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1.  The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals 
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.
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.
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.
PMCID: PMC3224782  PMID: 22034946
2.  Phylogenetic evidence for recent diversification of obligate coral-dwelling gobies compared with their host corals☆ 
Graphical abstract
•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.
PMCID: PMC4047829  PMID: 23680856
Cospeciation; Mutualism; Coral reef; Gobiodon; Acropora; Molecular dating
3.  Major Radiations in the Evolution of Caviid Rodents: Reconciling Fossils, Ghost Lineages, and Relaxed Molecular Clocks 
PLoS ONE  2012;7(10):e48380.
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”).
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.
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.
PMCID: PMC3483234  PMID: 23144757
4.  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.
PMCID: PMC3616043  PMID: 23573205
5.  Leaves and fruits of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the Oligocene Ningming Formation of Guangxi, South China and their biogeographic implications 
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.
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.
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.
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
6.  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.
PMCID: PMC3576394  PMID: 23431379
7.  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.
PMCID: PMC4071052  PMID: 24963664
8.  Phylogenetic Analysis of Pelecaniformes (Aves) Based on Osteological Data: Implications for Waterbird Phylogeny and Fossil Calibration Studies 
PLoS ONE  2010;5(10):e13354.
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.
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.
PMCID: PMC2954798  PMID: 20976229
9.  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.
PMCID: PMC3407557  PMID: 22790835
Anthozoa; Phylogeny; Fossil record; Molecular clock; China
10.  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.
PMCID: PMC3605610  PMID: 23519209
11.  Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales) 
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.
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.
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.
PMCID: PMC4030046  PMID: 24884487
Aquatic plants, Austral, Ephemeral habitats, Extinction rates, Intercontinental dispersal, ANITA-grade angiosperms, Trithuria; Vicariance
12.  Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages 
BMC Biology  2008;6:6.
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.
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.
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.
PMCID: PMC2267772  PMID: 18226223
13.  A multi-locus inference of the evolutionary diversification of extant flamingos (Phoenicopteridae) 
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.
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.
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.
PMCID: PMC4016592  PMID: 24580860
Flamingo; Phylogeny; Divergence time; Biogeography; Fossil; Bill; Filter feeding
14.  A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics 
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.
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.
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.
PMCID: PMC3751017  PMID: 23927069
Fossil calibration; Ruminantia; Bayesian analysis; Phylogenetic systematics; Neogene
15.  Molecules, morphometrics and new fossils provide an integrated view of the evolutionary history of Rhinopomatidae (Mammalia: Chiroptera) 
The Rhinopomatidae, traditionally considered to be one of the most ancient chiropteran clades, remains one of the least known groups of Rhinolophoidea. No relevant fossil record is available for this family. Whereas there have been extensive radiations in related families Rhinolophidae and Hipposideridae, there are only a few species in the Rhinopomatidae and their phylogenetic relationship and status are not fully understood.
Here we present (a) a phylogenetic analysis based on a partial cytochrome b sequence, (b) new fossils from the Upper Miocene site Elaiochoria 2 (Chalkidiki, Greece), which represents the first appearance datum of the family based on the fossil record, and (c) discussion of the phylogeographic patterns in both molecular and morphological traits. We found deep divergences in the Rhinopoma hardwickii lineage, suggesting that the allopatric populations in (i) Iran and (ii) North Africa and the Middle East should have separate species status. The latter species (R. cystops) exhibits a shallow pattern of isolation by distance (separating the Middle East and the African populations) that contrasts with the pattern of geographic variation in the morphometrical traits. A deep genetic gap was also found in Rhinopoma muscatellum (Iran vs. Yemen). We found only minute genetic distance between R. microphyllum from the Levant and India, which fails to support the sub/species distinctness of the Indian form (R. microphyllum kinneari).
The mtDNA survey provided phylogenetic tree of the family Rhinopomatidae for the first time and revealed an unexpected diversification of the group both within R. hardwickii and R. muscatellum morphospecies. The paleobiogeographic scenario compiled in respect to molecular clock data suggests that the family originated in the region south of the Eocene Western Tethyan seaway or in India, and extended its range during the Early Miocene. The fossil record suggests a Miocene spread into the Mediterranean region, followed by a post-Miocene retreat. Morphological analysis compared with genetic data indicates considerable phenotypic plasticity in this group.
