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1.  Bilobate leaves of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the middle Miocene of Fujian Province, southeastern China and their biogeographic implications 
Morphological and molecular phylogenetic studies suggest that the pantropical genus Bauhinia L. s.l. (Bauhiniinae, Cercideae, Leguminosae) is paraphyletic and may as well be subdivided into nine genera, including Bauhinia L. s.s. and its allies. Their leaves are usually characteristic bilobate and are thus easily recognized in the fossil record. This provides the opportunity to understand the early evolution, diversification, and biogeographic history of orchid trees from an historical perspective under the framework of morphological and molecular studies.
The taxonomy, distribution, and leaf architecture of Bauhinia and its allies across the world are summarized in detail, which formed the basis for classifying the bilobate leaf fossils and evaluating the fossil record and biogeography of Bauhinia. Two species of Bauhinia are described from the middle Miocene Fotan Group of Fujian Province, southeastern China. Bauhinia ungulatoides sp. nov. is characterized by shallowly to moderately bilobate, pulvinate leaves with shallowly cordate bases and acute apices on each lobe, as well as paracytic stomatal complexes. Bauhinia fotana F.M.B. Jacques et al. emend. possesses moderately bilobate, pulvinate leaves with moderately to deeply cordate bases and acute or slightly obtuse apices on each lobe.
Bilobate leaf fossils Bauhinia ungulatoides and B. fotana together with other late Paleogene – early Neogene Chinese record of the genus suggest that Bauhinia had been diverse in South China by the late Paleogene. Their great similarities to some species from South America and South Asia respectively imply that Bauhinia might have undergone extensive dispersals and diversification during or before the Miocene. The fossil record, extant species diversity, as well as molecular phylogenetic analyses demonstrate that the Bauhiniinae might have originated in the Paleogene of low-latitudes along the eastern Tethys Seaway. They dispersed southwards into Africa, migrated from Eurasia to North America via the North Atlantic Land Bridge or floating islands during the Oligocene. Then the genus spread into South America probably via the Isthmus of Panama since the Miocene onward, and underwent regional extinctions in the Boreotropics of mid-high-latitudes during the Neogene climatic cooling. Hence, Bauhinia presently exhibits a pantropical intercontinental disjunct distribution.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-015-0540-9) contains supplementary material, which is available to authorized users.
PMCID: PMC4647482  PMID: 26572133
Bauhinia; Bauhiniinae; Bilobate leaves; Biogeography; Caesalpinioideae; Cercideae; Evolution; Fotan Group; Legumes; Leguminosae; Miocene; North Atlantic Land Bridge; Orchid trees; Pantropical intercontinental disjunct; South China; Tethys Seaway
2.  Spider crabs of the Western Atlantic with special reference to fossil and some modern Mithracidae 
PeerJ  2015;3:e1301.
Spider crabs (Majoidea) are well-known from modern oceans and are also common in the western part of the Atlantic Ocean. When spider crabs appeared in the Western Atlantic in deep time, and when they became diverse, hinges on their fossil record. By reviewing their fossil record, we show that (1) spider crabs first appeared in the Western Atlantic in the Late Cretaceous, (2) they became common since the Miocene, and (3) most species and genera are found in the Caribbean region from the Miocene onwards. Furthermore, taxonomic work on some modern and fossil Mithracidae, a family that might have originated in the Western Atlantic, was conducted. Specifically, Maguimithrax gen. nov. is erected to accommodate the extant species Damithrax spinosissimus, while Damithrax cf. pleuracanthus is recognized for the first time from the fossil record (late Pliocene–early Pleistocene, Florida, USA). Furthermore, two new species are described from the lower Miocene coral-associated limestones of Jamaica (Mithrax arawakum sp. nov. and Nemausa windsorae sp. nov.). Spurred by a recent revision of the subfamily, two known species from the same deposits are refigured and transferred to new genera: Mithrax donovani to Nemausa, and Mithrax unguis to Damithrax. The diverse assemblage of decapods from these coral-associated limestones underlines the importance of reefs for the abundance and diversity of decapods in deep time. Finally, we quantitatively show that these crabs possess allometric growth in that length/width ratios drop as specimens grow, a factor that is not always taken into account while describing and comparing among taxa.
