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1.  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
2.  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
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.  Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability 
The risk of global extinction of reef-building coral species is increasing. We evaluated extinction risk using a biological trait-based resiliency index that was compared with Caribbean extinction during the Plio-Pleistocene, and with extinction risk determined by the International Union for Conservation of Nature (IUCN). Through the Plio-Pleistocene, the Caribbean supported more diverse coral assemblages than today and shared considerable overlap with contemporary Indo-Pacific reefs. A clear association was found between extant Plio-Pleistocene coral genera and our positive resilience scores. Regional extinction in the past and vulnerability in the present suggests that Pocillopora, Stylophora and foliose Pavona are among the most susceptible taxa to local and regional isolation. These same taxa were among the most abundant corals in the Caribbean Pliocene. Therefore, a widespread distribution did not equate with immunity to regional extinction. The strong relationship between past and present vulnerability suggests that regional extinction events are trait-based and not merely random episodes. We found several inconsistencies between our data and the IUCN scores, which suggest a need to critically re-examine what constitutes coral vulnerability.
PMCID: PMC3350676  PMID: 22337694
biological trait; coral; extinction risk; Plio-Pleistocene; resilience; vulnerability
5.  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
6.  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
7.  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
8.  Population history, phylogeography, and conservation genetics of the last Neotropical mega-herbivore, the lowland tapir (Tapirus terrestris) 
Understanding the forces that shaped Neotropical diversity is central issue to explain tropical biodiversity and inform conservation action; yet few studies have examined large, widespread species. Lowland tapir (Tapirus terrrestris, Perissodactyla, Tapiridae) is the largest Neotropical herbivore whose ancestors arrived in South America during the Great American Biotic Interchange. A Pleistocene diversification is inferred for the genus Tapirus from the fossil record, but only two species survived the Pleistocene megafauna extinction. Here, we investigate the history of lowland tapir as revealed by variation at the mitochondrial gene Cytochrome b, compare it to the fossil data, and explore mechanisms that could have shaped the observed structure of current populations.
Separate methodological approaches found mutually exclusive divergence times for lowland tapir, either in the late or in the early Pleistocene, although a late Pleistocene divergence is more in tune with the fossil record. Bayesian analysis favored mountain tapir (T. pinchaque) paraphyly in relation to lowland tapir over reciprocal monophyly, corroborating the inferences from the fossil data these species are sister taxa. A coalescent-based analysis rejected a null hypothesis of allopatric divergence, suggesting a complex history. Based on the geographic distribution of haplotypes we propose (i) a central role for western Amazonia in tapir diversification, with a key role of the ecological gradient along the transition between Andean subcloud forests and Amazon lowland forest, and (ii) that the Amazon river acted as an barrier to gene flow. Finally, the branching patterns and estimates based on nucleotide diversity indicate a population expansion after the Last Glacial Maximum.
This study is the first examining lowland tapir phylogeography. Climatic events at the end of the Pleistocene, parapatric speciation, divergence along the Andean foothill, and role of the Amazon river, have similarly shaped the history of other taxa. Nevertheless further work with additional samples and loci is needed to improve our initial assessment. From a conservation perspective, we did not find a correspondence between genetic structure in lowland tapir and ecogeographic regions proposed to define conservation priorities in the Neotropics. This discrepancy sheds doubt into this scheme's ability to generate effective conservation planning for vagile species.
PMCID: PMC2949869  PMID: 20840756
9.  A New Horned Crocodile from the Plio-Pleistocene Hominid Sites at Olduvai Gorge, Tanzania 
PLoS ONE  2010;5(2):e9333.
The fossil record reveals surprising crocodile diversity in the Neogene of Africa, but relationships with their living relatives and the biogeographic origins of the modern African crocodylian fauna are poorly understood. A Plio-Pleistocene crocodile from Olduvai Gorge, Tanzania, represents a new extinct species and shows that high crocodylian diversity in Africa persisted after the Miocene. It had prominent triangular “horns” over the ears and a relatively deep snout, these resemble those of the recently extinct Malagasy crocodile Voay robustus, but the new species lacks features found among osteolaemines and shares derived similarities with living species of Crocodylus.
Methodology/Principal Findings
The holotype consists of a partial skull and skeleton and was collected on the surface between two tuffs dated to approximately 1.84 million years (Ma), in the same interval near the type localities for the hominids Homo habilis and Australopithecus boisei. It was compared with previously-collected material from Olduvai Gorge referable to the same species. Phylogenetic analysis places the new form within or adjacent to crown Crocodylus.
