Marine planktonic microbes survived climatic instabilities in the past

In the geological past, changes in climate and tectonic activity are thought to have spurred the tempo of evolutionary change among major taxonomic groups of plants and animals. However, the extent to which these historical contingencies increased the risk of extinction of microbial plankton species remains largely unknown. Here, I analyse fossil records of marine planktonic diatoms and calcareous nannoplankton over the past 65 million years from the world oceans and show that the probability of species' extinction is not correlated with secular changes in climatic instability. Further supporting these results, analyses of genera survivorship curves based on fossil data concurred with the predictions of a birth-death model that simulates the extinction of genera through time assuming stochastically constant rates of speciation and extinction. However, my results also show that these marine microbes responded to exceptional climatic contingencies in a manner that appears to have promoted net diversification. These results highlight the ability of marine planktonic microbes to survive climatic instabilities in the geological past, and point to different mechanisms underlying the processes of speciation and extinction in these micro-organisms.     

Plant hemoglobins: a molecular fossil record for the evolution of oxygen transport

The evolution of oxygen transport hemoglobins occurred on at least two independent occasions. The earliest event led to myoglobin and red blood cell hemoglobin in animals. In plants, oxygen transport "leghemoglobins" evolved much more recently. In both events, pentacoordinate heme sites capable of inert oxygen transfer evolved from hexacoordinate hemoglobins that have unrelated functions. High sequence homology between hexacoordinate and pentacoordinate hemoglobins in plants has poised them for potential structural analysis leading to a molecular understanding of this important evolutionary event. However, the lack of a plant hexacoordinate hemoglobin structure in the exogenously ligand-bound form has prevented such comparison. Here we report the crystal structure of the cyanide-bound hexacoordinate hemoglobin from barley. This presents the first opportunity to examine conformational changes in plant hexacoordinate hemoglobins upon exogenous ligand binding, and reveals structural mechanisms for stabilizing the high-energy pentacoordinate heme conformation critical to the evolution of reversible oxygen binding hemoglobins.     

Persistence of high diversity in non-equilibrium ecological communities: implications for modern and fossil ecosystems

Explaining the origin and maintenance of biodiversity is critical for understanding the potential consequences of present-day environmental change on ecological communities, as well as the evolutionary history of ecosystems in the Earth's past. Much effort in theoretical ecology has focused on identifying mechanisms that promote stable coexistence of species at equilibrium. However, in a consumer-resource model of competition along an environmental gradient, high-diversity assemblages have the potential to persist in non-equilibrium states for millions of generations with very little species loss. Species' populations in such competitively accommodated communities show slow drift; if disrupted, they rapidly reorganize into alternative persistent states. Fossil examples of prolonged ecological stability lasting 1-5 Myr punctuated by rapid reorganization (e.g. brachiopods from the Permian Reef of west Texas) suggest that some palaeocommunities represent a record of periodically disrupted transient states rather than stable equilibria. The similarity between the theoretical results reported here and palaeontological data suggests that the maintenance of high-diversity communities, both in the past and present, may reflect long-duration, non-equilibrium transient dynamics. If so, this has implications for the response of such communities to present-day environmental change, as well as for the evolution of lineages in such systems.     

Caught in the act: the first record of copulating fossil vertebrates

The behaviour of fossil organisms can typically be inferred only indirectly, but rare fossil finds can provide surprising insights. Here, we report from the Eocene Messel Pit Fossil Site between Darmstadt and Frankfurt, Germany numerous pairs of the fossil carettochelyid turtle Allaeochelys crassesculpta that represent for the first time among fossil vertebrates couples that perished during copulation. Females of this taxon can be distinguished from males by their relatively shorter tails and development of plastral kinesis. The preservation of mating pairs has important taphonomic implications for the Messel Pit Fossil Site, as it is unlikely that the turtles would mate in poisonous surface waters. Instead, the turtles initiated copulation in habitable surface waters, but perished when their skin absorbed poisons while sinking into toxic layers. The mating pairs from Messel are therefore more consistent with a stratified, volcanic maar lake with inhabitable surface waters and a deadly abyss.     

Symbiosis catalyses niche expansion and diversification

Interactions between species are important catalysts of the evolutionary processes that generate the remarkable diversity of life. Symbioses, conspicuous and inherently interesting forms of species interaction, are pervasive throughout the tree of life. However, nearly all studies of the impact of species interactions on diversification have concentrated on competition and predation leaving unclear the importance of symbiotic interaction. Here, I show that, as predicted by evolutionary theories of symbiosis and diversification, multiple origins of a key innovation, symbiosis between gall-inducing insects and fungi, catalysed both expansion in resource use (niche expansion) and diversification. Symbiotic lineages have undergone a more than sevenfold expansion in the range of host-plant taxa they use relative to lineages without such fungal symbionts, as defined by the genetic distance between host plants. Furthermore, symbiotic gall-inducing insects are more than 17 times as diverse as their non-symbiotic relatives. These results demonstrate that the evolution of symbiotic interaction leads to niche expansion, which in turn catalyses diversification.     