PMCID: PMC4636416  PMID: 26557432
Biodiversity; Paleontology; Decapoda; Crustacea; Biogeography; Taxonomy; Majoidea; Systematics; Paleoecology; Reef
3.  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
4.  Parascolymia (Scleractinia: Lobophylliidae) in the Central Paratethys Sea (Vienna Basin, Austria) and its possible biogeographic implications 
PLoS ONE  2015;10(7):e0132243.
Palaeobiogeographical and palaeodiversity patterns of scleractinian reef corals are generally biased due to uncertain taxonomy and a loss of taxonomic characters through dissolution and recrystallization of the skeletal aragonite in shallow marine limestones. Herein, we describe a fossil lobophylliid coral in mouldic preservation from the early middle Miocene Leitha Limestone of the Central Paratethys Sea (Vienna Basin, Austria). By using grey-scale image inversion and silicone rubber casts for the visualization of the original skeletal anatomy and the detection of distinct micromorphological characters (i.e. shape of septal teeth, granulation of septocostae) Parascolymia bracherti has been identified as a new species in spite of the dissolved skeleton. In the recent era, Parascolymia like all Lobophylliidae is restricted to the Indo-Pacific region, where it is represented by a single species. The new species proves the genus also in the Miocene Mediterranean reef coral province. A review of the spatio-temporal relationships of fossil corals related to Parascolymia indicates that the genus was probably rooted in the Eastern Atlantic‒Western Tethys region during the Paleocene to Eocene and reached the Indo-Pacific region not before the Oligocene. The revealed palaeobiogeographical pattern shows an obvious congruence with that of Acropora and tridacnine bivalves reflecting a gradual equatorwards retreat of the marine biodiversity center parallel to the Cenozoic climate deterioration.
PMCID: PMC4511765  PMID: 26201071
5.  Isthminia panamensis, a new fossil inioid (Mammalia, Cetacea) from the Chagres Formation of Panama and the evolution of ‘river dolphins’ in the Americas 
PeerJ  2015;3:e1227.
In contrast to dominant mode of ecological transition in the evolution of marine mammals, different lineages of toothed whales (Odontoceti) have repeatedly invaded freshwater ecosystems during the Cenozoic era. The so-called ‘river dolphins’ are now recognized as independent lineages that converged on similar morphological specializations (e.g., longirostry). In South America, the two endemic ‘river dolphin’ lineages form a clade (Inioidea), with closely related fossil inioids from marine rock units in the South Pacific and North Atlantic oceans. Here we describe a new genus and species of fossil inioid, Isthminia panamensis, gen. et sp. nov. from the late Miocene of Panama. The type and only known specimen consists of a partial skull, mandibles, isolated teeth, a right scapula, and carpal elements recovered from the Piña Facies of the Chagres Formation, along the Caribbean coast of Panama. Sedimentological and associated fauna from the Piña Facies point to fully marine conditions with high planktonic productivity about 6.1–5.8 million years ago (Messinian), pre-dating the final closure of the Isthmus of Panama. Along with ecomorphological data, we propose that Isthminia was primarily a marine inhabitant, similar to modern oceanic delphinoids. Phylogenetic analysis of fossil and living inioids, including new codings for Ischyrorhynchus, an enigmatic taxon from the late Miocene of Argentina, places Isthminia as the sister taxon to Inia, in a broader clade that includes Ischyrorhynchus and Meherrinia, a North American fossil inioid. This phylogenetic hypothesis complicates the possible scenarios for the freshwater invasion of the Amazon River system by stem relatives of Inia, but it remains consistent with a broader marine ancestry for Inioidea. Based on the fossil record of this group, along with Isthminia, we propose that a marine ancestor of Inia invaded Amazonia during late Miocene eustatic sea-level highs.
PMCID: PMC4562255  PMID: 26355720
River dolphins; Cetacea; Panama; Fossil record; Evolution; Neogene; Inioidea; Amazonia
6.  Cenozoic Methane-Seep Faunas of the Caribbean Region 
PLoS ONE  2015;10(10):e0140788.
