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1.  The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals 
Background
Scleractinian corals are currently a focus of major interest because of their ecological importance and the uncertain fate of coral reefs in the face of increasing anthropogenic pressure. Despite this, remarkably little is known about the evolutionary origins of corals. The Scleractinia suddenly appear in the fossil record about 240 Ma, but the range of morphological variation seen in these Middle Triassic fossils is comparable to that of modern scleractinians, implying much earlier origins that have so far remained elusive. A significant weakness in reconstruction(s) of early coral evolution is that deep-sea corals have been poorly represented in molecular phylogenetic analyses.
Results
By adding new data from a large and representative range of deep-water species to existing molecular datasets and applying a relaxed molecular clock, we show that two exclusively deep-sea families, the Gardineriidae and Micrabaciidae, diverged prior to the Complexa/Robusta coral split around 425 Ma, thereby pushing the evolutionary origin of scleractinian corals deep into the Paleozoic.
Conclusions
The early divergence and distinctive morphologies of the extant gardineriid and micrabaciid corals suggest a link with Ordovician "scleractiniamorph" fossils that were previously assumed to represent extinct anthozoan skeletonized lineages. Therefore, scleractinian corals most likely evolved from Paleozoic soft-bodied ancestors. Modern shallow-water Scleractinia, which are dependent on symbionts, appear to have had several independent origins from solitary, non-symbiotic precursors. The Scleractinia have survived periods of massive climate change in the past, suggesting that as a lineage they may be less vulnerable to future changes than often assumed.
doi:10.1186/1471-2148-11-316
PMCID: PMC3224782  PMID: 22034946
2.  Evolutionary History of Lagomorphs in Response to Global Environmental Change 
PLoS ONE  2013;8(4):e59668.
Although species within Lagomorpha are derived from a common ancestor, the distribution range and body size of its two extant groups, ochotonids and leporids, are quite differentiated. It is unclear what has driven their disparate evolutionary history. In this study, we compile and update all fossil records of Lagomorpha for the first time, to trace the evolutionary processes and infer their evolutionary history using mitochondrial genes, body length and distribution of extant species. We also compare the forage selection of extant species, which offers an insight into their future prospects. The earliest lagomorphs originated in Asia and later diversified in different continents. Within ochotonids, more than 20 genera occupied the period from the early Miocene to middle Miocene, whereas most of them became extinct during the transition from the Miocene to Pliocene. The peak diversity of the leporids occurred during the Miocene to Pliocene transition, while their diversity dramatically decreased in the late Quaternary. Mantel tests identified a positive correlation between body length and phylogenetic distance of lagomorphs. The body length of extant ochotonids shows a normal distribution, while the body length of extant leporids displays a non-normal pattern. We also find that the forage selection of extant pikas features a strong preference for C3 plants, while for the diet of leporids, more than 16% of plant species are identified as C4 (31% species are from Poaceae). The ability of several leporid species to consume C4 plants is likely to result in their size increase and range expansion, most notably in Lepus. Expansion of C4 plants in the late Miocene, the so-called ‘nature’s green revolution’, induced by global environmental change, is suggested to be one of the major ‘ecological opportunities’, which probably drove large-scale extinction and range contraction of ochotonids, but inversely promoted diversification and range expansion of leporids.
doi:10.1371/journal.pone.0059668
PMCID: PMC3616043  PMID: 23573205
3.  Leaves and fruits of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the Oligocene Ningming Formation of Guangxi, South China and their biogeographic implications 
Background
The pantropical genus Bauhinia, along with the northern temperate Cercis and several tropical genera, bear bilobate, bifoliolate, or sometimes unifoliolate leaves, which constitute the tribe Cercideae as sister to the rest of the family Leguminosae based on molecular phylogenetics. Hence, the fossil record of Cercideae is pivotal to understand the early evolution and biogeographic history of legumes.
Results
Three fossil species of Bauhinia were described from the Oligocene Ningming Formation of Guangxi, South China. Bauhinia ningmingensis sp. nov. is characterized by its bifoliolate, pulvinate leaves bearing basal acrodromous primary veins and brochidodromous secondary veins. B. cheniae sp. nov. bears moderately or deeply bilobate, pulvinate leaves, with basal actinodromous primary veins and eucamptodromous secondary veins. B. larsenii D.X. Zhang et Y.F. Chen emend. possesses shallowly or moderately bilobate, pulvinate leaves bearing basal actinodromous primary veins and brochidodromous secondary veins, as well as elliptic, stipitate, non-winged, and oligo-seeded fruits. Meanwhile, previously reported Bauhinia fossils were reviewed, and those pre-Oligocene foliage across the world are either questionable or have been rejected due to lacking of reliable evidence for their pulvini or/and basal actinodromous or acrodromous venations. Besides Oligocene leaves and fruits presented here, foliage and/or wood of Bauhinia have been documented from the Miocene–Pliocene of Thailand, India, Nepal, Uganda, and Ecuador.
Conclusions
Bauhinia has exhibited a certain diversity with bifoliolate- and bilobate-leafed species in a low-latitude locality–Ningming since at least the Oligocene, implying that the tropical zone of South China may represent one of the centres for early diversification of the genus. The reliable macrofossils of Bauhinia and Cercis have made their debut in the Eocene–Oligocene floras from mid-low latitudes and appeared to lack in the coeval floras at high latitudes, implying a possible Tethys Seaway origin and spread of legumes. However, detailed scenarios for the historical biogeography of Bauhinia and its relatives still need more robust dataset from palaeobotany and molecular phylogeny in future research.
doi:10.1186/1471-2148-14-88
PMCID: PMC4101841  PMID: 24758153
Bauhinia; Bifoliolate leaf; Bilobate leaf; Biogeography; Cercideae; Cercis; Eocene; Evolution; Fruits; Legumes; Leguminosae; Low latitude; Ningming Formation; Oligocene; Pulvinus; Tethys Seaway origin; Unifoliolate leaf
4.  Mitogenomic Evidence for an Indo-West Pacific Origin of the Clupeoidei (Teleostei: Clupeiformes) 
PLoS ONE  2013;8(2):e56485.
