was initially placed in the family Scrophulariaceae, but this has never been phylogenetically tested. This group is ecologically restricted to rocky inselberg habitats that function as island-like systems (ILS) with spatial fragmentation, limited area, environmental heterogeneity, temporal isolation and low connectivity. Here we use a phylogenetic perspective to test the hypothesis that Ameroglossum diversification was related to island-like radiation in inselbergs. Our results support that Ameroglossum is monophyletic only with the inclusion of Catimbaua and Isabelcristinia (named here as Ameroglossum sensu lato) and this group was well-supported in the family Linderniaceae. Biogeographic analyses suggest that the ancestral of Ameroglossum and related genus arrived in South America c.a. 15 million years ago by long-distance dispersal, given the ancestral distribution of Linderniaceae in Africa. In rocky outcrop habitats, Ameroglossum s.l. developed floral morphological specialization associated with pollinating hummingbirds, compatible with an island-like model. However, no increase in speciation rate was detected, which may be related to high extinction rates and/or slow diversification rate in this ecologically restrictive environment. Altogether, in Ameroglossum key innovations involving flowers seem to have offered opportunities for evolution of greater phenotypic diversity and occupation of new niches in rocky outcrop environments.

The phylogeny of Syntrichia: An ecologically diverse clade of mosses with an origin in South America.

PREMISE: To address the biodiversity crisis, we need to understand the evolution of all organisms and how they fill geographic and ecological space. Syntrichia is one of the most diverse and dominant genera of mosses, ranging from alpine habitats to desert biocrusts, yet its evolutionary history remains unclear. METHODS: We present a comprehensive phylogenetic analysis of Syntrichia, based on both molecular and morphological data, with most of the named species and closest outgroups represented. In addition, we provide ancestral-state reconstructions of water-related traits and a global biogeographic analysis. RESULTS: We found 10 major well-resolved subclades of Syntrichia that possess geographical or morphological coherence, in some cases representing previously accepted genera. We infer that the extant species diversity of Syntrichia likely originated in South America in the early Eocene (56.5-43.8 million years ago [Mya]), subsequently expanded its distribution to the neotropics, and finally dispersed to the northern hemisphere. There, the clade experienced a recent diversification (15-12 Mya) into a broad set of ecological niches (e.g., the S. caninervis and S. ruralis complexes). The transition from terricolous to either saxicolous or epiphytic habitats occurred more than once and was associated with changes in water-related traits. CONCLUSIONS: Our study provides a framework for understanding the evolutionary history of Syntrichia through the combination of morphological and molecular characters, revealing that migration events that shaped the current distribution of the clade have implications for morphological character evolution in relation to niche diversity.

Molecular Phylogeny, Character Evolution, and Biogeography of Hydrangea Section Cornidia, Hydrangeaceae.

Background: Hydrangea section Cornidia consists of 26 currently accepted species and a yet undefined number of new species and erroneously synonymized taxa. This clade consists of (sub)tropical lianas occurring from northern Mexico to southern Chile and Argentina, and one species from Southeast Asia. Currently, no molecular phylogenetic hypothesis is available that includes more than a few species of this section. Hence, a resolved and well-sampled molecular phylogenetic hypothesis may help to enforce taxonomic decisions. In this study, we present a phylogenetic framework based on sequences from two low copy nuclear genes from a comprehensive taxon sampling of H. section Cornidia and a selection of outgroups. Our phylogenetic reconstructions prove the non-monophyly of the traditionally recognized subsections Monosegia and Polysegia and their corresponding series, Speciosae and Aphananthae, and Synstyleae and Chorystyleae, respectively. Three morphologically defined species were recovered with high support as monophyletic, namely, Hydrangea panamensis, Hydrangea serratifolia, and Hydrangea tarapotensis. However, statistical support for some shallow nodes did not allow to refute, with high support, the monophyly of several of the herein recognized species for which more than one individual could be analyzed. Based on the obtained phylogenetic framework, we reconstructed the evolution of selected reproductive characters. Hydrangea section Cornidia is the only genus section for which dioecism has been extensively documented. Our character reconstruction of sexual dimorphism shows that dioecism is the ancestral state in this section and that this was reversed to monoecy in Hydrangea seemannii and Hydrangea integrifolia. Character reconstruction for the enlarged marginal flowers recovered their presence as the ancestral character state in H. section Cornidia, although at least three internal lineages independently lost them; thus, losses were reconstructed to be more likely than gain. With respect to the flower color, more species exhibit white than red flowers, and white is reconstructed as the ancestral state. Cornidia also shows an unusual disjunct geographic distribution between Asia and Central Mesoamerica-South America, as it is not present in the USA and Canada. The origin of Cornidia is reconstructed to be the New World with higher probability, and the presence of one species in Asia is likely due to long-distance dispersal.