The new crocodile species was the largest predator encountered by our ancestors at Olduvai Gorge, as indicated by hominid specimens preserving crocodile bite marks from these sites. The new species also reinforces the emerging view of high crocodylian diversity throughout the Neogene, and it represents one of the few extinct species referable to crown genus Crocodylus.
PMCID: PMC2827537  PMID: 20195356
10.  Diversification of Neoaves: integration of molecular sequence data and fossils 
Biology Letters  2006;2(4):543-547.
Patterns of diversification and timing of evolution within Neoaves, which includes almost 95% of all bird species, are virtually unknown. On the other hand, molecular data consistently indicate a Cretaceous origin of many neoavian lineages and the fossil record seems to support an Early Tertiary diversification. Here, we present the first well-resolved molecular phylogeny for Neoaves, together with divergence time estimates calibrated with a large number of stratigraphically and phylogenetically well-documented fossils. Our study defines several well-supported clades within Neoaves. The calibration results suggest that Neoaves, after an initial split from Galloanseres in Mid-Cretaceous, diversified around or soon after the K/T boundary. Our results thus do not contradict palaeontological data and show that there is no solid molecular evidence for an extensive pre-Tertiary radiation of Neoaves.
PMCID: PMC1834003  PMID: 17148284
Neoaves; phylogeny; nuclear DNA; fossils; molecular clock; divergence times
11.  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
12.  Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction 
The spiny-finned teleost fishes (Acanthomorpha) include nearly one-third of all living vertebrate species and assume a bewildering array of bodyplans, but the macroevolutionary assembly of modern acanthomorph biodiversity remains largely unexplored. Here, I reconstruct the trajectory of morphological diversification in this major radiation from its first appearance in the Late Cretaceous to the Miocene using a geometric morphometric database comprising more than 600 extinct species known from complete body fossils. The anatomical diversity (disparity) of acanthomorphs is low throughout the Cretaceous, increases sharply and significantly in the wake of the Cretaceous–Palaeogene (K–P) extinction, and shows little change throughout subsequent Cenozoic intervals. This pattern of morphological diversification appears robust to two potential biasing factors: the ‘Lagerstätten effect’, and the non-random segregation of rare and common taxa along phenotypic axes. Dissecting the trajectory of acanthomorph radiation along phylogenetic lines reveals that the abrupt post-extinction increase in disparity is driven largely by the proliferation of trophically diverse modern groups within Percomorpha, a spiny-fin subclade containing more than 15 000 living species and identified as showing a substantially elevated diversification rate relative to background vertebrate levels. A major component of the Palaeogene acanthomorph radiation reflects colonization of morphospace previously occupied by non-acanthomorph victims of the K–P. However, other aspects of morphological diversification cannot be explained by this simple ecological release model, suggesting that multiple factors contributed to the prolific anatomical radiation of acanthomorphs.
PMCID: PMC2871855  PMID: 20133356
Acanthomorpha; adaptive radiation; biodiversity; ecological release; morphometrics; Teleostei
13.  A comparison between coral colonies of the genus Madracis and simulated forms 
In addition to experimental studies, computational models provide valuable information about colony development in scleractinian corals. Using our simulation model, we show how environmental factors such as nutrient distribution and light availability affect growth patterns of coral colonies. To compare the simulated coral growth forms with those of real coral colonies, we quantitatively compared our modelling results with coral colonies of the morphologically variable Caribbean coral genus Madracis. Madracis species encompass a relatively large morphological variation in colony morphology and hence represent a suitable genus to compare, for the first time, simulated and real coral growth forms in three dimensions using a quantitative approach. This quantitative analysis of three-dimensional growth forms is based on a number of morphometric parameters (such as branch thickness, branch spacing, etc.). Our results show that simulated coral morphologies share several morphological features with real coral colonies (M. mirabilis, M. decactis, M. formosa and M. carmabi). A significant correlation was found between branch thickness and branch spacing for both real and simulated growth forms. Our present model is able to partly capture the morphological variation in closely related and morphologically variable coral species of the genus Madracis.
PMCID: PMC2982250  PMID: 20573621
corals; morphogenesis; morphology; simulation; CT scan; Madracis
14.  Long Distance Dispersal and Connectivity in Amphi-Atlantic Corals at Regional and Basin Scales 
PLoS ONE  2011;6(7):e22298.
