Charles R. Marshall

Has the Earth’s sixth mass extinction already arrived?

Palaeontologists characterize mass extinctions as times when the Earth loses more than three-quarters of its species in a geologically short interval, as has happened only five times in the past 540 million years or so. Biologists now suggest that a sixth mass extinction may be under way, given the known species losses over the past few centuries and millennia. Here we review how differences between fossil and modern data and the addition of recently available palaeontological information influence our understanding of the current extinction crisis. Our results confirm that current extinction rates are higher than would be expected from the fossil record, highlighting the need for effective conservation measures.

Approaching a state shift in Earth’s biosphere

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale ‘tipping point’ highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

Phanerozoic trends in the global diversity of marine invertebrates.

It has previously been thought that there was a steep Cretaceous and Cenozoic radiation of marine invertebrates. This pattern can be replicated with a new data set of fossil occurrences representing 3.5 million specimens, but only when older analytical protocols are used. Moreover, analyses that employ sampling standardization and more robust counting methods show a modest rise in diversity with no clear trend after the mid-Cretaceous. Globally, locally, and at both high and low latitudes, diversity was less than twice as high in the Neogene as in the mid-Paleozoic. The ratio of global to local richness has changed little, and a latitudinal diversity gradient was present in the early Paleozoic.

Effects of sampling standardization on estimates of Phanerozoic marine diversification.

Global diversity curves reflect more than just the number of taxa that have existed through time: they also mirror variation in the nature of the fossil record and the way the record is reported. These sampling effects are best quantified by assembling and analyzing large numbers of locality-specific biotic inventories. Here, we introduce a new database of this kind for the Phanerozoic fossil record of marine invertebrates. We apply four substantially distinct analytical methods that estimate taxonomic diversity by quantifying and correcting for variation through time in the number and nature of inventories. Variation introduced by the use of two dramatically different counting protocols also is explored. We present sampling-standardized diversity estimates for two long intervals that sum to 300 Myr (Middle Ordovician-Carboniferous; Late Jurassic-Paleogene). Our new curves differ considerably from traditional, synoptic curves. For example, some of them imply unexpectedly low late Cretaceous and early Tertiary diversity levels. However, such factors as the current emphasis in the database on North America and Europe still obscure our view of the global history of marine biodiversity. These limitations will be addressed as the database and methods are refined.

Confidence intervals on stratigraphic ranges

Observed stratigraphic ranges almost always underestimate true longevities. Strauss and Sadler (1987, 1989) provide a method for calculating confidence intervals on the endpoints of local stratigraphic ranges. Their method can also be applied to composite sections; confidence intervals may be placed on times of origin and extinction for entire species or lineages. Confidence interval sizes depend only on the length of the stratigraphic range and the number of fossil horizons. The techniques most important assumptions are that fossil horizons are distributed randomly and that collecting intensity has been uniform over the stratigraphic range. These assumptions are more difficult to test and less likely to be fulfilled for composite sections than for local sections. Confidence intervals give useful baseline estimates of the incompleteness of the fossil record, even if the underlying assumptions cannot be tested. Confidence intervals, which can be very large, should be calculated when the fossil record is used to assess absolute rates of molecular or morphological evolution, especially for poorly preserved groups. Confidence intervals have other functions: to determine how rich the fossil record has to be before radiometric dating errors become the dominant source of error in estimated times of origin or extinction; to predict future fossil finds; to predict which species with fossil records should be extant; and to assess phylogenetic hypotheses and taxonomic assignments.

Diversity dynamics: molecular phylogenies need the fossil record

Over the last two decades, new tools in the analysis of molecular phylogenies have enabled study of the diversification dynamics of living clades in the absence of information about extinct lineages. However, computer simulations and the fossil record show that the inability to access extinct lineages severely limits the inferences that can be drawn from molecular phylogenies. It appears that molecular phylogenies can tell us only when there have been changes in diversification rates, but are blind to the true diversity trajectories and rates of origination and extinction that have led to the species that are alive today. We need to embrace the fossil record if we want to fully understand the diversity dynamics of the living biota.