PMCID: PMC2249596  PMID: 17868440
16.  Evolutionary divergence times in the Annonaceae: evidence of a late Miocene origin of Pseuduvaria in Sundaland with subsequent diversification in New Guinea 
Phylogenetic analyses of the Annonaceae consistently identify four clades: a basal clade consisting of Anaxagorea, and a small 'ambavioid' clade that is sister to two main clades, the 'long branch clade' (LBC) and 'short branch clade' (SBC). Divergence times in the family have previously been estimated using non-parametric rate smoothing (NPRS) and penalized likelihood (PL). Here we use an uncorrelated lognormal (UCLD) relaxed molecular clock in BEAST to estimate diversification times of the main clades within the family with a focus on the Asian genus Pseuduvaria within the SBC. Two fossil calibration points are applied, including the first use of the recently discovered Annonaceae fossil Futabanthus. The taxonomy and morphology of Pseuduvaria have been well documented, although no previous dating or biogeographical studies have been undertaken. Ancestral areas at internal nodes within Pseuduvaria are determined using dispersal-vicariance analysis (DIVA) and weighted ancestral area analysis (WAAA).
The divergence times of the main clades within the Annonaceae were found to deviate slightly from previous estimates that used different calibration points and dating methods. In particular, our estimate for the SBC crown (55.2-26.9 Mya) is much younger than previous estimates (62.5-53.1 ± 3.6 Mya and ca. 58.76 Mya). Early diversification of Pseuduvaria was estimated to have occurred 15-8 Mya, possibly associated with the 'mid-Miocene climatic optimum.' Pseuduvaria is inferred to have originated in Sundaland in the late Miocene, ca. 8 Mya; subsequent migration events were predominantly eastwards towards New Guinea and Australia, although several migratory reversals are also postulated. Speciation of Pseuduvaria within New Guinea may have occurred after ca. 6.5 Mya, possibly coinciding with the formation of the Central Range orogeny from ca. 8 Mya.
Our divergence time estimates within the Annonaceae are likely to be more precise as we used a UCLD clock model and calibrated the phylogeny using new fossil evidence. Pseuduvaria is shown to have dispersed from Sundaland after the late Miocene. The present-day paleotropical distribution of Pseuduvaria may have been achieved by long-distance dispersal, and speciation events might be explained by global climatic oscillations, sea level fluctuations, and tectonic activity.
PMCID: PMC2722625  PMID: 19573225
17.  Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara) 
Lepidosauria (lizards, snakes, tuatara) is a globally distributed and ecologically important group of over 9,000 reptile species. The earliest fossil records are currently restricted to the Late Triassic and often dated to 227 million years ago (Mya). As these early records include taxa that are relatively derived in their morphology (e.g. Brachyrhinodon), an earlier unknown history of Lepidosauria is implied. However, molecular age estimates for Lepidosauria have been problematic; dates for the most recent common ancestor of all lepidosaurs range between approximately 226 and 289 Mya whereas estimates for crown-group Squamata (lizards and snakes) vary more dramatically: 179 to 294 Mya. This uncertainty restricts inferences regarding the patterns of diversification and evolution of Lepidosauria as a whole.
Here we report on a rhynchocephalian fossil from the Middle Triassic of Germany (Vellberg) that represents the oldest known record of a lepidosaur from anywhere in the world. Reliably dated to 238–240 Mya, this material is about 12 million years older than previously known lepidosaur records and is older than some but not all molecular clock estimates for the origin of lepidosaurs. Using RAG1 sequence data from 76 extant taxa and the new fossil specimens two of several calibrations, we estimate that the most recent common ancestor of Lepidosauria lived at least 242 Mya (238–249.5), and crown-group Squamata originated around 193 Mya (176–213).
A Early/Middle Triassic date for the origin of Lepidosauria disagrees with previous estimates deep within the Permian and suggests the group evolved as part of the faunal recovery after the end-Permain mass extinction as the climate became more humid. Our origin time for crown-group Squamata coincides with shifts towards warmer climates and dramatic changes in fauna and flora. Most major subclades within Squamata originated in the Cretaceous postdating major continental fragmentation. The Vellberg fossil locality is expected to become an important resource for providing a more balanced picture of the Triassic and for bridging gaps in the fossil record of several other major vertebrate groups.