The clupeoid fishes are distributed worldwide, with marine, freshwater and euryhaline species living in either tropical or temperate environments. Regional endemism is important at the species and genus levels, and the highest species diversity is found in the tropical marine Indo-West Pacific region. The clupeoid distribution follows two general pattern of species richness, the longitudinal and latitudinal gradients. To test historical hypotheses explaining the formation of these two gradients, we have examined the early biogeography of the Clupeoidei in reconstructing the evolution of their habitat preferences along with their ancestral range distributions on a time-calibrated mitogenomic phylogeny. The phylogenetic results support the distinction of nine main lineages within the Clupeoidei, five of them new. We infer several independent transitions from a marine to freshwater environment and from a tropical to temperate environment that occurred after the initial diversification period of the Clupeoidei. These results combined with our ancestral range reconstruction hypothesis suggest that the probable region of origin and diversification of the Clupeoidei during the Cretaceous period was the tropical marine precursor to the present Indo-West Pacific region. Thus, our study favors the hypotheses of “Region of origin” and “Tropical conservatism” to explain the origins of the longitudinal and latitudinal gradients of clupeoid species richness, respectively. Additional geological and paleontological evidence further define the tropical marine paleo-region of origin as the eastern Tethys Sea region. The Cretaceous fossil record of the Clupeoidei is partially incongruent with the results here as it contains taxa found outside this region. We discuss three possible causes of conflict between our biogeographical hypothesis and the distributions of the Cretaceous clupeoid fossils: regional extinction, incomplete taxonomic sampling and incorrect timescale estimation.
doi:10.1371/journal.pone.0056485
PMCID: PMC3576394  PMID: 23431379
5.  In the Wake of Invasion: Tracing the Historical Biogeography of the South American Cricetid Radiation (Rodentia, Sigmodontinae) 
PLoS ONE  2014;9(6):e100687.
The Great American Biotic Interchange (GABI) was greatly influenced by the completion of the Isthmus of Panama and impacted the composition of modern faunal assemblages in the Americas. However, the contribution of preceding events has been comparatively less explored, even though early immigrants in the fossil records are evidence for waif dispersals. The cricetid rodents of the subfamily Sigmodontinae are a classic example of a species-rich South American radiation resulting from an early episode of North American invasion. Here, we provide a temporal and spatial framework to address key aspects of the historical biogeography and diversification of this diverse mammal group by using mitochondrial and nuclear DNA datasets coupled with methods of divergence time estimation, ancestral area reconstruction and comparative phylogenetics. Relaxed-clock time estimates indicate that divergence of the Sigmodontinae began in the middle–late Miocene (ca. 12–9 Ma). Dispersal-vicariance analyses point to the arrival of a single lineage of northern invaders with a widespread ancestral distribution and imply that the initial differentiation between Central and South America gave rise to the most basal groups within the subfamily. These two major clades diversified in the late Miocene followed by the radiation of main tribes until the early Pliocene. Within the Oryzomyalia, tribes diverged initially in eastern South America whereas multiple dispersals into the Andes promoted further diversification of the majority of modern genera. A comparatively uniform background tempo of diversification explains the species richness of sigmodontines across most nodes, except for two akodontine genera with recent increases in diversification rates. The bridging of the Central American seaway and episodes of low sea levels likely facilitated the invasion of South America long before the onset of the post-Isthmian phase of the GABI.
doi:10.1371/journal.pone.0100687
PMCID: PMC4071052  PMID: 24963664
6.  Phylogenetic evidence for recent diversification of obligate coral-dwelling gobies compared with their host corals☆ 
Graphical abstract
Highlights
•The coral reef-dwelling genus Gobiodon diversified within the last 10 My.•Acroporid hosts of Gobiodon fishes have radiated since the Eocene (49 Mya).•Despite a mutualistic association Gobiodon fishes did not co-speciate with corals.•Testing dates of diversification is fundamental before assuming co-speciation.•Phylogenetics of Gobiodon differ in part with previous morphological analyses.
The rich diversity of coral reef organisms is supported, at least in part, by the diversity of coral reef habitat. Some of the most habitat specialised fishes on coral reefs are obligate coral-dwelling gobies of the genus Gobiodon that inhabit a range of coral species, mostly of the genus Acropora. However, the role of this specialised pattern of habitat use in the evolution of coral-dwelling gobies is not well understood. Diversification of coral-dwelling gobies may be driven by the diversification of their host corals (cospeciation), or alternatively, diversification of these fishes may have occurred independently of the diversification of host corals. The cospeciation hypothesis assumes similar timing in evolution of the gobies and their host corals. We used four genes for each group and the available fossil records to reconstruct and date phylogenies for 20 species of Gobiodon from the Indo-Pacific and the Red Sea, and for 28 species of the coral genus Acropora. Our results indicate that Gobiodon diversified mostly in the last ∼5 My, whereas Acropora corals have consistently diversified since the Eocene, making the hypothesis of cospeciation untenable. The fully resolved molecular phylogeny of the genus Gobiodon is in part at odds with previous analyses incorporating morphological data and indicates that some morphological traits form paraphyletic clades within Gobiodon. Our phylogeny supports a hypothesis in which Gobiodon diversified in the Indo-Pacific Ocean and then radiated recently, with multiple new variants found in the Red Sea.
doi:10.1016/j.ympev.2013.04.033
PMCID: PMC4047829  PMID: 23680856
Cospeciation; Mutualism; Coral reef; Gobiodon; Acropora; Molecular dating
7.  Major Radiations in the Evolution of Caviid Rodents: Reconciling Fossils, Ghost Lineages, and Relaxed Molecular Clocks 
PLoS ONE  2012;7(10):e48380.