The fossil record and estimating divergence times between lineages: Maximum divergene times and the importance of reliable phylogenies

Summary Bounded estimates on divergence times between lineaes are crucial to the calculation of absolute rates of molecular evolution. Upper (minimum) bounds on divergence times are easily estimated based on earliest fossil finds. Lower (maximum) bounds are more difficult to estimate; the age of putative ancestors may be used, though in practice it is virtually impossible to distinguish ancestors from primitive sister groups, which do not, of logical necessit, consitute lower bounds on divergence times. Two relatively new approaches to estimating lower bounds directly assess the incompleteness of the fossil record. The first uses taphonomic control groups to distinguish real absences from nonpreservation, while the second, and probably more powerful, uses the quality of the fossil recored to estimate confidence intervals on the bases of stratigraphic ranges. For some groups, especially vertebrates, the inclusion or exclusion of problematic fossils can dramaticaly affect estimated lower bounds on divergence times, often swamping the uncertainties due to the incompleteness of the fossil record and/or corelation and dating errors. When datable paleogeographic events reflect ancient divisions of faunas, a lower bound on the divergence time of speices within a fauna can be established based on the geologic, rather than fossil, record. The fossil records of hominids, eutherianmammals, echinoids, and geese are used as examples.This article was presented at the C.S.E.O.L. Conferrence on DNA-DNA Hybridization and Evolution, Lake Arrowhead, California, May 11–14, 1989     

Review of the monotreme fossil record and comparison of palaeontological and molecular data

Monotremes have traditionally been considered a remnant group of mammals descended from archaic Mesozoic stock, surviving to the present day on the relatively isolated Australian continent. Challenges to this orthodoxy have been spurred by discoveries of 'advanced' Cretaceous monotremes (Steropodon galmani, Archer, M., et al., 1985. First Mesozoic mammal from Australia-an Early Cretaceous monotreme, Nature. 318, 363-366) as well as by results from molecular data linking monotremes to therian mammals (specifically to marsupials in some studies). This paper reviews the monotreme fossil record and briefly discusses significant new information from additional Cretaceous Australian material. Mesozoic monotremes (including S. galmani) were a diverse group as evidenced by new material from the Early Cretaceous of New South Wales and Victoria currently under study. Although most of these new finds are edentulous jaws (limiting dental comparisons and determination of dietary niches), a range of sizes and forms has been determined. Some of these Cretaceous jaws exhibit archaic features-in particular evidence for the presence of a splenial bone in S. galmani-not seen in therian mammals or in post-Mesozoic (Tertiary and Quaternary) monotreme taxa. Tertiary monotremes were either archaic ornithorhynchids (toothed platypuses in the genera Monotrematum and Obdurodon) or tachyglossids (large echidnas in the genera Megalibgwilia and Zaglossus). Quaternary ornithorhynchid material is referable to the sole living platypus species Ornithorhynchus anatinus. Quaternary echidnas, however, were moderately diverse and several forms are known (Megalibgwilia species; 'Zaglossus' hacketti; Zaglossus species and Tachyglossus aculeatus).     

The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense "species complex" (Dinophyceae)

The cosmopolitan dinoflagellate genus Alexandrium, and especially the A. tamarense species complex, contain both toxic and nontoxic strains. An understanding of their evolution and paleogeography is a necessary precursor to unraveling the development and spread of toxic forms. The inclusion of more strains into the existing phylogenetic trees of the Alexandrium tamarense species complex from large subunit rDNA sequences has confirmed that geographic distribution is consistent with the molecular clades but not with the three morphologically defined species that constitute the complex. In addition, a new clade has been discovered, representing Mediterranean nontoxic strains. The dinoflagellates fossil record was used to calibrate a molecular clock: key dates used in this calibration are the origins of the Peridiniales (estimated at 190 MYA), Gonyaulacaceae (180 MYA), and Ceratiaceae (145 MYA). Based on the data set analyzed, the origin of the genus Alexandrium was estimated to be around late Cretaceous (77 MYA), with its earliest possible origination in the mid Cretaceous (119 MYA). The A. tamarense species complex potentially diverged around the early Neogene (23 MYA), with a possible first appearance in the late Paleogene (45 MYA). A paleobiogeographic scenario for Alexandrium is based on (1) the calculated possible ages of origination for the genus and its constituent groups; (2) paleogeographic events determined by plate movements, changing ocean configurations and currents, as well as climatic fluctuations; and (3) the present geographic distribution of the various clades of the Alexandrium tamarense species complex.     

