The complex effects of mass extinctions on morphological disparity

Studies of biodiversity through deep time have been a staple for biologists and paleontologists for over 60 years. Investigations of species richness (diversity) revealed that at least five mass extinctions punctuated the last half billion years, each seeing the rapid demise of a large proportion of contemporary taxa. In contrast to diversity, the response of morphological diversity (disparity) to mass extinctions is unclear. Generally, diversity and disparity are decoupled, such that diversity may decline as morphological disparity increases, and vice versa. Here, we develop simulations to model disparity changes across mass extinctions using continuous traits and birth-death trees. We find no simple null for disparity change following a mass extinction but do observe general patterns. The range of trait values decreases following either random or trait-selective mass extinctions, whereas variance and the density of morphospace occupation only decline following trait-selective events. General trends may differentiate random and trait-selective mass extinctions, but methods struggle to identify trait selectivity. Long-term effects of mass extinction trait selectivity change support for phylogenetic comparative methods away from the simulated Brownian motion toward Ornstein-Uhlenbeck and Early Burst models. We find that morphological change over mass extinction is best studied by quantifying multiple aspects of morphospace occupation.     

Reconstructing past species assemblages reveals the changing patterns and drivers of extinction through time

Predicting future species extinctions from patterns of past extinctions or current threat status relies on the assumption that the taxonomic and biological selectivity of extinction is consistent through time. If the driving forces of extinction change through time, this assumption may be unrealistic. Testing the consistency of extinction patterns between the past and the present has been difficult, because the phylogenetically explicit methods used to model present-day extinction risk typically cannot be applied to the data from the fossil record. However, the detailed historical and fossil records of the New Zealand avifauna provide a unique opportunity to reconstruct a complete, large faunal assemblage for different periods in the past. Using the first complete phylogeny of all known native New Zealand bird species, both extant and extinct, we show how the taxonomic and phylogenetic selectivity of extinction, and biological correlates of extinction, change from the pre-human period through Polynesian and European occupation, to the present. These changes can be explained both by changes in primary threatening processes, and by the operation of extinction filter effects. The variable patterns of extinction through time may confound attempts to identify risk factors that apply across time periods, and to infer future species declines from past extinction patterns and current threat status.     

Phylogenetic Clustering of Origination and Extinction across the Late Ordovician Mass Extinction

Mass extinctions can have dramatic effects on the trajectory of life, but in some cases the effects can be relatively small even when extinction rates are high. For example, the Late Ordovician mass extinction is the second most severe in terms of the proportion of genera eliminated, yet is noted for the lack of ecological consequences and shifts in clade dominance. By comparison, the end-Cretaceous mass extinction was less severe but eliminated several major clades while some rare surviving clades diversified in the Paleogene. This disconnect may be better understood by incorporating the phylogenetic relatedness of taxa into studies of mass extinctions, as the factors driving extinction and recovery are thought to be phylogenetically conserved and should therefore promote both origination and extinction of closely related taxa. Here, we test whether there was phylogenetic selectivity in extinction and origination using brachiopod genera from the Middle Ordovician through the Devonian. Using an index of taxonomic clustering (R_CL) as a proxy for phylogenetic clustering, we find that A) both extinctions and originations shift from taxonomically random or weakly clustered within families in the Ordovician to strongly clustered in the Silurian and Devonian, beginning with the recovery following the Late Ordovician mass extinction, and B) the Late Ordovician mass extinction was itself only weakly clustered. Both results stand in stark contrast to Cretaceous-Cenozoic bivalves, which showed significant levels of taxonomic clustering of extinctions in the Cretaceous, including strong clustering in the mass extinction, but taxonomically random extinctions in the Cenozoic. The contrasting patterns between the Late Ordovician and end-Cretaceous events suggest a complex relationship between the phylogenetic selectivity of mass extinctions and the long-term phylogenetic signal in origination and extinction patterns.     