We report new examples of Cenozoic cold-seep communities from Colombia, Cuba, the Dominican Republic, Trinidad, and Venezuela, and attempt to improve the stratigraphic dating of Cenozoic Caribbean seep communities using strontium isotope stratigraphy. Two seep faunas are distinguished in Barbados: the late Eocene mudstone-hosted ‘Joes River fauna’ consists mainly of large lucinid bivalves and tall abyssochrysoid gastropods, and the early Miocene carbonate-hosted ‘Bath Cliffs fauna’ containing the vesicomyid Pleurophopsis, the mytilid Bathymodiolus and small gastropods. Two new Oligocene seep communities from the Sinú River basin in Colombia consist of lucinid bivalves including Elongatolucina, thyasirid and solemyid bivalves, and Pleurophopsis. A new early Miocene seep community from Cuba includes Pleurophopsis and the large lucinid Meganodontia. Strontium isotope stratigraphy suggests an Eocene age for the Cuban Elmira asphalt mine seep community, making it the oldest in the Caribbean region. A new basal Pliocene seep fauna from the Dominican Republic is characterized by the large lucinid Anodontia (Pegophysema). In Trinidad we distinguish two types of seep faunas: the mudstone-hosted Godineau River fauna consisting mainly of lucinid bivalves, and the limestone-hosted Freeman’s Bay fauna consisting chiefly of Pleurophopsis, Bathymodiolus, and small gastropods; they are all dated as late Miocene. Four new seep communities of Oligocene to Miocene age are reported from Venezuela. They consist mainly of large globular lucinid bivalves including Meganodontia, and moderately sized vesicomyid bivalves. After the late Miocene many large and typical ‘Cenozoic’ lucinid genera disappeared from the Caribbean seeps and are today known only from the central Indo-Pacific Ocean. We speculate that the increasingly oligotrophic conditions in the Caribbean Sea after the closure of the Isthmus of Panama in the Pliocene may have been unfavorable for such large lucinids because they are only facultative chemosymbiotic and need to derive a significant proportion of their nutrition from suspended organic matter.
PMCID: PMC4607474  PMID: 26468887
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.  Near-Stasis in the Long-Term Diversification of Mesozoic Tetrapods 
PLoS Biology  2016;14(1):e1002359.
How did evolution generate the extraordinary diversity of vertebrates on land? Zero species are known prior to ~380 million years ago, and more than 30,000 are present today. An expansionist model suggests this was achieved by large and unbounded increases, leading to substantially greater diversity in the present than at any time in the geological past. This model contrasts starkly with empirical support for constrained diversification in marine animals, suggesting different macroevolutionary processes on land and in the sea. We quantify patterns of vertebrate standing diversity on land during the Mesozoic–early Paleogene interval, applying sample-standardization to a global fossil dataset containing 27,260 occurrences of 4,898 non-marine tetrapod species. Our results show a highly stable pattern of Mesozoic tetrapod diversity at regional and local levels, underpinned by a weakly positive, but near-zero, long-term net diversification rate over 190 million years. Species diversity of non-flying terrestrial tetrapods less than doubled over this interval, despite the origins of exceptionally diverse extant groups within mammals, squamates, amphibians, and dinosaurs. Therefore, although speciose groups of modern tetrapods have Mesozoic origins, rates of Mesozoic diversification inferred from the fossil record are slow compared to those inferred from molecular phylogenies. If high speciation rates did occur in the Mesozoic, then they seem to have been balanced by extinctions among older clades. An apparent 4-fold expansion of species richness after the Cretaceous/Paleogene (K/Pg) boundary deserves further examination in light of potential taxonomic biases, but is consistent with the hypothesis that global environmental disturbances such as mass extinction events can rapidly adjust limits to diversity by restructuring ecosystems, and suggests that the gradualistic evolutionary diversification of tetrapods was punctuated by brief but dramatic episodes of radiation.
A large-scale examination of the fossil record reveals slow diversification rates in tetrapods across the 190-million-year Mesozoic era, followed by a possible rapid and abrupt 4-fold increase in species richness after the Cretaceous-Paleogene mass extinction event.