Molecular signatures of long-distance oceanic dispersal and the colonization of Pacific islands in Lycium carolinianum.

PREMISE: Long-distance dispersal has been important in explaining the present distributions of many plant species. Despite being infrequent, such dispersal events have considerable evolutionary consequences, because bottlenecks during colonization can result in reduced genetic diversity. We examined the phylogeographic history of Lycium carolinianum, a widespread taxon that ranges from southeastern North America to several Pacific islands, with intraspecific diversity in sexual and mating systems. METHODS: We used Bayesian, likelihood, and coalescent approaches with nuclear and plastid sequence data and genome-wide single nucleotide polymorphisms to reconstruct the dispersal history of this species. We also compared patterns of genetic variation in mainland and island populations using single nucleotide polymorphisms and allelic diversity at the S-RNase mating system gene. RESULTS: Lycium carolinianum is monophyletic and dispersed once from the North American mainland, colonizing the Pacific islands ca. 40,100 years ago. This dispersal was accompanied by a loss of genetic diversity in SNPs and the S-RNase locus due to a colonization bottleneck and the loss of self-incompatibility. Additionally, we documented at least two independent transitions to gynodioecy: once following the colonization of the Hawaiian Islands and loss of self-incompatibility, and a second time associated with polyploidy in the Yucatán region of Mexico. CONCLUSIONS: Long-distance dispersal via fleshy, bird dispersed fruits best explains the unusually widespread distribution of L. carolinianum. The collapse of diversity at the S-RNase locus in island populations suggests that self-fertilization may have facilitated the subsequent colonization of Pacific islands following a single dispersal from mainland North America.

The "evil tribe" spreads across the land: A dated molecular phylogeny provides insight into dispersal, expansion, and biogeographic relationships within one of the largest tribes of the sunflower family (Vernonieae: Compositae).

PREMISE: With over 1500 species, the globally distributed Vernonieae is one of the most successful members of the largest family of flowering plants, the Compositae. However, due to its morphological complexity and limited geographic representation in previous studies, subtribal and biogeographic relationships are unclear. Here, new DNA sequence data spanning the geographic range of the tribe provides a taxonomically robust time-calibrated phylogeny, estimates migration pathways and timing of important biogeographic events, and allows inference of environmental factors that have contributed to the success of the Vernonieae worldwide. METHODS: Phylogenetic relationships were estimated for 368 taxa representing all Vernonieae subtribes. Molecular clock and ancestral range estimation analyses provide a framework for inference of the biogeographic history of the tribe. RESULTS: Relationships among the subtribes were established and correct placement determined for problematic taxa, along with the first model-based assessment of the biogeographic history of the tribe. The Vernonieae were estimated to have evolved ~50 mya. Africa was the first center of diversity, from which a single dispersal event established the monophyletic New World lineage. Long-distance dispersal from Africa and Brazil established the tribe on five continents and Oceania. CONCLUSIONS: The New World lineage is monophyletic, but Old World taxa are not. New subtribal taxonomies are needed. Moquinieae are nested in Vernonieae. Long-distance dispersal from Africa beginning 45 mya was key to establishing the tribe's near-global distribution. Migration corridors created by volcanic mountain chains and iron-rich soils in Africa and the Americas promoted radiation and range expansion.

Contrasting biogeographical patterns in Margarella (Gastropoda: Calliostomatidae: Margarellinae) across the Antarctic Polar Front.