Understanding extinction debts: spatio–temporal scales,mechanisms and a roadmap for future research

Extinction debt refers to delayed species extinctions expected as a consequence of ecosystem perturbation. Quantifying such extinctions and investigating long‐term consequences of perturbations has proven challenging, because perturbations are not isolated and occur across various spatial and temporal scales, from local habitat losses to global warming. Additionally, the relative importance of eco‐evolutionary processes varies across scales, because levels of ecological organization, i.e. individuals, (meta)populations and (meta)communities, respond hierarchically to perturbations. To summarize our current knowledge of the scales and mechanisms influencing extinction debts, we reviewed recent empirical, theoretical and methodological studies addressing either the spatio–temporal scales of extinction debts or the eco‐evolutionary mechanisms delaying extinctions. Extinction debts were detected across a range of ecosystems and taxonomic groups, with estimates ranging from 9 to 90% of current species richness. The duration over which debts have been sustained varies from 5 to 570 yr, and projections of the total period required to settle a debt can extend to 1000 yr. Reported causes of delayed extinctions are 1) life‐history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Other potential factors that may extend survival time such as microevolutionary dynamics, or delayed extinctions of interaction partners, have rarely been analyzed. Therefore, we propose a roadmap for future research with three key avenues: 1) the microevolutionary dynamics of extinction processes, 2) the disjunctive loss of interacting species and 3) the impact of multiple regimes of perturbation on the payment of debts. For their ability to integrate processes occurring at different levels of ecological organization, we highlight mechanistic simulation models as tools to address these knowledge gaps and to deepen our understanding of extinction dynamics.     

The two Early Toarcian (Early Jurassic) extinction events in ammonoids

The Early Toarcian (Early Jurassic) biological crisis was one of the ‘minor’ mass extinctions. It is linked with an oceanic anoxic event. Fossil data from sections located in northwestern European (epicontinental platforms and basins) and Tethyan (distal, epioceanic) areas indicate that Late Pliensbachian–Early Toarcian ammonoids experienced two extinction events during the Early Toarcian. The older one is linked with disruption of the Tethyan–Boreal provinciality, whereas the younger event correlates with the onset of anoxia and corresponds with the Early Toarcian mass‐extinction event. These two extinctions cannot be interpreted as episodes of a single, stepwise, event. Values of the net diversification, more than the number of extinctions, allow the two extinction events to be clearly recognized and distinguished. Values of regional net diversification for northwestern European and Tethyan faunas point to greater evolutionary dynamics in the epioceanic areas. The inclusion of Mediterranean faunas in the database proves that the ammonite turnover at the Early Toarcian mass‐extinction event was more important than previously thought. Progenitor (evolute Neolioceratoides), survivor (Dactylioceras, Polyplectus pluricostatus) and Lazarus (Procliviceras) taxa have been recognized. Different selectivity patterns are shown for the two events. The first one, linked to the disruption of the Tethyan–Boreal provinciality, has mainly affected ammonites adapted to epicontinental platforms. In the mass‐extinction event, no selectivity is recognized, because also Phylloceratina and Lytoceratina were deeply affected at species level, although their wide biogeographical distribution at clade level was a significant buffer against extinction. In contrast to Palaeozoic mass extinctions, ammonoid survivors and Lazarus taxa are characterized by complex sutures: Phylloceratina (long‐ranging ammonoids) and Polyplectus (relatively long‐ranging compared to other Ammonitina).     

Signatures of random and selective mass extinctions in phylogenetic tree balance

Current models of diversification with evolving speciation rates have trouble mimicking the extreme imbalance seen in estimated phylogenies. However, these models have not incorporated extinction. Here, we report on a simple simulation model that includes heritable and evolving speciation rates coupled with mass extinctions, Random (but not selective) mass extinctions, coupled with evolving among-lineage variation in speciation rates, increase imbalance of postrecovery clades. Thus, random mass extinctions are plausible contributors to the imbalance of modern clades. Paleontological evidence suggests that mass extinctions are often random with respect to ecological and morphological traits, consistent with our simulations. In contrast, evidence that the current anthropogenic mass extinction is phylogenetically selective suggests that the current extinction episode may be qualitatively different from past ones in the way it reshapes future biotas.     