Author Summary
Vertebrates invaded the land more than 360 million years ago. Since then, they diversified to more than 30,000 tetrapod species today, including birds, mammals, squamates, and amphibians. The fossil record provides our best window onto diversification across such long spans of time, but is unevenly sampled. Previous studies counted observed families of fossil tetrapods and supported an expansionist model, entailing large and unbounded diversity increases through time. We applied methods that correct for differences in sampling through time and space to a comprehensive species-level database of Mesozoic to early Cenozoic fossil tetrapods. We find strong evidence that tetrapod diversity increased during the Mesozoic, but that the long-term net rate of diversification was low; species richness only doubled or tripled over 190 million years. This is enigmatic because today’s high biodiversity could not have been realised at such a slow rate. Diversification rates must have been much higher during other intervals, or rapid diversification might have been concentrated during brief episodes such as the earliest Cenozoic. Patterns of diversification on geological timescales and their relationships to hypothesised drivers such as ecological opportunity and environmental volatility must receive renewed scrutiny if we are to understand how land vertebrates and other animals attained the high biodiversity seen today.
PMCID: PMC4726655  PMID: 26807777
9.  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
10.  New Biogeographic insight into Bauhinia s.l. (Leguminosae): integration from fossil records and molecular analyses 
Given that most species that have ever existed on earth are extinct, it stands to reason that the evolutionary history can be better understood with fossil taxa. Bauhinia is a typical genus of pantropical intercontinental disjunction among the Asian, African, and American continents. Geographic distribution patterns are better recognized when fossil records and molecular sequences are combined in the analyses. Here, we describe a new macrofossil species of Bauhinia from the Upper Miocene Xiaolongtan Formation in Wenshan County, Southeast Yunnan, China, and elucidate the biogeographic significance through the analyses of molecules and fossils.
Morphometric analysis demonstrates that the leaf shapes of B. acuminata, B. championii, B. chalcophylla, B. purpurea, and B. podopetala closely resemble the leaf shapes of the new finding fossil. Phylogenetic relationships among the Bauhinia species were reconstructed using maximum parsimony and Bayesian inference, which inferred that species in Bauhinia species are well-resolved into three main groups. Divergence times were estimated by the Bayesian Markov chain Monte Carlo (MCMC) method under a relaxed clock, and inferred that the stem diversification time of Bauhinia was ca. 62.7 Ma. The Asian lineage first diverged at ca. 59.8 Ma, followed by divergence of the Africa lineage starting during the late Eocene, whereas that of the neotropical lineage starting during the middle Miocene.
Hypotheses relying on vicariance or continental history to explain pantropical disjunct distributions are dismissed because they require mostly Palaeogene and older tectonic events. We suggest that Bauhinia originated in the middle Paleocene in Laurasia, probably in Asia, implying a possible Tethys Seaway origin or an “Out of Tropical Asia”, and dispersal of legumes. Its present pantropical disjunction resulted from disruption of the boreotropical flora by climatic cooling after the Paleocene-Eocene Thermal Maximum (PETM). North Atlantic land bridges (NALB) seem the most plausible route for migration of Bauhinia from Asia to America; and additional aspects of the Bauhinia species distribution are explained by migration and long distance dispersal (LDD) from Eurasia to the African and American continents.
PMCID: PMC4360257  PMID: 25288346
Bauhinia; Pantropical intercontinental disjunction; Evolution; Biogeography; Paleocene-Eocene thermal maximum; Boreotropical flora; Long distance dispersal
11.  Speciation in the dark: diversification and biogeography of the deep‐sea gastropod genus Scaphander in the Atlantic Ocean 
Journal of Biogeography  2015;42(5):843-855.
The aim of this work was to improve understanding about the mode, geography and tempo of diversification in deep‐sea organisms, using a time‐calibrated molecular phylogeny of the heterobranch gastropod genus Scaphander.
Atlantic and Indo‐West Pacific (IWP) oceans.
Two mitochondrial gene markers (COI and 16S) and one nuclear ribosomal gene (28S) from six Atlantic species of Scaphander, and four IWP species were used to generate a multilocus phylogenetic hypothesis using uncorrelated relaxed‐clock Bayesian methods implemented in beast and calibrated with the first occurrence of Scaphander in the fossil record (58.7–55.8 Ma).
Two main clades were supported: clade A, with sister relationships between species and subclades from the Atlantic and IWP; and clade B, with two western Atlantic sister species. Our estimates indicate that the two earliest divergences in clade A occurred between the middle Eocene and late Miocene and the most recent speciation occurred within the middle Miocene to Pleistocene. The divergence between the two western Atlantic species in clade B was estimated at late Oligocene–Pliocene.