Members of the trochoidean genus Margarella (Calliostomatidae) are broadly distributed across Antarctic and sub-Antarctic ecosystems. Here we used novel mitochondrial and nuclear gene sequences to clarify species boundaries and phylogenetic relationships among seven nominal species distributed on either side of the Antarctic Polar Front (APF). Molecular reconstructions and species-delimitation analyses recognized only four species: M. antarctica (the Antarctic Peninsula), M. achilles (endemic to South Georgia), M. steineni (South Georgia and Crozet Island) and the morphologically variable M. violacea (=M. expansa, M. porcellana and M. pruinosa), with populations in southern South America, the Falkland/Malvinas, Crozet and Kerguelen Islands. Margarella violacea and M. achilles are sister species, closely related to M. steineni, with M. antarctica sister to all these. This taxonomy reflects contrasting biogeographic patterns on either side of the APF in the Southern Ocean. Populations of Margarella north of the APF (M. violacea) showed significant genetic variation but with many shared haplotypes between geographically distant populations. By contrast, populations south of the APF (M. antarctica, M. steineni and M. achilles) exhibited fewer haplotypes and comprised three distinct species, each occurring across a separate geographical range. We hypothesize that the biogeographical differences may be the consequence of the presence north of the APF of buoyant kelps - potential long-distance dispersal vectors for these vetigastropods with benthic-protected development - and their near-absence to the south. Finally, we suggest that the low levels of genetic diversity within higher-latitude Margarella reflect the impact of Quaternary glacial cycles that exterminated local populations during their maxima.

Historical biogeography of Vochysiaceae reveals an unexpected perspective of plant evolution in the Neotropics.

PREMISE: Despite the fast pace of exploration of the patterns and processes influencing Neotropical plant hyperdiversity, the taxa explored are mostly from large groups that are widely distributed, morphologically diverse, or economically important. Vochysiaceae is an example of an undersampled taxon, providing an excellent system for investigating Neotropical biogeography. We present a phylogenomics-based hypothesis of species relationships in Vochysiaceae to investigate its evolutionary history through space and time. METHODS: We inferred a phylogeny for 122 species from Vochysiaceae and seven other families of Myrtales. Fossils from four myrtalean families were used to estimate the divergence times within Vochysiaceae. Historical biogeography was estimated using ancestral range probabilities and stochastic mapping. RESULTS: Monophyly of all genera was supported except for Qualea, which was split by Ruizterania into two clades. Vochysiaceae originated ~100 mya, splitting into an Afrotropical and a Neotropical lineage ~50 mya, and its ancestral range is in the area currently occupied by the Cerrado. CONCLUSIONS: The most recent common ancestor of Vochysiaceae + Myrtaceae had a West Gondwanan distribution, supporting a South American + African ancestral range of Vochysiaceae. On a global scale, geographic range reduction was the principal biogeographic event. At a finer scale, initial range reduction was also important and the Cerrado region was the most ancestral area with multiple colonization events to the Amazon, Central America, and the Atlantic Forest. Colonization events occurred from open areas to forest vegetation, an unusual finding regarding the evolution of plants in the Neotropics.

Open ocean nocturnal insect migration in the Brazilian South Atlantic with comments on flight endurance.

We observed a nocturnal insect swarm aboard the oceanographic ship Cruzeiro do Sul of the Brazilian Navy, while conducting a survey of the Montague guyot (seamount), 389 km distant from the nearest land in the South Atlantic. The insects came from open sea toward the ship from all directions, attracted by the powerful light of the deck. Most insects collided with the hull and fell into the ocean, but we managed to capture and determine 17 (13 Hemiptera of a single species, three Lepidoptera of three species and one Odonata). With one exception, we are certain that none of the specimens caught originated from the ship. The geographic origin, most likely the coast of Brazil, and flight endurance of these insects were inferred using data on wind speed and direction, provided by the crew of the ship, and were reconstructed using Hysplit modeling of air current trajectories.

Vicariance and dispersal in southern hemisphere freshwater fish clades: a palaeontological perspective.

Widespread fish clades that occur mainly or exclusively in fresh water represent a key target of biogeographical investigation due to limited potential for crossing marine barriers. Timescales for the origin and diversification of these groups are crucial tests of vicariant scenarios in which continental break-ups shaped modern geographic distributions. Evolutionary chronologies are commonly estimated through node-based palaeontological calibration of molecular phylogenies, but this approach ignores most of the temporal information encoded in the known fossil record of a given taxon. Here, we review the fossil record of freshwater fish clades with a distribution encompassing disjunct landmasses in the southern hemisphere. Palaeontologically derived temporal and geographic data were used to infer the plausible biogeographic processes that shaped the distribution of these clades. For seven extant clades with a relatively well-known fossil record, we used the stratigraphic distribution of their fossils to estimate confidence intervals on their times of origin. To do this, we employed a Bayesian framework that considers non-uniform preservation potential of freshwater fish fossils through time, as well as uncertainty in the absolute age of fossil horizons. We provide the following estimates for the origin times of these clades: Lepidosireniformes [125-95 million years ago (Ma)]; total-group Osteoglossomorpha (207-167 Ma); Characiformes (120-95 Ma; a younger estimate of 97-75 Ma when controversial Cenomanian fossils are excluded); Galaxiidae (235-21 Ma); Cyprinodontiformes (80-67 Ma); Channidae (79-43 Ma); Percichthyidae (127-69 Ma). These dates are mostly congruent with published molecular timetree estimates, despite the use of semi-independent data. Our reassessment of the biogeographic history of southern hemisphere freshwater fishes shows that long-distance dispersals and regional extinctions can confound and erode pre-existing vicariance-driven patterns. It is probable that disjunct distributions in many extant groups result from complex biogeographic processes that took place during the Late Cretaceous and Cenozoic. Although long-distance dispersals likely shaped the distributions of several freshwater fish clades, their exact mechanisms and their impact on broader macroevolutionary and ecological dynamics are still unclear and require further investigation.