Among Atlantic scleractinian corals, species diversity is highest in the Caribbean, but low diversity and high endemism are observed in various peripheral populations in central and eastern Atlantic islands and along the coasts of Brazil and West Africa. The degree of connectivity between these distantly separated populations is of interest because it provides insight into processes at both evolutionary and ecological time scales, such as speciation, recruitment dynamics and the persistence of coral populations. To assess connectivity in broadly distributed coral species of the Atlantic, DNA sequence data from two nuclear markers were obtained for six coral species spanning their distributional ranges. At basin-wide scales, significant differentiation was generally observed among populations in the Caribbean, Brazil and West Africa. Concordance of patterns in connectivity among co-distributed taxa indicates that extrinsic barriers, such as the Amazon freshwater plume or long stretches of open ocean, restrict dispersal of coral larvae from region to region. Within regions, dispersal ability appears to be influenced by aspects of reproduction and life history. Two broadcasting species, Siderastrea siderea and Montastraea cavernosa, were able to maintain gene flow among populations separated by as much as 1,200 km along the coast of Brazil. In contrast, brooding species, such as Favia gravida and Siderastrea radians, had more restricted gene flow along the Brazilian coast.
PMCID: PMC3142122  PMID: 21799816
15.  Macroevolutionary Dynamics and Historical Biogeography of Primate Diversification Inferred from a Species Supermatrix 
PLoS ONE  2012;7(11):e49521.
Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
PMCID: PMC3500307  PMID: 23166696
16.  A sphenodontine (Rhynchocephalia) from the Miocene of New Zealand and palaeobiogeography of the tuatara (Sphenodon) 
Jaws and dentition closely resembling those of the extant tuatara (Sphenodon) are described from the Manuherikia Group (Early Miocene; 19–16 million years ago, Mya) of Central Otago, New Zealand. This material is significant in bridging a gap of nearly 70 million years in the rhynchocephalian fossil record between the Late Pleistocene of New Zealand and the Late Cretaceous of Argentina. It provides the first pre-Pleistocene record of Rhynchocephalia in New Zealand, a finding consistent with the view that the ancestors of Sphenodon have been on the landmass since it separated from the rest of Gondwana 82–60 Mya. However, if New Zealand was completely submerged near the Oligo-Miocene boundary (25–22 Mya), as recently suggested, an ancestral sphenodontine would need to have colonized the re-emergent landmass via ocean rafting from a currently unrecorded and now extinct Miocene population. Although an Early Miocene record does not preclude that possibility, it substantially reduces the temporal window of opportunity. Irrespective of pre-Miocene biogeographic history, this material also provides the first direct evidence that the ancestors of the tuatara, an animal often perceived as unsophisticated, survived in New Zealand despite substantial local climatic and environmental changes.
PMCID: PMC2660973  PMID: 19203920
biogeography; fossil; Gondwana; Miocene; Rhynchocephalia; Sphenodontinae
17.  The avian fossil record in Insular Southeast Asia and its implications for avian biogeography and palaeoecology 
PeerJ  2014;2:e295.
Excavations and studies of existing collections during the last decades have significantly increased the abundance as well as the diversity of the avian fossil record for Insular Southeast Asia. The avian fossil record covers the Eocene through the Holocene, with the majority of bird fossils Pleistocene in age. Fossil bird skeletal remains represent at least 63 species in 54 genera and 27 families, and two ichnospecies are represented by fossil footprints. Birds of prey, owls and swiftlets are common elements. Extinctions seem to have been few, suggesting continuity of avian lineages since at least the Late Pleistocene, although some shifts in species ranges have occurred in response to climatic change. Similarities between the Late Pleistocene avifaunas of Flores and Java suggest a dispersal route across southern Sundaland. Late Pleistocene assemblages of Niah Cave (Borneo) and Liang Bua (Flores) support the rainforest refugium hypothesis in Southeast Asia as they indicate the persistence of forest cover, at least locally, throughout the Late Pleistocene and Holocene.