Background
Caviidae is a diverse group of caviomorph rodents that is broadly distributed in South America and is divided into three highly divergent extant lineages: Caviinae (cavies), Dolichotinae (maras), and Hydrochoerinae (capybaras). The fossil record of Caviidae is only abundant and diverse since the late Miocene. Caviids belongs to Cavioidea sensu stricto (Cavioidea s.s.) that also includes a diverse assemblage of extinct taxa recorded from the late Oligocene to the middle Miocene of South America (“eocardiids”).
Results
A phylogenetic analysis combining morphological and molecular data is presented here, evaluating the time of diversification of selected nodes based on the calibration of phylogenetic trees with fossil taxa and the use of relaxed molecular clocks. This analysis reveals three major phases of diversification in the evolutionary history of Cavioidea s.s. The first two phases involve two successive radiations of extinct lineages that occurred during the late Oligocene and the early Miocene. The third phase consists of the diversification of Caviidae. The initial split of caviids is dated as middle Miocene by the fossil record. This date falls within the 95% higher probability distribution estimated by the relaxed Bayesian molecular clock, although the mean age estimate ages are 3.5 to 7 Myr older. The initial split of caviids is followed by an obscure period of poor fossil record (refered here as the Mayoan gap) and then by the appearance of highly differentiated modern lineages of caviids, which evidentially occurred at the late Miocene as indicated by both the fossil record and molecular clock estimates.
Conclusions
The integrated approach used here allowed us identifying the agreements and discrepancies of the fossil record and molecular clock estimates on the timing of the major events in cavioid evolution, revealing evolutionary patterns that would not have been possible to gather using only molecular or paleontological data alone.
doi:10.1371/journal.pone.0048380
PMCID: PMC3483234  PMID: 23144757
8.  470-Million-year-old black corals from China 
Die Naturwissenschaften  2012;99(8):645-653.
Phosphatic (possibly secondarily phosphatised) remains of antipatharian coralla, previously unknown in the fossil record, occur abundantly in the early Ordovician Fenxiang Formation in the Hubei Province, southern China. Probably two species (and genera) are represented, which differ in spinosity of branches. The more spinose one, Sinopathes reptans, has its lateral spines bearing regular, longitudinally arranged costellae. The early Floian geological age of this finding, about 470 Ma, supports predictions on the timing of anthozoan phylogeny derived from the molecular phylogenetic evidence. Black corals (Antipatharia) are basal to the scleractinians in the Hexacorallia clade, being more derived than sea anemones and the Zoantharia. Based on calibration of the molecular clock with Mesozoic data, the first split of lineages within the scleractinian hexacorals was proposed to take place approximately 425 million years ago. This implies that the origin of Antipatharia should precede this date. They have not been known in the fossil record because of unmineralised skeleton composed primarily of laminar chitin complexed with a protein. Unlike all recent species, the encrusting basal part of the colony dominated in the Ordovician ones and only occasionally erect branches developed, rather chaotically ramified. This presumably plesiomorphic trait seems consistent with ancient geological age and suggests that some problematic fossils from the Late Cambrian may be their, even less-derived, relatives.
doi:10.1007/s00114-012-0947-8
PMCID: PMC3407557  PMID: 22790835
Anthozoa; Phylogeny; Fossil record; Molecular clock; China
9.  Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales) 
Background
The aquatic flowering-plant family Hydatellaceae has a classic Gondwanan distribution, as it is found in Australia, India and New Zealand. To shed light on the biogeographic history of this apparently ancient branch of angiosperm phylogeny, we dated the family in the context of other seed-plant divergences, and evaluated its biogeography using parsimony and likelihood methods. We also explicitly tested the effect of different extinction rates on biogeographic inferences.
Results
We infer that the stem lineage of Hydatellaceae originated in the Lower Cretaceous; in contrast, its crown originated much more recently, in the early Miocene, with the bulk of its diversification after the onset of the Pliocene. Biogeographic reconstructions predict a mix of dispersal and vicariance events, but considerations of geological history preclude most vicariance events, besides a split at the root of the family between southern and northern clades. High extinction rates are plausible in the family, and when these are taken into account there is greater uncertainty in biogeographic inferences.
Conclusions
A stem origin for Hydatellaceae in the Lower Cretaceous is consistent with the initial appearance of fossils attributed to its sister clade, the water lilies. In contrast, the crown clade is young, indicating that vicariant explanations for species outside Australia are improbable. Although long-distance dispersal is likely the primary driver of biogeographic distribution in Hydatellaceae, we infer that the recent drying out of central Australia divided the family into tropical vs. subtropical/temperate clades around the beginning of the Miocene.
doi:10.1186/1471-2148-14-102
PMCID: PMC4030046  PMID: 24884487
Aquatic plants, Austral, Ephemeral habitats, Extinction rates, Intercontinental dispersal, ANITA-grade angiosperms, Trithuria; Vicariance
10.  Ancient Nursery Area for the Extinct Giant Shark Megalodon from the Miocene of Panama 
PLoS ONE  2010;5(5):e10552.