PMCID: PMC4016551  PMID: 24063680
Dating; Fossil; Jurassic; Lepidosauria; Lizards; Molecular; Origin; Squamata; Triassic; Tuatara
18.  Ancient Nursery Area for the Extinct Giant Shark Megalodon from the Miocene of Panama 
PLoS ONE  2010;5(5):e10552.
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.
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.
PMCID: PMC2866656  PMID: 20479893
19.  A multi-locus species phylogeny of African forest duikers in the subfamily Cephalophinae: evidence for a recent radiation in the Pleistocene 
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.
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.
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.
PMCID: PMC3523051  PMID: 22823504
Duiker; Pleistocene refuge hypothesis; Speciation; Molecular clock; Partition; Species tree
20.  Divergence Times and the Evolutionary Radiation of New World Monkeys (Platyrrhini, Primates): An Analysis of Fossil and Molecular Data 
PLoS ONE  2013;8(6):e68029.
The estimation of phylogenetic relationships and divergence times among a group of organisms is a fundamental first step toward understanding its biological diversification. The time of the most recent or last common ancestor (LCA) of extant platyrrhines is one of the most controversial among scholars of primate evolution. Here we use two molecular based approaches to date the initial divergence of the platyrrhine clade, Bayesian estimations under a relaxed-clock model and substitution rate plus generation time and body size, employing the fossil record and genome datasets. We also explore the robustness of our estimations with respect to changes in topology, fossil constraints and substitution rate, and discuss the implications of our findings for understanding the platyrrhine radiation. Our results suggest that fossil constraints, topology and substitution rate have an important influence on our divergence time estimates. Bayesian estimates using conservative but realistic fossil constraints suggest that the LCA of extant platyrrhines existed at ca. 29 Ma, with the 95% confidence limit for the node ranging from 27–31 Ma. The LCA of extant platyrrhine monkeys based on substitution rate corrected by generation time and body size was established between 21–29 Ma. The estimates based on the two approaches used in this study recalibrate the ages of the major platyrrhine clades and corroborate the hypothesis that they constitute very old lineages. These results can help reconcile several controversial points concerning the affinities of key early Miocene fossils that have arisen among paleontologists and molecular systematists. However, they cannot resolve the controversy of whether these fossil species truly belong to the extant lineages or to a stem platyrrhine clade. That question can only be resolved by morphology. Finally, we show that the use of different approaches and well supported fossil information gives a more robust divergence time estimate of a clade.
PMCID: PMC3694915  PMID: 23826358
21.  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.
PMCID: PMC2653552  PMID: 19278298
22.  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.
PMCID: PMC3500307  PMID: 23166696
23.  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.
PMCID: PMC3786985  PMID: 24098778
24.  Iterative Evolution of Sympatric Seacow (Dugongidae, Sirenia) Assemblages during the Past ∼26 Million Years 
PLoS ONE  2012;7(2):e31294.
Extant sirenians show allopatric distributions throughout most of their range. However, their fossil record shows evidence of multispecies communities throughout most of the past ∼26 million years, in different oceanic basins. Morphological differences among co-occurring sirenian taxa suggest that resource partitioning played a role in structuring these communities. We examined body size and ecomorphological differences (e.g., rostral deflection and tusk morphology) among sirenian assemblages from the late Oligocene of Florida, early Miocene of India and early Pliocene of Mexico; each with three species of the family Dugongidae. Although overlapping in several ecomorphological traits, each assemblage showed at least one dominant trait in which coexisting species differed. Fossil sirenian occurrences occasionally are monotypic, but the assemblages analyzed herein show iterative evolution of multispecies communities, a phenomenon unparalleled in extant sirenian ecology. As primary consumers of seagrasses, these communities likely had a strong impact on past seagrass ecology and diversity, although the sparse fossil record of seagrasses limits direct comparisons. Nonetheless, our results provide robust support for previous suggestions that some sirenians in these extinct assemblages served as keystone species, controlling the dominance of climax seagrass species, permitting more taxonomically diverse seagrass beds (and sirenian communities) than many of those observed today.
PMCID: PMC3272043  PMID: 22319622
25.  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.
PMCID: PMC3678474  PMID: 23762506
Phylogenetic conservatism; phylogenetic diversity; Scleractinia; supertree; tree shape

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