Body length of bony fishes was not a selective factor during the biggest mass extinction of all time

The Permo‐Triassic mass extinction devastated life on land and in the sea, but it is not clear why some species survived and others went extinct. One explanation is that lineage loss during mass extinctions is a random process in which luck determines which species survive. Alternatively, a phylogenetic signal in extinction may indicate a selection process operating on phenotypic traits. Large body size has often emerged as an extinction risk factor in studies of modern extinction risk, but this is not so commonly the case for mass extinctions in deep time. Here, we explore the evolution of non‐teleostean Actinopterygii (bony fishes) from the Devonian to the present day, and we concentrate on the Permo‐Triassic mass extinction. We apply a variety of time‐scaling metrics to date the phylogeny, and show that diversity peaked in the latest Permian and declined severely during the Early Triassic. In line with previous evidence, we find the phylogenetic signal of extinction increases across the mass extinction boundary: extinction of species in the earliest Triassic is more clustered across phylogeny compared to the more randomly distributed extinction signal in the late Permian. However, body length plays no role in differential survival or extinction of taxa across the boundary. In the case of fishes, size did not determine which species survived and which went extinct, but phylogenetic signal indicates that the mass extinction was not a random field of bullets.     

Impact of the Late Triassic mass extinction on functional diversity and composition of marine ecosystems

Mass extinctions have profoundly influenced the history of life, not only through the death of species but also through changes in ecosystem function and structure. Importantly, these events allow us the opportunity to study ecological dynamics under levels of environmental stress for which there are no recent analogues. Here, we examine the impact and selectivity of the Late Triassic mass extinction event on the functional diversity and functional composition of the global marine ecosystem, and test whether post‐extinction communities in the Early Jurassic represent a regime shift away from pre‐extinction communities in the Late Triassic. Our analyses show that, despite severe taxonomic losses, there is no unequivocal loss of global functional diversity associated with the extinction. Even though no functional groups were lost, the extinction event was, however, highly selective against some modes of life, in particular sessile suspension feeders. Although taxa with heavily calcified skeletons suffered higher extinction than other taxa, lightly calcified taxa also appear to have been selected against. The extinction appears to have invigorated the already ongoing faunal turnover associated with the Mesozoic Marine Revolution. The ecological effects of the Late Triassic mass extinction were preferentially felt in the tropical latitudes, especially amongst reefs, and it took until the Middle Jurassic for reef ecosystems to fully recover to pre‐extinction levels.     

Sexual selection and the risk of extinction in mammals

Sexual selection is commonly envisaged as a force working in opposition to natural selection, because extravagant or exaggerated traits could apparently have never evolved via natural selection alone. There is good evidence that a selection load imposed by sexual selection may be eased experimentally by restricting the opportunity for it to operate. Sexual selection could therefore potentially play an important role in influencing the risk of extinction that a population faces, thereby contributing to the apparent selectivity of extinctions. Conversely, recent theory predicts that the likelihood of extinction may decrease when sexual selection is operating because it could accelerate the rate of adaptation in concert with natural selection. So far, comparative evidence (coming mostly from birds) has generally indicated support for the former scenario, but the question remains open. The aim of this study was therefore to examine whether the level of sexual selection (measured as residual testes mass and sexual size dimorphism) was related to the risk of extinction that mammals are currently experiencing. We found no evidence for a relationship between these factors, although our analyses may have been confounded by the possible dominating effect of contemporary anthropogenic factors.     

From success to persistence: Identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida,driven by the Devonian biotic crisis

Mass extinctions have altered the trajectory of evolution a number of times over the Phanerozoic. During these periods of biotic upheaval a different selective regime appears to operate, although it is still unclear whether consistent survivorship rules apply across different extinction events. We compare variations in diversity and disparity across the evolutionary history of a major Paleozoic arthropod group, the Eurypterida. Using these data, we explore the group's transition from a successful, dynamic clade to a stagnant persistent lineage, pinpointing the Devonian as the period during which this evolutionary regime shift occurred. The late Devonian biotic crisis is potentially unique among the “Big Five” mass extinctions in exhibiting a drop in speciation rates rather than an increase in extinction. Our study reveals eurypterids show depressed speciation rates throughout the Devonian but no abnormal peaks in extinction. Loss of morphospace occupation is random across all Paleozoic extinction events; however, differential origination during the Devonian results in a migration and subsequent stagnation of occupied morphospace. This shift appears linked to an ecological transition from euryhaline taxa to freshwater species with low morphological diversity alongside a decrease in endemism. These results demonstrate the importance of the Devonian biotic crisis in reshaping Paleozoic ecosystems.     