Background
As we know from modern species, nursery areas are essential shark habitats for vulnerable young. Nurseries are typically highly productive, shallow-water habitats that are characterized by the presence of juveniles and neonates. It has been suggested that in these areas, sharks can find ample food resources and protection from predators. Based on the fossil record, we know that the extinct Carcharocles megalodon was the biggest shark that ever lived. Previous proposed paleo-nursery areas for this species were based on the anecdotal presence of juvenile fossil teeth accompanied by fossil marine mammals. We now present the first definitive evidence of ancient nurseries for C. megalodon from the late Miocene of Panama, about 10 million years ago.
Methodology/Principal Findings
We collected and measured fossil shark teeth of C. megalodon, within the highly productive, shallow marine Gatun Formation from the Miocene of Panama. Surprisingly, and in contrast to other fossil accumulations, the majority of the teeth from Gatun are very small. Here we compare the tooth sizes from the Gatun with specimens from different, but analogous localities. In addition we calculate the total length of the individuals found in Gatun. These comparisons and estimates suggest that the small size of Gatun's C. megalodon is neither related to a small population of this species nor the tooth position within the jaw. Thus, the individuals from Gatun were mostly juveniles and neonates, with estimated body lengths between 2 and 10.5 meters.
Conclusions/Significance
We propose that the Miocene Gatun Formation represents the first documented paleo-nursery area for C. megalodon from the Neotropics, and one of the few recorded in the fossil record for an extinct selachian. We therefore show that sharks have used nursery areas at least for 10 millions of years as an adaptive strategy during their life histories.
doi:10.1371/journal.pone.0010552
PMCID: PMC2866656  PMID: 20479893
11.  A multi-locus species phylogeny of African forest duikers in the subfamily Cephalophinae: evidence for a recent radiation in the Pleistocene 
Background
Duikers in the subfamily Cephalophinae are a group of tropical forest mammals believed to have first originated during the late Miocene. However, knowledge of phylogenetic relationships, pattern and timing of their subsequent radiation is poorly understood. Here we present the first multi-locus phylogeny of this threatened group of tropical artiodactyls and use a Bayesian uncorrelated molecular clock to estimate divergence times.
Results
A total of 4152 bp of sequence data was obtained from two mitochondrial genes and four nuclear introns. Phylogenies were estimated using maximum parsimony, maximum likelihood, and Bayesian analysis of concatenated mitochondrial, nuclear and combined datasets. A relaxed molecular clock with two fossil calibration points was used to estimate divergence times. The first was based on the age of the split between the two oldest subfamilies within the Bovidae whereas the second was based on the earliest known fossil appearance of the Cephalophinae and molecular divergence time estimates for the oldest lineages within this group. Findings indicate strong support for four major lineages within the subfamily, all of which date to the late Miocene/early Pliocene. The first of these to diverge was the dwarf duiker genus Philantomba, followed by the giant, eastern and western red duiker lineages, all within the genus Cephalophus. While these results uphold the recognition of Philantomba, they do not support the monotypic savanna-specialist genus Sylvicapra, which as sister to the giant duikers leaves Cephalophus paraphyletic. BEAST analyses indicate that most sister species pairs originated during the Pleistocene, suggesting that repeated glacial cycling may have played an important role in the recent diversification of this group. Furthermore, several red duiker sister species pairs appear to be either paraphyletic (C.callipygus/C. ogilbyi and C. harveyi/C. natalensis) or exhibit evidence of mitochondrial admixture (C. nigrifrons and C. rufilatus), consistent with their recent divergence and/or possible hybridization with each other.
Conclusions
Molecular phylogenetic analyses suggest that Pleistocene-era climatic oscillations have played an important role in the speciation of this largely forest-dwelling group. Our results also reveal the most well supported species phylogeny for the subfamily to date, but also highlight several areas of inconsistency between our current understanding of duiker taxonomy and the evolutionary relationships depicted here. These findings may therefore prove particularly relevant to future conservation efforts, given that many species are presently regulated under the Convention for Trade in Endangered Species.
doi:10.1186/1471-2148-12-120
PMCID: PMC3523051  PMID: 22823504
Duiker; Pleistocene refuge hypothesis; Speciation; Molecular clock; Partition; Species tree
12.  Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages 
PLoS Biology  2009;7(3):e1000056.
The Neotropics contains half of remaining rainforests and Earth's largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.
Author Summary
The Neotropics, which includes South and Central America, contains half of remaining rainforests and the largest reservoir of amphibian diversity. Why there are so many species in certain areas and how such diversity arose before the Quaternary (i.e., more that 1.8 million years ago [MYA]) are largely unstudied. One hypothesis is that the Amazon Basin was the key source of diversity, and species dispersed from there to other areas. Here, we reconstruct a time-calibrated phylogeny and track, in space and time, the distribution of the endemic and species-rich clade of poison frogs (Dendrobatidae) during the Cenozoic (more than 65 MYA) across the continental Neotropics. Our results indicate a far more complex pattern of lineage dispersals and radiations during the past 10 MY. Rather than the Amazon Basin being the center of origin, our results show that the diversity stemmed from repeated dispersals from adjacent areas, especially from the Andes. We also found a recurrent pattern of colonization of Central America from the Chocó at 4–5 MY earlier than the formation of the Panamanian Land Bridge at 1.5 MYA. Thus, the major patterns of dispersals and radiations in the Neotropics were already set by ∼5–6 MYA (the Miocene–Pliocene boundary), but the ongoing process of Neotropical radiation is still happening now, especially in the Chocó–Central America region and Amazonian rainforest.