PMCID: PMC3961167
Insular Southeast Asia; Dispersal; Wallacea; Extinction; Paleontology; Fossil birds; Avian biogeography
18.  Light gradients and optical microniches in coral tissues 
Light quantity and quality are among the most important factors determining the physiology and stress response of zooxanthellate corals. Yet, almost nothing is known about the light field that Symbiodinium experiences within their coral host, and the basic optical properties of coral tissue are unknown. We used scalar irradiance microprobes to characterize vertical and lateral light gradients within and across tissues of several coral species. Our results revealed the presence of steep light gradients with photosynthetically available radiation decreasing by about one order of magnitude from the tissue surface to the coral skeleton. Surface scalar irradiance was consistently higher over polyp tissue than over coenosarc tissue in faviid corals. Coral bleaching increased surface scalar irradiance by ~150% (between 500 and 700 nm) relative to a healthy coral. Photosynthesis peaked around 300 μm within the tissue, which corresponded to a zone exhibiting strongest depletion of scalar irradiance. Deeper coral tissue layers, e.g., ~1000 μm into aboral polyp tissues, harbor optical microniches, where only ~10% of the incident irradiance remains. We conclude that the optical microenvironment of corals exhibits strong lateral and vertical gradients of scalar irradiance, which are affected by both tissue and skeleton optical properties. Our results imply that zooxanthellae populations inhabit a strongly heterogeneous light environment and highlight the presence of different optical microniches in corals; an important finding for understanding the photobiology, stress response, as well as the phenotypic and genotypic plasticity of coral symbionts.
PMCID: PMC3427877  PMID: 22969755
coral photobiology; bio-optics; microenvironment; tissue optics; zooxanthellae; microsensor; microgradients; ecophysiology
19.  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
20.  Cyanobacteria Associated with Coral Black Band Disease in Caribbean and Indo-Pacific Reefs 
For 30 years it has been assumed that a single species of cyanobacteria, Phormidium corallyticum, is the volumetrically dominant component of all cases of black band disease (BBD) in coral. Cyanobacterium-specific 16S rRNA gene primers and terminal restriction fragment length polymorphism analyses were used to determine the phylogenetic diversity of these BBD cyanobacteria on coral reefs in the Caribbean and Indo-Pacific Seas. These analyses indicate that the cyanobacteria that inhabit BBD bacterial mats collected from the Caribbean and Indo-Pacific Seas belong to at least three different taxa, despite the fact that the corals in each case exhibit similar signs and patterns of BBD mat development.
PMCID: PMC154794  PMID: 12676731
21.  Miocene honey bees from the Randeck Maar of southwestern Germany (Hymenoptera, Apidae) 
ZooKeys  2011;11-37.
The Miocene Randeck Maar (southwestern Germany) is one of the only sites with abundant material of fossil honey bees. The fauna has been the focus of much scrutiny by early authors who recognized multiple species or subspecies within the fauna. The history of work on the Randeck Maar is briefly reviewed and these fossils placed into context with other Tertiary and living species of the genus Apis Linnaeus (Apinae: Apini). Previously unrecorded specimens from Randeck Maar were compared with earlier series in an attempt to evaluate the observed variation. A morphometric analysis of forewing venation angles across representative Recent and Tertiary species of Apis as well as various non-Apini controls was undertaken to evaluate the distribution of variation in fossil honey bees. The resulting dendrogram shows considerable variation concerning the wing venation of Miocene Apini, but intergradation of other morphological characters reveals no clear pattern of separate species. This suggests that a single, highly variable species was present in Europe during the Miocene. The pattern also supports the notion that the multiple species and subspecies proposed by earlier authors for the Randeck Maar honey bee fauna are not valid, and all are accordingly recognized as Apis armbrusteri Zeuner.
PMCID: PMC3095134  PMID: 21594072
Apoidea; Anthophila; Apinae; Apis; honey bees; taxonomy; Tertiary; morphometrics
22.  Evidence of constant diversification punctuated by a mass extinction in the African cycads 
Ecology and Evolution  2013;4(1):50-58.
The recent evidence that extant cycads are not living fossils triggered a renewed search for a better understanding of their evolutionary history. In this study, we investigated the evolutionary diversification history of the genus Encephalartos, a monophyletic cycad endemic to Africa. We found an antisigmoidal pattern with a plateau and punctual explosive radiation. This pattern is typical of a constant radiation with mass extinction. The rate shift that we found may therefore be a result of a rapid recolonization of niches that have been emptied owing to mass extinction. Because the explosive radiation occurred during the transition Pliocene–Pleistocene, we argued that the processes might have been climatically mediated.
PMCID: PMC3894887  PMID: 24455160
Climate change; Encephalartos; extinction; gymnosperms; adaptive radiation; subtropical Africa.
23.  Radiation of Extant Cetaceans Driven by Restructuring of the Oceans 
Systematic Biology  2009;58(6):573-585.