Estimating seed and pollen dispersal kernels from genetic data demonstrates a high pollen dispersal capacity for an endangered palm species.

PREMISE OF THE STUDY: Seed and pollen dispersal are key processes shaping plant population dynamics and maintaining genetic diversity. The essence of these processes is the movement of propagules from a parental tree to the site of propagule establishment. The estimation of plant dispersal kernels has remained challenging due to the difficulty of making direct observations. We estimated the dispersal capacity of the endangered palm Euterpe edulis, whose seeds are dispersed by vertebrates and pollen by insects. METHODS: We used a hierarchical Bayesian model with genetic data from reproductive plants, juveniles, and embryos to estimate dispersal kernels. Our analyses account for genotyping error and uncertainty in parental assignment. KEY RESULTS: We found that seeds were dispersed at most a few hundred meters, but pollen was dispersed up to several kilometers. We hypothesize that this long-distance pollen dispersal is generated mainly by euglossine bees, whereas the main dispersal vectors for short-distance seed dispersal are thrushes. The long-distance dispersal of pollen suggests a high level of gene flow that should maintain genetic diversity of E. edulis. Despite the relation between long-distance dispersal and genetic diversity, we observed low genetic diversity and inbreeding within the local population, which are probably due to restricted gene flow due to the low density of this population and its aggregated spatial distribution. CONCLUSIONS: We conclude that if conservation actions are able to restore the population density of E. edulis, the recovery of its genetic diversity will be facilitated because of its high dispersal capacity, especially with regard to pollen.

Spatial and Temporal Scales of Range Expansion in Wild Phaseolus vulgaris.

The wild progenitor of common-bean has an exceptionally large distribution from northern Mexico to northwestern Argentina, unusual among crop wild progenitors. This research sought to document major events of range expansion that led to this distribution and associated environmental changes. Through the use of genotyping-by-sequencing (∼20,000 SNPs) and geographic information systems applied to a sample of 246 accessions of wild Phaseolus vulgaris, including 157 genotypes of the Mesoamerican, 77 of the southern Andean, and 12 of the Northern Peru-Ecuador gene pools, we identified five geographically distinct subpopulations. Three of these subpopulations belong to the Mesoamerican gene pool (Northern and Central Mexico, Oaxaca, and Southern Mexico, Central America and northern South America) and one each to the Northern Peru-Ecuador (PhI) and the southern Andean gene pools. The five subpopulations were distributed in different floristic provinces of the Neotropical seasonally dry forest and showed distinct distributions for temperature and rainfall resulting in decreased local potential evapotranspiration (PhI and southern Andes groups) compared with the two Mexican groups. Three of these subpopulations represent long-distance dispersal events from Mesoamerica into Northern Peru-Ecuador, southern Andes, and Central America and Colombia, in chronological order. Of particular note is that the dispersal to Northern Peru-Ecuador markedly predates the dispersal to the southern Andes (∼400 vs. ∼100 ky), consistent with the ancestral nature of the phaseolin seed protein and chloroplast sequences observed in the PhI group. Seed dispersal in common bean can be, therefore, described at different spatial and temporal scales, from localized, annual seed shattering to long-distance, evolutionarily rare migration.

Parallel Pleistocene amphitropical disjunctions of a parasitic plant and its host.