Phylogenetic analysis and ancestral range modeling of the poison-frog clade (Dendrobatidae) indicates that Amazonian species richness derives from repeated dispersals from adjacent regions, especially the Andes.
doi:10.1371/journal.pbio.1000056
PMCID: PMC2653552  PMID: 19278298
13.  Phylogenetic Analysis of Pelecaniformes (Aves) Based on Osteological Data: Implications for Waterbird Phylogeny and Fossil Calibration Studies 
PLoS ONE  2010;5(10):e13354.
Background
Debate regarding the monophyly and relationships of the avian order Pelecaniformes represents a classic example of discord between morphological and molecular estimates of phylogeny. This lack of consensus hampers interpretation of the group's fossil record, which has major implications for understanding patterns of character evolution (e.g., the evolution of wing-propelled diving) and temporal diversification (e.g., the origins of modern families). Relationships of the Pelecaniformes were inferred through parsimony analyses of an osteological dataset encompassing 59 taxa and 464 characters. The relationships of the Plotopteridae, an extinct family of wing-propelled divers, and several other fossil pelecaniforms (Limnofregata, Prophaethon, Lithoptila, ?Borvocarbo stoeffelensis) were also assessed. The antiquity of these taxa and their purported status as stem members of extant families makes them valuable for studies of higher-level avian diversification.
Methodology/Principal Findings
Pelecaniform monophyly is not recovered, with Phaethontidae recovered as distantly related to all other pelecaniforms, which are supported as a monophyletic Steganopodes. Some anatomical partitions of the dataset possess different phylogenetic signals, and partitioned analyses reveal that these discrepancies are localized outside of Steganopodes, and primarily due to a few labile taxa. The Plotopteridae are recovered as the sister taxon to Phalacrocoracoidea, and the relationships of other fossil pelecaniforms representing key calibration points are well supported, including Limnofregata (sister taxon to Fregatidae), Prophaethon and Lithoptila (successive sister taxa to Phaethontidae), and ?Borvocarbo stoeffelensis (sister taxon to Phalacrocoracidae). These relationships are invariant when ‘backbone’ constraints based on recent avian phylogenies are imposed.
Conclusions/Significance
Relationships of extant pelecaniforms inferred from morphology are more congruent with molecular phylogenies than previously assumed, though notable conflicts remain. The phylogenetic position of the Plotopteridae implies that wing-propelled diving evolved independently in plotopterids and penguins, representing a remarkable case of convergent evolution. Despite robust support for the placement of fossil taxa representing key calibration points, the successive outgroup relationships of several “stem fossil + crown family” clades are variable and poorly supported across recent studies of avian phylogeny. Thus, the impact these fossils have on inferred patterns of temporal diversification depends heavily on the resolution of deep nodes in avian phylogeny.
doi:10.1371/journal.pone.0013354
PMCID: PMC2954798  PMID: 20976229
14.  Palaeontological Evidence for the Last Temporal Occurrence of the Ancient Western Amazonian River Outflow into the Caribbean 
PLoS ONE  2013;8(9):e76202.
Fossil catfishes from fluvio-lacustrine facies of late Miocene Urumaco, early Pliocene Castilletes and late Pliocene San Gregorio formations provide evidence of a hydrographic connection in what is today desert regions of northern Colombia and Venezuela. New discoveries and reevaluation of existing materials leads to the recognition of two new records of the pimelodid Brachyplatystoma cf. vaillantii, and of three distinct doradid taxa: Doraops sp., Rhinodoras sp., and an unidentified third form. The presence of fossil goliath long-whiskered catfishes and thorny catfishes are indicative of the persistence of a fluvial drainage system inflow into the South Caribbean during the Pliocene/Pleistocene boundary, complementary to the previous western Amazonian hydrographic system described from the Middle Miocene Villavieja Formation in central Colombia and Late Miocene Urumaco Formation in northwestern Venezuela. The Pliocene Castilletes and San Gregorio formations potentially represent the last lithostratigraphic units related with an ancient western Amazonian fish fauna and that drainage system in the Caribbean. Alternatively, it may preserve faunas from a smaller, peripheral river basin that was cut off earlier from the Amazon-Orinoco, today found in the Maracaibo basin and the Magdalena Rivers.
doi:10.1371/journal.pone.0076202
PMCID: PMC3786985  PMID: 24098778
15.  Macroevolutionary Dynamics and Historical Biogeography of Primate Diversification Inferred from a Species Supermatrix 
PLoS ONE  2012;7(11):e49521.
Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
doi:10.1371/journal.pone.0049521
PMCID: PMC3500307  PMID: 23166696
16.  DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities 
Scientific Reports  2013;3:1520.