The remarkable fossil record of whales and dolphins (Cetacea) has made them an exemplar of macroevolution. Although their overall adaptive transition from terrestrial to fully aquatic organisms is well known, this is not true for the radiation of modern whales. Here, we explore the diversification of extant cetaceans by constructing a robust molecular phylogeny that includes 87 of 89 extant species. The phylogeny and divergence times are derived from nuclear and mitochondrial markers, calibrated with fossils. We find that the toothed whales are monophyletic, suggesting that echolocation evolved only once early in that lineage some 36–34 Ma. The rorqual family (Balaenopteridae) is restored with the exclusion of the gray whale, suggesting that gulp feeding evolved 18–16 Ma. Delphinida, comprising all living dolphins and porpoises other than the Ganges/Indus dolphins, originated about 26 Ma; it contains the taxonomically rich delphinids, which began diversifying less than 11 Ma. We tested 2 hypothesized drivers of the extant cetacean radiation by assessing the tempo of lineage accumulation through time. We find no support for a rapid burst of speciation early in the history of extant whales, contrasting with expectations of an adaptive radiation model. However, we do find support for increased diversification rates during periods of pronounced physical restructuring of the oceans. The results imply that paleogeographic and paleoceanographic changes, such as closure of major seaways, have influenced the dynamics of radiation in extant cetaceans.
PMCID: PMC2777972  PMID: 20525610
Cetacea; evolution; molecular phylogeny; palaeo-ocean restructuring; speciation
24.  Marine Biodiversity in the Caribbean: Regional Estimates and Distribution Patterns 
PLoS ONE  2010;5(8):e11916.
This paper provides an analysis of the distribution patterns of marine biodiversity and summarizes the major activities of the Census of Marine Life program in the Caribbean region. The coastal Caribbean region is a large marine ecosystem (LME) characterized by coral reefs, mangroves, and seagrasses, but including other environments, such as sandy beaches and rocky shores. These tropical ecosystems incorporate a high diversity of associated flora and fauna, and the nations that border the Caribbean collectively encompass a major global marine biodiversity hot spot. We analyze the state of knowledge of marine biodiversity based on the geographic distribution of georeferenced species records and regional taxonomic lists. A total of 12,046 marine species are reported in this paper for the Caribbean region. These include representatives from 31 animal phyla, two plant phyla, one group of Chromista, and three groups of Protoctista. Sampling effort has been greatest in shallow, nearshore waters, where there is relatively good coverage of species records; offshore and deep environments have been less studied. Additionally, we found that the currently accepted classification of marine ecoregions of the Caribbean did not apply for the benthic distributions of five relatively well known taxonomic groups. Coastal species richness tends to concentrate along the Antillean arc (Cuba to the southernmost Antilles) and the northern coast of South America (Venezuela – Colombia), while no pattern can be observed in the deep sea with the available data. Several factors make it impossible to determine the extent to which these distribution patterns accurately reflect the true situation for marine biodiversity in general: (1) highly localized concentrations of collecting effort and a lack of collecting in many areas and ecosystems, (2) high variability among collecting methods, (3) limited taxonomic expertise for many groups, and (4) differing levels of activity in the study of different taxa.
PMCID: PMC2914069  PMID: 20689856
25.  On the origin of the Synodontis catfish species flock from Lake Tanganyika 
Biology Letters  2006;2(4):548-552.
Species flocks within Great Lakes provide unique insights into the factors affecting diversification. Lake Tanganyika (LT) is of particular interest because it contains many endemic groups for which general factors affecting diversification can be discerned. Here, we present the first phylogenetic study of the LT Synodontis (Siluriformes, Mochokidae) species flock using mtDNA sequence data. Our data reveal some previously unrecognized species diversity and indicate that the LT species flock is not monophyletic, and that two closely related clades of endemics may have independently colonized LT. Other comparable small species flocks are characterized by a single colonization event. Molecular date estimates of the timing of the initial within-lake diversification of the LT endemics, based on a fossil calibration, are comparable to those reported for other groups, suggesting that extrinsic factors maybe important common causes of clade diversification. The basal divergence in the sampled Synodontis reveals an East–West African faunal split seen in many terrestrial, but few aquatic groups, the timing of which coincides with East African rifting events.
PMCID: PMC1833983  PMID: 17148285
speciation; ancient lakes; diversification; molecular clock; cichlids

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