How well can the exponential-growth coalescent approximate constant-rate birth–death population dynamics?

One of the central objectives in the field of phylodynamics is the quantification of population dynamic processes using genetic sequence data or in some cases phenotypic data. Phylodynamics has been successfully applied to many different processes, such as the spread of infectious diseases, within-host evolution of a pathogen, macroevolution and even language evolution. Phylodynamic analysis requires a probability distribution on phylogenetic trees spanned by the genetic data. Because such a probability distribution is not available for many common stochastic population dynamic processes, coalescent-based approximations assuming deterministic population size changes are widely employed. Key to many population dynamic models, in particular epidemiological models, is a period of exponential population growth during the initial phase. Here, we show that the coalescent does not well approximate stochastic exponential population growth, which is typically modelled by a birth–death process. We demonstrate that introducing demographic stochasticity into the population size function of the coalescent improves the approximation for values of R₀ close to 1, but substantial differences remain for large R₀. In addition, the computational advantage of using an approximation over exact models vanishes when introducing such demographic stochasticity. These results highlight that we need to increase efforts to develop phylodynamic tools that correctly account for the stochasticity of population dynamic models for inference.     

Myxomycete diversity and distribution from the fossil record to the present

The myxomycetes (plasmodial slime molds or myxogastrids) are a group of eukaryotic microorganisms usually present and sometimes abundant in terrestrial ecosystems. Evidence from molecular studies suggests that the myxomycetes have a significant evolutionary history. However, due to the fragile nature of the fruiting body, fossil records of the group are exceedingly rare. Although most myxomycetes are thought to have very large distributional ranges and many species appear to be cosmopolitan or nearly so, results from recent studies have provided evidence that spatial distribution patterns of these organisms can be successfully related to (1) differences in climate and/or vegetation on a global scale and (2) the ecological differences that exist for particular habitats on a local scale. A detailed examination of the global distribution of four examples (Barbeyella minutissima, Ceratiomyxa morchella, Leocarpus fragilis and Protophysarum phloiogenum) demonstrates that these species have recognizable distribution patterns in spite of the theoretical ability of their spores to bridge continents. Special Issue: Protist diversity and geographic distribution. Guest editor: W. Foissner.     

Using ghost lineages to identify diversification events in the fossil record

Observed rises in taxic diversity could reflect bias of the fossil record or a genuine diversification. Here we outline a new method that attempts to differentiate between these two possible explanations. The method is based on the calculations of average ghost lineage duration through successive intervals of time. Biases due to variation in preservational conditions affect taxa independently from their position in the tree of life. A genuine radiation event will affect some parts of the tree of life more than others. During periods of rapid diversification, there will be a high proportion of new taxa showing short ghost lineages and therefore the average ghost lineage duration will drop as diversity rises, allowing us to distinguish such events from preservational bias during which ghost lineage duration remains unchanged. We test the method on Aptian-Maastrichtian (Cretaceous) ray-finned fish diversity. The result shows that a peak of diversity in the Cenomanian is associated with a drop in average ghost lineage duration, indicating that a genuine biological radiation occurred at that time.     

Island phytophagy: explaining the remarkable diversity of plant-feeding insects

Plant-feeding insects have undergone unparalleled diversification among different plant taxa, yet explanations for variation in their diversity lack a quantitative, predictive framework. Island biogeographic theory has been applied to spatially discrete habitats but not to habitats, such as host plants, separated by genetic distance. We show that relationships between the diversity of gall-inducing flies and their host plants meet several fundamental predictions from island biogeographic theory. First, plant-taxon genetic distinctiveness, an integrator for long-term evolutionary history of plant lineages, is a significant predictor of variance in the diversity of gall-inducing flies among host-plant taxa. Second, range size and structural complexity also explain significant proportions of the variance in diversity of gall-inducing flies among different host-plant taxa. Third, as with other island systems, plant-lineage age does not predict species diversity. Island biogeographic theory, applied to habitats defined by genetic distance, provides a novel, comprehensive framework for analysing and explaining the diversity of plant-feeding insects and other host-specific taxa.     

Switching from a mechanistic model to a continuous model to study at different scales the effect of vine growth on the dynamic of a powdery mildew epidemic

Background and Aims

Epidemiological simulation models coupling plant growth with the dispersal and disease dynamics of an airborne plant pathogen were devised for a better understanding of host–pathogen dynamic interactions and of the capacity of grapevine development to modify the progress of powdery mildew epidemics.

Methods

The first model is a complex discrete mechanistic model (M-model) that explicitly incorporates the dynamics of host growth and the development and dispersion of the pathogen at the vine stock scale. The second model is a simpler ordinary differential equations (ODEs) compartmental SEIRT model (C-model) handling host growth (foliar surface) and the ontogenic resistance of the leaves. With the M-model various levels of vine development are simulated under three contrasting climatic scenarios and the relationship between host and disease variables are examined at key periods in the epidemic process. The ability of the C-model to retrieve the main dynamics of the disease for a range of vine growth given by the M-model is investigated.