Stylophora pistillata is a widely used coral “lab-rat” species with highly variable morphology and a broad biogeographic range (Red Sea to western central Pacific). Here we show, by analysing Cytochorme Oxidase I sequences, from 241 samples across this range, that this taxon in fact comprises four deeply divergent clades corresponding to the Pacific-Western Australia, Chagos-Madagascar-South Africa, Gulf of Aden-Zanzibar-Madagascar, and Red Sea-Persian/Arabian Gulf-Kenya. On the basis of the fossil record of Stylophora, these four clades diverged from one another 51.5-29.6 Mya, i.e., long before the closure of the Tethyan connection between the tropical Indo-West Pacific and Atlantic in the early Miocene (16–24 Mya) and should be recognised as four distinct species. These findings have implications for comparative ecological and/or physiological studies carried out using Stylophora pistillata as a model species, and highlight the fact that phenotypic plasticity, thought to be common in scleractinian corals, can mask significant genetic variation.
doi:10.1038/srep01520
PMCID: PMC3605610  PMID: 23519209
17.  Anthropogenic extinction threats and future loss of evolutionary history in reef corals 
Ecology and Evolution  2013;3(5):1184-1193.
Extinction always results in loss of phylogenetic diversity (PD), but phylogenetically selective extinctions have long been thought to disproportionately reduce PD. Recent simulations show that tree shapes also play an important role in determining the magnitude of PD loss, potentially offsetting the effects of clustered extinctions. While patterns of PD loss under different extinction scenarios are becoming well characterized in model phylogenies, analyses of real clades that often have unbalanced tree shapes remain scarce, particularly for marine organisms. Here, we use a fossil-calibrated phylogeny of all living scleractinian reef corals in conjunction with IUCN data on extinction vulnerabilities to quantify how loss of species in different threat categories will affect the PD of this group. Our analyses reveal that predicted PD loss in corals varies substantially among different threats, with extinctions due to bleaching and disease having the largest negative effects on PD. In general, more phylogenetically clustered extinctions lead to larger losses of PD in corals, but there are notable exceptions; extinction of rare corals from distantly-related old and unique lineages can also result in substantial PD loss. Thus our results show that loss of PD in reef corals is dependent on both tree shape and the nature of extinction threats.
doi:10.1002/ece3.527
PMCID: PMC3678474  PMID: 23762506
Phylogenetic conservatism; phylogenetic diversity; Scleractinia; supertree; tree shape
18.  Long Distance Dispersal and Connectivity in Amphi-Atlantic Corals at Regional and Basin Scales 
PLoS ONE  2011;6(7):e22298.
Among Atlantic scleractinian corals, species diversity is highest in the Caribbean, but low diversity and high endemism are observed in various peripheral populations in central and eastern Atlantic islands and along the coasts of Brazil and West Africa. The degree of connectivity between these distantly separated populations is of interest because it provides insight into processes at both evolutionary and ecological time scales, such as speciation, recruitment dynamics and the persistence of coral populations. To assess connectivity in broadly distributed coral species of the Atlantic, DNA sequence data from two nuclear markers were obtained for six coral species spanning their distributional ranges. At basin-wide scales, significant differentiation was generally observed among populations in the Caribbean, Brazil and West Africa. Concordance of patterns in connectivity among co-distributed taxa indicates that extrinsic barriers, such as the Amazon freshwater plume or long stretches of open ocean, restrict dispersal of coral larvae from region to region. Within regions, dispersal ability appears to be influenced by aspects of reproduction and life history. Two broadcasting species, Siderastrea siderea and Montastraea cavernosa, were able to maintain gene flow among populations separated by as much as 1,200 km along the coast of Brazil. In contrast, brooding species, such as Favia gravida and Siderastrea radians, had more restricted gene flow along the Brazilian coast.
doi:10.1371/journal.pone.0022298
PMCID: PMC3142122  PMID: 21799816
19.  Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages 
BMC Biology  2008;6:6.
Background
Determining an absolute timescale for avian evolutionary history has proven contentious. The two sources of information available, paleontological data and inference from extant molecular genetic sequences (colloquially, 'rocks' and 'clocks'), have appeared irreconcilable; the fossil record supports a Cenozoic origin for most modern lineages, whereas molecular genetic estimates suggest that these same lineages originated deep within the Cretaceous and survived the K-Pg (Cretaceous-Paleogene; formerly Cretaceous-Tertiary or K-T) mass-extinction event. These two sources of data therefore appear to support fundamentally different models of avian evolution. The paradox has been speculated to reflect deficiencies in the fossil record, unrecognized biases in the treatment of genetic data or both. Here we attempt to explore uncertainty and limit bias entering into molecular divergence time estimates through: (i) improved taxon (n = 135) and character (n = 4594 bp mtDNA) sampling; (ii) inclusion of multiple cladistically tested internal fossil calibration points (n = 18); (iii) correction for lineage-specific rate heterogeneity using a variety of methods (n = 5); (iv) accommodation of uncertainty in tree topology; and (v) testing for possible effects of episodic evolution.
Results
The various 'relaxed clock' methods all indicate that the major (basal) lineages of modern birds originated deep within the Cretaceous, although temporal intraordinal diversification patterns differ across methods. We find that topological uncertainty had a systematic but minor influence on date estimates for the origins of major clades, and Bayesian analyses assuming fixed topologies deliver similar results to analyses with unconstrained topologies. We also find that, contrary to expectation, rates of substitution are not autocorrelated across the tree in an ancestor-descendent fashion. Finally, we find no signature of episodic molecular evolution related to either speciation events or the K-Pg boundary that could systematically mislead inferences from genetic data.