PREMISE OF THE STUDY: Aphyllon is a clade of holoparasites that includes closely related North American and South American species parasitic on Grindelia. Both Aphyllon (Orobanchaceae) and Grindelia (Asteraceae) have amphitropical disjunctions between North America and South America; however, the timing of these patterns and the processes to explain them are unknown. METHODS: Chronograms for the Orobanchaceae and Grindelia and their relatives were constructed using fossil and secondary calibration points, one of which was based on the inferred timing of horizontal gene transfer from a papilionoid legume into the common ancestor of Orobanche and Phelipanche. Elevated rates of molecular evolution in the Orobanchaceae have hindered efforts to determine reliable divergence time estimates in the absence of a fossil record. However, using a horizontal gene transfer event as a secondary calibration overcomes this limitation. These chronograms were used to reconstruct the biogeography of Aphyllon, Grindelia, and relatives using a DEC+J model implemented in RevBayes. KEY RESULTS: Aphyllon had two amphitropical dispersals from North America to South America, while Grindelia had a single dispersal. The dispersal of the Aphyllon lineage that is parasitic on Grindelia (0.40 Ma) took place somewhat after Grindelia began to diversify in South America (0.93 Ma). Using a secondary calibration based on horizontal gene transfer, we infer more recent divergence dates of holoparasitic Orobancheae than previous studies. CONCLUSIONS: Parallel host-parasite amphitropical disjunctions in Grindelia and Aphyllon illustrate one means by which ecological specialization may result in nonindependent patterns of diversity in distantly related lineages. Although Grindelia and Aphyllon both dispersed to South America recently, Grindelia appears to have diversified more extensively following colonization. More broadly, recent Pleistocene glaciations probably have also contributed to patterns of diversity and biogeography of temperate northern hemisphere Orobancheae. We also demonstrate the utility of using horizontal gene transfer events from well-dated clades to calibrate parasite phylogenies in the absence of a fossil record.

Species delimitation and biogeography of a southern hemisphere liverwort clade, Frullania subgenus Microfrullania (Frullaniaceae, Marchantiophyta).

Frullania subgenus Microfrullania is a clade of ca. 15 liverwort species occurring in Australasia, Malesia, and southern South America. We used combined nuclear and chloroplast sequence data from 265 ingroup accessions to test species circumscriptions and estimate the biogeographic history of the subgenus. With dense infra-specific sampling, we document an important role of long-distance dispersal in establishing phylogeographic patterns of extant species. At deeper time scales, a combination of phylogenetic analyses, divergence time estimation and ancestral range estimation were used to reject vicariance and to document the role of long-distance dispersal in explaining the evolution and biogeography of the clade across the southern Hemisphere. A backbone phylogeny for the subgenus is proposed, providing insight into evolution of morphological patterns and establishing the basis for an improved sectional classification of species within Microfrullania. Several species complexes are identified, the presence of two undescribed but genetically and morphologically distinct species is noted, and previously neglected names are discussed.

Corrigendum to: The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico.

[This corrects the article on p. 433 in vol. 5, PMID: 25566320.].

The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico.

Biogeography and community ecology can mutually illuminate the formation of a regional species pool or biome. Here, we apply phylogenetic methods to a large and diverse plant clade, Malpighiaceae, to characterize the formation of its species pool in Mexico, and its occupancy of the seasonally dry tropical forest (SDTF) biome that occurs there. We find that the ~162 species of Mexican Malpighiaceae represent ~33 dispersals from South America beginning in the Eocene and continuing until the Pliocene (~46.4-3.8 Myr). Furthermore, dispersal rates between South America and Mexico show a significant six-fold increase during the mid-Miocene (~23.9 Myr). We hypothesize that this increase marked the availability of Central America as an important corridor for Neotropical plant migration. We additionally demonstrate that this high rate of dispersal contributed substantially more to the phylogenetic diversity of Malpighiaceae in Mexico than in situ diversification. Finally, we show that most lineages arrived in Mexico pre-adapted with regard to one key SDTF trait, total annual precipitation. In contrast, these lineages adapted to a second key trait, precipitation seasonality, in situ as mountain building in the region gave rise to the abiotic parameters of extant SDTF. The timing of this in situ adaptation to seasonal precipitation suggests that SDTF likely originated its modern characteristics by the late Oligocene, but was geographically more restricted until its expansion in the mid-Miocene. These results highlight the complex interplay of dispersal, adaptation, and in situ diversification in the formation of tropical biomes. Our results additionally demonstrate that these processes are not static, and their relevance can change markedly over evolutionary time. This has important implications for understanding the origin of SDTF in Mexico, but also for understanding the temporal and spatial origin of biomes and regional species pools more broadly.