Using the fossil record to estimate the age of the last common ancestor of extant primates

Divergence times estimated from molecular data often considerably predate the earliest known fossil representatives of the groups studied. For the order Primates, molecular data calibrated with various external fossil dates uniformly suggest a mid-Cretaceous divergence from other placental mammals, some 90 million years (Myr) ago, whereas the oldest known fossil primates are from the basal Eocene epoch (54–55 Myr ago). The common ancestor of primates should be earlier than the oldest known fossils, but adequate quantification is needed to interpret possible discrepancies between molecular and palaeontological estimates. Here we present a new statistical method, based on an estimate of species preservation derived from a model of the diversification pattern, that suggests a Cretaceous last common ancestor of primates, approximately 81.5 Myr ago, close to the initial divergence time inferred from molecular data. It also suggests that no more than 7% of all primate species that have ever existed are known from fossils. The approach unites all the available palaeontological methods of timing evolutionary events: the fossil record, extant species and clade diversification models.

Recent Synchronous Radiation of a Living Fossil

Despite their ancient origin, the majority of extant cycad species radiated within the past 10 million years. Modern survivors of previously more diverse lineages are regarded as living fossils, particularly when characterized by morphological stasis. Cycads are often cited as a classic example, reaching their greatest diversity during the Jurassic–Cretaceous (199.6 to 65.5 million years ago) then dwindling to their present diversity of ~300 species as flowering plants rose to dominance. Using fossil-calibrated molecular phylogenies, we show that cycads underwent a near synchronous global rediversification beginning in the late Miocene, followed by a slowdown toward the Recent. Although the cycad lineage is ancient, our timetrees indicate that living cycad species are not much older than ~12 million years. These data reject the hypothesized role of dinosaurs in generating extant diversity and the designation of today’s cycad species as living fossils.

Dating the origin of the Orchidaceae from a fossil orchid with its pollinator

Since the time of Darwin, evolutionary biologists have been fascinated by the spectacular adaptations to insect pollination exhibited by orchids. However, despite being the most diverse plant family on Earth, the Orchidaceae lack a definitive fossil record and thus many aspects of their evolutionary history remain obscure. Here we report an exquisitely preserved orchid pollinarium (of Meliorchis caribea gen. et sp. nov.) attached to the mesoscutellum of an extinct stingless bee, Proplebeia dominicana, recovered from Miocene amber in the Dominican Republic, that is 15–20 million years (Myr) old. This discovery constitutes both the first unambiguous fossil of Orchidaceae and an unprecedented direct fossil observation of a plant–pollinator interaction. By applying cladistic methods to a morphological character matrix, we resolve the phylogenetic position of M. caribea within the extant subtribe Goodyerinae (subfamily Orchidoideae). We use the ages of other fossil monocots and M. caribea to calibrate a molecular phylogenetic tree of the Orchidaceae. Our results indicate that the most recent common ancestor of extant orchids lived in the Late Cretaceous (76–84 Myr ago), and also suggest that the dramatic radiation of orchids began shortly after the mass extinctions at the K/T boundary. These results further support the hypothesis of an ancient origin for Orchidaceae.

Confidence intervals on stratigraphic ranges with nonrandom distributions of fossil horizons

A generalized method for calculating confidence intervals on the position of the true end point of a stratigraphic range when the distributions of fossil horizons is nonrandom is presented. The method requires a quantitative measure of collecting and/or preservation biases with stratigraphic position. This fossil recovery potential function may be based on (among other variables) bedding-plane surface areas, or, given a water depth curve, an a priori estimate of the preservation potential with water depth. The approach assumes that the observed distribution of fossil horizons is consistent with the distribution predicted by the fossil recovery potential function, an assumption that must be tested before the method is applied. Unlike previous methods for calculating confidence intervals on the end points of stratigraphic ranges, this method may be applied when the number of fossil horizons is correlated with stratigraphic ranges, this method may be applied when the number of fossil horizons is correlated with stratigraphic position. The approach should only be applied to sections that have been sampled continuously, or approximately continuously. Its efficacy will depend on how accurately fossil recovery potentials can be determined. A method is also presented for estimating the probability that a species became extinct during a major hiatus in the rock record.