Main conclusions
The prevailing mode of speciation in Scaphander was allopatric, but one possible case of sympatric speciation was detected between two western Atlantic species. Sister relationships between IWP and Atlantic lineages suggest the occurrence both of vicariance events caused by the closure of the Tethyan Seaway and of dispersal between the two ocean basins, probably around South Africa during episodic disruptions of the deep‐sea regional current system caused by glacial–interglacial cycles. Cladogenetic estimates do not support comparatively older diversification of deep‐sea faunas, but corroborate the hypothesis of a pulse of diversification centred in the Oligocene and Miocene epochs. Amphi‐Atlantic species were found to occur at deeper depths (bathyal–abyssal) and we hypothesize that trans‐Atlantic connectivity is maintained by dispersal between neighbouring reproductive populations inhabiting the abyssal sea floor and by dispersal across the shelf and slope of Arctic and sub‐Arctic regions.
PMCID: PMC4964956  PMID: 27524853
Allopatric speciation; amphi‐Atlantic; Cephalaspidea; dispersal; diversification pulse; Heterobranchia; marine biogeography; Mollusca; Tethyan vicariance
12.  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
13.  Sawfishes and Other Elasmobranch Assemblages from the Mio-Pliocene of the South Caribbean (Urumaco Sequence, Northwestern Venezuela) 
PLoS ONE  2015;10(10):e0139230.
The Urumaco stratigraphic sequence, western Venezuela, preserves a variety of paleoenvironments that include terrestrial, riverine, lacustrine and marine facies. A wide range of fossil vertebrates associated with these facies supports the hypothesis of an estuary in that geographic area connected with a hydrographic system that flowed from western Amazonia up to the Proto-Caribbean Sea during the Miocene. Here the elasmobranch assemblages of the middle Miocene to middle Pliocene section of the Urumaco sequence (Socorro, Urumaco and Codore formations) are described. Based on new findings, we document at least 21 taxa of the Lamniformes, Carcharhiniformes, Myliobatiformes and Rajiformes, and describe a new carcharhiniform species (†Carcharhinus caquetius sp. nov.). Moreover, the Urumaco Formation has a high number of well-preserved fossil Pristis rostra, for which we provide a detailed taxonomic revision, and referral in the context of the global Miocene record of Pristis as well as extant species. Using the habitat preference of the living representatives, we hypothesize that the fossil chondrichthyan assemblages from the Urumaco sequence are evidence for marine shallow waters and estuarine habitats.
PMCID: PMC4619466  PMID: 26488163
14.  Into Tibet: An Early Pliocene Dispersal of Fossil Zokor (Rodentia: Spalacidae) from Mongolian Plateau to the Hinterland of Tibetan Plateau 
PLoS ONE  2015;10(12):e0144993.
This paper reports the fossil zokors (Myospalacinae) collected from the lower Pliocene (~4.4 Ma) of Zanda Basin, southwestern Tibet, which is the first record in the hinterland of Tibetan Plateau within the Himalayan Range. Materials include 29 isolated molars belonging to Prosiphneus eriksoni (Schlosser, 1924) by having characters including large size, highly fused roots, upper molars of orthomegodont type, m1 anterior cap small and centrally located, and first pair of m1 reentrants on opposing sides, high crowns, and high value of dentine tract parameters. Based on the cladistics analysis, all seven species of Prosiphneus and P. eriksoni of Zanda form a monophyletic clade. P. eriksoni from Zanda, on the other hand, is nearly the terminal taxon of this clade. The appearance of P. eriksoni in Zanda represents a significant dispersal in the early Pliocene from its center of origin in north China and Mongolian Plateau, possibly via the Hol Xil-Qiangtang hinterland in northern Tibet. The fast evolving zokors are highly adapted to open terrains at a time when regional climates had become increasingly drier in the desert zones north of Tibetan Plateau during the late Miocene to Pliocene. The occurrence of this zokor in Tibet thus suggests a rather open steppe environment. Based on fossils of large mammals, we have formulated an “out of Tibet” hypothesis that suggests earlier and more primitive large mammals from the Pliocene of Tibet giving rise to the Ice Age megafauna. However, fossil records for large mammals are still too poor to evaluate whether they have evolved from lineages endemic to the Tibetan Plateau or were immigrants from outside. The superior record of small mammals is in a better position to address this question. With relatively dense age intervals and numerous localities in much of northern Asia, fossil zokors provide the first example of an “into Tibet” scenario–earlier and more primitive taxa originated from outside of the Tibetan Plateau and the later the lineage became extinct in southwestern Tibet.