Key Results

The M-model strengthens experimental results observed regarding the effect of the rate of leaf emergence and of the number of leaves at flowering on the severity of the disease. However, it also underlines strong variations of the dynamics of disease depending on the vigour and indirectly on the climatic scenarios. The C-model could be calibrated by using the M-model provided that different parameters before and after shoot topping and for various vigour levels and inoculation time are used. Biologically relevant estimations of the parameters that could be used for its extension to the vineyard scale are obtained.

Conclusions

The M-model is able to generate a wide range of growth scenarios with a strong impact on disease evolution. The C-model is a promising tool to be used at a larger scale.     

Behavioural changes and the adaptive diversification of pigeons and doves

What factors determine the extent of evolutionary diversification remains a major question in evolutionary biology. Behavioural changes have long been suggested to be a major driver of phenotypic diversification by exposing animals to new selective pressures. Nevertheless, the role of behaviour in evolution remains controversial because behavioural changes can also retard evolutionary change by hiding genetic variation from selection. In the present study, we apply recently implemented Ornstein–Uhlenbeck evolutionary models to show that behavioural changes led to associated evolutionary responses in functionally relevant morphological traits of pigeons and doves (Columbiformes). Specifically, changes from terrestrial to arboreal foraging behaviour reconstructed in a set of phylogenies brought associated shorter tarsi and longer tails, consistent with functional predictions. Interestingly, the transition to arboreality accelerated the rates of evolutionary divergence, leading to an increased morphological specialization that seems to have subsequently constrained reversals to terrestrial foraging. Altogether, our results support the view that behaviour may drive evolutionary diversification, but they also highlight that its evolutionary consequences largely depend on the limits imposed by the functional demands of the adaptive zone.     

First record of Neolindus Scheerpeltz from French Guiana (Coleoptera, Staphylinidae, Paederinae), with a key to males

The genus Neolindus Scheerpeltz, 1933, of the tribe Cylindroxystina Bierig, 1943, is recorded from French Guiana for the first time. Two new species, Neolindus irmlerisp. n. and Neolindus hermanisp. n., are described and illustrated. A key to males of Neolindus is provided.     

Statistical ecology comes of age

The desire to predict the consequences of global environmental change has been the driver towards more realistic models embracing the variability and uncertainties inherent in ecology. Statistical ecology has gelled over the past decade as a discipline that moves away from describing patterns towards modelling the ecological processes that generate these patterns. Following the fourth International Statistical Ecology Conference (1–4 July 2014) in Montpellier, France, we analyse current trends in statistical ecology. Important advances in the analysis of individual movement, and in the modelling of population dynamics and species distributions, are made possible by the increasing use of hierarchical and hidden process models. Exciting research perspectives include the development of methods to interpret citizen science data and of efficient, flexible computational algorithms for model fitting. Statistical ecology has come of age: it now provides a general and mathematically rigorous framework linking ecological theory and empirical data.     

Closing the gap between rocks and clocks using total-evidence dating

Total-evidence dating (TED) allows evolutionary biologists to incorporate a wide range of dating information into a unified statistical analysis. One might expect this to improve the agreement between rocks and clocks but this is not necessarily the case. We explore the reasons for such discordance using a mammalian dataset with rich molecular, morphological and fossil information. There is strong conflict in this dataset between morphology and molecules under standard stochastic models. This causes TED to push divergence events back in time when using inadequate models or vague priors, a phenomenon we term ‘deep root attraction’ (DRA). We identify several causes of DRA. Failure to account for diversified sampling results in dramatic DRA, but this can be addressed using existing techniques. Inadequate morphological models also appear to be a major contributor to DRA. The major reason seems to be that current models do not account for dependencies among morphological characters, causing distorted topology and branch length estimates. This is particularly problematic for huge morphological datasets, which may contain large numbers of correlated characters. Finally, diversification and fossil sampling priors that do not incorporate all the available background information can contribute to DRA, but these priors can also be used to compensate for DRA. Specifically, we show that DRA in the mammalian dataset can be addressed by introducing a modest extra penalty for ghost lineages that are unobserved in the fossil record, for instance by assuming rapid diversification, rare extinction or high fossil sampling rate; any of these assumptions produces highly congruent divergence time estimates with a minimal gap between rocks and clocks. Under these conditions, fossils have a stabilizing influence on divergence time estimates and significantly increase the precision of those estimates, which are generally close to the dates suggested by palaeontologists.This article is part of the themed issue ‘Dating species divergences using rocks and clocks’.