Conclusion
The 'rock-clock' gap has been interpreted by some to be a result of the vagaries of molecular genetic divergence time estimates. However, despite measures to explore different forms of uncertainty in several key parameters, we fail to reconcile molecular genetic divergence time estimates with dates taken from the fossil record; instead, we find strong support for an ancient origin of modern bird lineages, with many extant orders and families arising in the mid-Cretaceous, consistent with previous molecular estimates. Although there is ample room for improvement on both sides of the 'rock-clock' divide (e.g. accounting for 'ghost' lineages in the fossil record and developing more realistic models of rate evolution for molecular genetic sequences), the consistent and conspicuous disagreement between these two sources of data more likely reflects a genuine difference between estimated ages of (i) stem-group origins and (ii) crown-group morphological diversifications, respectively. Further progress on this problem will benefit from greater communication between paleontologists and molecular phylogeneticists in accounting for error in avian lineage age estimates.
doi:10.1186/1741-7007-6-6
PMCID: PMC2267772  PMID: 18226223
20.  Himalayan fossils of the oldest known pantherine establish ancient origin of big cats 
Pantherine felids (‘big cats’) include the largest living cats, apex predators in their respective ecosystems. They are also the earliest diverging living cat lineage, and thus are important for understanding the evolution of all subsequent felid groups. Although the oldest pantherine fossils occur in Africa, molecular phylogenies point to Asia as their region of origin. This paradox cannot be reconciled using current knowledge, mainly because early big cat fossils are exceedingly rare and fragmentary. Here, we report the discovery of a fossil pantherine from the Tibetan Himalaya, with an age of Late Miocene–Early Pliocene, replacing African records as the oldest pantherine. A ‘total evidence’ phylogenetic analysis of pantherines indicates that the new cat is closely related to the snow leopard and exhibits intermediate characteristics on the evolutionary line to the largest cats. Historical biogeographic models provide robust support for the Asian origin of pantherines. The combined analyses indicate that 75% of the divergence events in the pantherine lineage extended back to the Miocene, up to 7 Myr earlier than previously estimated. The deeper evolutionary origin of big cats revealed by the new fossils and analyses indicate a close association between Tibetan Plateau uplift and diversification of the earliest living cats.
doi:10.1098/rspb.2013.2686
PMCID: PMC3843846  PMID: 24225466
first appearance; Himalaya; Pantherinae; Felidae; Miocene; Asia
21.  Late Cenozoic History of the Genus Micromys (Mammalia, Rodentia) in Central Europe 
PLoS ONE  2013;8(5):e62498.
Molecular phylogeography suggests that Micromys minutus, the sole extant species of the genus, colonized its extensive range quite recently, during the Late Pleistocene-Holocene period. Rich Pliocene and Pleistocene fossil records both from Europe and China suggest rather continuous and gradual in situ phenotype rearrangements from the Pliocene to the Recent periods. To elucidate the discrepancy we reexamined a considerable part of the European fossil record of the genus (14 sites from MN15 to Q3, 0.4–4.2 Ma, including the type series of M. preaminutus from MN15 Csarnóta 2), analyzed them with the aid of detailed morphometric comparisons, and concluded that: (a) The European Pliocene form, M. praeminutus, differs significantly from the extant species; (b) it exhibits a broad phenotypic variation covering the presumptive diagnostic characters of MN16 M. caesaris; (c) despite having smaller dimensions, the Early and Middle Pleistocene forms (MN17-Q3, 2.6–0.4 Ma) seem to be closer to M. praeminutus than to the extant species; (d) the extinction of M. praeminutus during Q3 and the re-occupation of its niche by the recent expansion of M. minutus from E-European – C Asiatic sources (suggested by phylogeographic hypotheses) cannot be excluded. Discussing interpretations of the phylogenetic past of the genus we emphasize the distinct history of the West Palearctic clade (Late Miocene-Early Pleistocene) terminating with M. praeminutus and the East Asiatic clade (chalceus, tedfordi, minutus), and the possible identity of the Western clade with the Late Miocene genus Parapodemus.
doi:10.1371/journal.pone.0062498
PMCID: PMC3646007  PMID: 23671605
22.  A multi-locus inference of the evolutionary diversification of extant flamingos (Phoenicopteridae) 
Background
Modern flamingos (Phoenicopteridae) occupy a highly specialized ecology unique among birds and represent a potentially powerful model system for informing the mechanisms by which a lineage of birds adapts and radiates. However, despite a rich fossil record and well-studied feeding morphology, molecular investigations of the evolutionary progression among modern flamingos have been limited. Here, using three mitochondrial (mtDNA) markers, we present the first DNA sequence-based study of population genetic variation in the widely distributed Chilean Flamingo and, using two mtDNA and 10 nuclear (nDNA) markers, recover the species tree and divergence time estimates for the six extant species of flamingos. Phylogenetic analyses include likelihood and Bayesian frameworks and account for potential gene tree discordance. Analyses of divergence times are fossil calibrated at the divergence of Mirandornithes (flamingos + grebes) and the divergence of crown grebes.
Results
mtDNA sequences confirmed the presence of a single metapopulation represented by two minimally varying mtDNA barcodes in Chilean flamingos. Likelihood and Bayesian methods recovered identical phylogenies with flamingos falling into shallow-keeled (comprising the Greater, American and Chilean Flamingos) and deep-keeled (comprising the Lesser, Andean and James’s Flamingos) sub-clades. The initial divergence among flamingos occurred at or shortly after the Mio-Pliocene boundary (6–3 Ma) followed by quick consecutive divergences throughout the Plio-Pleistocene. There is significant incongruence between the ages recovered by the mtDNA and nDNA datasets, likely due to mutational saturation occurring in the mtDNA loci.