PMCID: PMC4678110  PMID: 26658457
15.  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
16.  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
17.  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
18.  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
19.  Trace fossil evidence of coral-inhabiting crabs (Cryptochiridae) and its implications for growth and paleobiogeography 
Scientific Reports  2016;6:23443.
Members of the Cryptochiridae are small, fragile, symbiotic crabs that live in domiciles in modern corals. Despite their worldwide occurrence with over 50 species known today, their fossil record is unknown. We provide the first unambiguous evidence of cryptochirids in the fossil record through their crescentic pits, typical for certain cryptochirids, in Western Atlantic fossil corals, while the Eocene genus Montemagrechirus is excluded from the Cryptochiridae and referred to Montemagrechiridae fam. nov. Nine Pleistocene corals with crescentic pits originate from Florida (USA), and single specimens with pits come from the late Pleistocene of Cuba and the late Pliocene of Florida, all of which are measured for growth analyses. These pits represent trace fossils named Galacticus duerri igen. nov., isp. nov. A study of modern cryptochirid domicile shape (crescentic pit, circular-oval pit, or a true gall) shows that species within crab genera tend to inhabit the same pit shape. Crescentic pits in corals occur not only in the Western Atlantic today, but also in the Indo-West Pacific and in the Eastern Pacific. Thus, examination of Cenozoic fossil coral collections from these regions should yield further examples of cryptochirid pits, which would help to constrain the antiquity of this cryptic crab family.
PMCID: PMC4806305  PMID: 27009806
20.  Glowing Seashells: Diversity of Fossilized Coloration Patterns on Coral Reef-Associated Cone Snail (Gastropoda: Conidae) Shells from the Neogene of the Dominican Republic 
PLoS ONE  2015;10(4):e0120924.
The biology of modern Conidae (cone snails)—which includes the hyperdiverse genus Conus—has been intensively studied, but the fossil record of the clade remains poorly understood, particularly within an evolutionary framework. Here, ultraviolet light is used to reveal and characterize the original shell coloration patterns of 28 species of cone snails from three Neogene coral reef-associated deposits from the Cibao Valley, northern Dominican Republic. These fossils come from the upper Miocene Cercado Fm. and lower Pliocene Gurabo Fm., and range in age from about 6.6-4.8 Ma. Comparison of the revealed coloration patterns with those of extant species allow the taxa to be assigned to three genera of cone snails (Profundiconus, Conasprella, and Conus) and at least nine subgenera. Thirteen members of these phylogenetically diverse reef faunas are described as new species. These include: Profundiconus? hennigi, Conasprella (Ximeniconus) ageri, Conus anningae, Conus lyelli, Conus (Atlanticonus?) franklinae, Conus (Stephanoconus) gouldi, Conus (Stephanoconus) bellacoensis, Conus (Ductoconus) cashi, Conus (Dauciconus) garrisoni, Conus (Dauciconus?) zambaensis, Conus (Spuriconus?) kaesleri, Conus (Spuriconus?) lombardii, and Conus (Lautoconus?) carlottae. Each of the three reef deposits contain a minimum of 14–16 cone snail species, levels of diversity that are similar to modern Indo-Pacific reef systems. Finally, most of the 28 species can be assigned to modern clades and thus have important implications for understanding the biogeographic and temporal histories of these clades in tropical America.
PMCID: PMC4382297  PMID: 25830769
21.  A New Late Miocene Odobenid (Mammalia: Carnivora) from Hokkaido, Japan Suggests Rapid Diversification of Basal Miocene Odobenids 
PLoS ONE  2015;10(8):e0131856.