Conclusion
The finding of a single metapopulation in the widespread Chilean Flamingo confirms similar findings in other widespread flamingo species. The robust species phylogeny is congruent with previous classifications of flamingos based on feeding morphology. Modern phoenicopterids likely originated in the New World with each sub-clade dispersing across the Atlantic at least once. Our divergence time estimates place flamingos among the youngest families of birds, counter to the classical notion of flamingos as among the oldest based on biogeography and the fossil record. Finally, we designate ‘Phoeniconaias’ as a junior synonym of ‘Phoenicoparrus’ and redefine the latter genus as containing all flamingos more closely related to Phoenicoparrus andinus than Phoenicopterus roseus.
doi:10.1186/1471-2148-14-36
PMCID: PMC4016592  PMID: 24580860
Flamingo; Phylogeny; Divergence time; Biogeography; Fossil; Bill; Filter feeding
23.  An Extraordinary Gobioid Fish Fossil from Southern France 
PLoS ONE  2013;8(5):e64117.
Background
The classification of gobioid fishes is still under discussion. Several lineages, including the Eleotridae and Butidae, remain difficult to characterize because synapomorphies are rare (Eleotridae) or have not yet been determined (Butidae). Moreover, the fossil record of these groups is scarce.
Results
Exceptionally well-preserved fish fossils with otoliths in situ from uppermost Oligocene sediments (≈23–24 Mio. y. ago) in Southern France provide the most in-depth description of a fossil gobioid to date. The species was initially described as Cottus aries Agassiz, then transferred to †Lepidocottus Sauvage, and subsequently assigned to Gobius. Based on a comparative analysis of meristic, osteological and otolith data, this species most likely is a member of the family Butidae. This discovery is important because it represents the first record of a fossil butid fish based on articulated skeletons from Europe.
Significance
The Butidae and Eleotridae are currently distributed in W-Africa, Madagascar, Asia and Australia, but they do not appear in Europe and also not in the Mediterranean Sea. The new results indicate that several species of the Butidae thrived in Europe during the Oligocene and Early Miocene. Similar to the recent Butidae and Eleotridae, these fishes were adapted to a wide range of salinities and thrived in freshwater, brackish and marginal marine habitats. The fossil Butidae disappeared from Europe and the Mediterranean and Paratethys areas during the Early Miocene, due probably to their lack of competitiveness compared to other Gobioidei that radiated during this period of time. In addition, this study documents the great value of otoliths for gobioid systematics.
doi:10.1371/journal.pone.0064117
PMCID: PMC3655028  PMID: 23691158
24.  Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability 
The risk of global extinction of reef-building coral species is increasing. We evaluated extinction risk using a biological trait-based resiliency index that was compared with Caribbean extinction during the Plio-Pleistocene, and with extinction risk determined by the International Union for Conservation of Nature (IUCN). Through the Plio-Pleistocene, the Caribbean supported more diverse coral assemblages than today and shared considerable overlap with contemporary Indo-Pacific reefs. A clear association was found between extant Plio-Pleistocene coral genera and our positive resilience scores. Regional extinction in the past and vulnerability in the present suggests that Pocillopora, Stylophora and foliose Pavona are among the most susceptible taxa to local and regional isolation. These same taxa were among the most abundant corals in the Caribbean Pliocene. Therefore, a widespread distribution did not equate with immunity to regional extinction. The strong relationship between past and present vulnerability suggests that regional extinction events are trait-based and not merely random episodes. We found several inconsistencies between our data and the IUCN scores, which suggest a need to critically re-examine what constitutes coral vulnerability.
doi:10.1098/rspb.2011.2621
PMCID: PMC3350676  PMID: 22337694
biological trait; coral; extinction risk; Plio-Pleistocene; resilience; vulnerability
25.  A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics 
Background
Molecular phylogenetics has provided unprecedented resolution in the ruminant evolutionary tree. However, molecular age estimates using only one or a few (often misapplied) fossil calibration points have produced a diversity of conflicting ages for important evolutionary events within this clade. I here identify 16 fossil calibration points of relevance to the phylogeny of Bovidae and Ruminantia and use these, individually and together, to construct a dated molecular phylogeny through a reanalysis of the full mitochondrial genome of over 100 ruminant species.
Results
The new multi-calibrated tree provides ages that are younger overall than found in previous studies. Among these are young ages for the origin of crown Ruminantia (39.3–28.8 Ma), and crown Bovidae (17.3–15.1 Ma). These are argued to be reasonable hypotheses given that many basal fossils assigned to these taxa may in fact lie on the stem groups leading to the crown clades, thus inflating previous age estimates. Areas of conflict between molecular and fossil dates do persist, however, especially with regard to the base of the rapid Pecoran radiation and the sister relationship of Moschidae to Bovidae. Results of the single-calibrated analyses also show that a very wide range of molecular age estimates are obtainable using different calibration points, and that the choice of calibration point can influence the topology of the resulting tree. Compared to the single-calibrated trees, the multi-calibrated tree exhibits smaller variance in estimated ages and better reflects the fossil record.
Conclusions
The use of a large number of vetted fossil calibration points with soft bounds is promoted as a better approach than using just one or a few calibrations, or relying on internal-congruency metrics to discard good fossil data. This study also highlights the importance of considering morphological and ecological characteristics of clades when delimiting higher taxa. I also illustrate how phylogeographic and paleoenvironmental hypotheses inferred from a tree containing only extant taxa can be problematic without consideration of the fossil record. Incorporating the fossil record of Ruminantia is a necessary step for future analyses aiming to reconstruct the evolutionary history of this clade.
doi:10.1186/1471-2148-13-166
PMCID: PMC3751017  PMID: 23927069
Fossil calibration; Ruminantia; Bayesian analysis; Phylogenetic systematics; Neogene

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