The modern walrus, Odobenus rosmarus, is specialized and only extant member of the family Odobenidae. They were much more diversified in the past, and at least 16 genera and 20 species of fossil walruses have been known. Although their diversity increased in the late Miocene and Pliocene (around 8–2 Million years ago), older records are poorly known. A new genus and species of archaic odobenid, Archaeodobenus akamatsui, gen. et sp. nov. from the late Miocene (ca. 10.0–9.5 Ma) top of the Ichibangawa Formation, Hokkaido, northern Japan, suggests rapid diversification of basal Miocene walruses. Archaeodobenus akamatsui is the contemporaneous Pseudotaria muramotoi from the same formation, but they are distinguishable from each other in size and shape of the occipital condyle, foramen magnum and mastoid process of the cranium, and other postcranial features. Based on our phylogenetic analysis, A. akamatsui might have split from P. muramotoi at the late Miocene in the western North Pacific. This rapid diversification of the archaic odobenids occurred with a combination of marine regression and transgression, which provided geological isolation among the common ancestors of extinct odobenids.
PMCID: PMC4526471  PMID: 26244784
22.  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
23.  Scorched mussels (Brachidontes spp., Bivalvia: Mytilidae) from the tropical and warm‐temperate southwestern Atlantic: the role of the Amazon River in their speciation 
Ecology and Evolution  2016;10.1002/ece3.2016.
Antitropicality is a distribution pattern where closely related taxa are separated by an intertropical latitudinal gap. Two potential examples include Brachidontes darwinianus (south eastern Brazil to Uruguay), considered by some authors as a synonym of B. exustus (Gulf of Mexico and the Caribbean), and B. solisianus, distributed along the Brazilian coast with dubious records north of the intertropical zone. Using two nuclear (18S and 28S rDNA) and one mitochondrial gene (mtDNA COI), we aimed to elucidate the phylogeographic and phylogenetic relationships among the scorched mussels present in the warm‐temperate region of the southwest Atlantic. We evaluated a divergence process mediated by the tropical zone over alternative phylogeographic hypotheses. Brachidontes solisianus was closely related to B. exustus I, a species with which it exhibits an antitropical distribution. Their divergence time was approximately 2.6 Ma, consistent with the intensification of Amazon River flow. Brachidontes darwinianus, an estuarine species is shown here not to be related to this B. exustus complex. We suspect ancestral forms may have dispersed from the Caribbean to the Atlantic coast via the Trans‐Amazonian seaway (Miocene). The third species, B rodriguezii is presumed to have a long history in the region with related fossil forms going back to the Miocene. Although scorched mussels are very similar in appearance, their evolutionary histories are very different, involving major historical contingencies as the formation of the Amazon River, the Panama Isthmus, and the last marine transgression.
PMCID: PMC4758806  PMID: 26929816
Amazon River; mussels; southwestern Atlantic ocean; speciation
24.  Scorched mussels (Brachidontes spp., Bivalvia: Mytilidae) from the tropical and warm‐temperate southwestern Atlantic: the role of the Amazon River in their speciation 
Ecology and Evolution  2016;6(6):1778-1798.
Antitropicality is a distribution pattern where closely related taxa are separated by an intertropical latitudinal gap. Two potential examples include Brachidontes darwinianus (south eastern Brazil to Uruguay), considered by some authors as a synonym of B. exustus (Gulf of Mexico and the Caribbean), and B. solisianus, distributed along the Brazilian coast with dubious records north of the intertropical zone. Using two nuclear (18S and 28S rDNA) and one mitochondrial gene (mtDNA COI), we aimed to elucidate the phylogeographic and phylogenetic relationships among the scorched mussels present in the warm‐temperate region of the southwest Atlantic. We evaluated a divergence process mediated by the tropical zone over alternative phylogeographic hypotheses. Brachidontes solisianus was closely related to B. exustus I, a species with which it exhibits an antitropical distribution. Their divergence time was approximately 2.6 Ma, consistent with the intensification of Amazon River flow. Brachidontes darwinianus, an estuarine species is shown here not to be related to this B. exustus complex. We suspect ancestral forms may have dispersed from the Caribbean to the Atlantic coast via the Trans‐Amazonian seaway (Miocene). The third species, B rodriguezii is presumed to have a long history in the region with related fossil forms going back to the Miocene. Although scorched mussels are very similar in appearance, their evolutionary histories are very different, involving major historical contingencies as the formation of the Amazon River, the Panama Isthmus, and the last marine transgression.
PMCID: PMC4758806  PMID: 26929816
Amazon River; mussels; southwestern Atlantic ocean; speciation
25.  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

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