Organism activity levels predict marine invertebrate survival during ancient global change extinctions

Multistressor global change, the combined influence of ocean warming, acidification, and deoxygenation, poses a serious threat to marine organisms. Experimental studies imply that organisms with higher levels of activity should be more resilient, but testing this prediction and understanding organism vulnerability at a global scale, over evolutionary timescales, and in natural ecosystems remain challenging. The fossil record, which contains multiple extinctions triggered by multistressor global change, is ideally suited for testing hypotheses at broad geographic, taxonomic, and temporal scales. Here, I assess the importance of activity level for survival of well‐skeletonized benthic marine invertebrates over a 100‐million‐year‐long interval (Permian to Jurassic periods) containing four global change extinctions, including the end‐Permian and end‐Triassic mass extinctions. More active organisms, based on a semiquantitative score incorporating feeding and motility, were significantly more likely to survive during three of the four extinction events (Guadalupian, end‐Permian, and end‐Triassic). In contrast, activity was not an important control on survival during nonextinction intervals. Both the end‐Permian and end‐Triassic mass extinctions also triggered abrupt shifts to increased dominance by more active organisms. Although mean activity gradually returned toward pre‐extinction values, the net result was a permanent ratcheting of ecosystem‐wide activity to higher levels. Selectivity patterns during ancient global change extinctions confirm the hypothesis that higher activity, a proxy for respiratory physiology, is a fundamental control on survival, although the roles of specific physiological traits (such as extracellular pCO₂ or aerobic scope) cannot be distinguished. Modern marine ecosystems are dominated by more active organisms, in part because of selectivity ratcheting during these ancient extinctions, so on average may be less vulnerable to global change stressors than ancient counterparts. However, ancient extinctions demonstrate that even active organisms can suffer major extinction when the intensity of environmental disruption is intense.     

Functional Group Change within and across Scales following Invasions and Extinctions in the Everglades Ecosystem

Cross-scale resilience theory predicts that the combination of functional diversity within scales and functional redundancy across scales is an important attribute of ecosystems because it helps these systems resist minor ecological disruptions and regenerate after major disturbances such as hurricanes and fire. Using the vertebrate fauna of south Florida, we quantified how the loss of native species and invasion by nonnatives may alter functional group richness within and across scales. We found that despite large changes in species composition due to potential extinctions and successful invasions by nonnative species, functional group richness will not change significantly within scales, there will not be any significant loss of overall redundancy of ecology function across scales, and overall body mass pattern will not undergo substantial change. However, the types of functions performed will change, and this change may have profound effects on not only the Everglades ecosystem but on the entire landscape of south Florida. Received 14 November 2000; accepted 20 December 2001.     

Extinctive evolution: Extinctive and competitive evolution combine into a unified model of evolution

Individual extinctions of abundant and widespread species of marine Protista are abrupt and precede the appearance of new species. New species evolve gradually in marginal marine environments and spread only if a suitable ecological domain is available or if such a domain is made available by the disappearance of its occupant species. Competitive evolution, with its classic processes of genetic drift, adaptation, competition, and survival of the fittest, occurs mainly in marginal environments (and possibly within broadly distributed but rare species). Extinctive evolution, on the other hand, with its processes of sudden extinctions and sudden appearances, absence of competition, absence of “missing links”, and frequent survival of the misfit or the indifferently fit is prevalent in broader environments, and more generally applicable to the paleontological record. The modern biosphere is not necessarily better adapted than its predecessors. Global mass extinction affecting different taxa across a broad spectrum of environments is caused by extraordinary environmental disturbances. A major ecosphere is vacated, which is immediately occupied by surviving misfits. These are replaced, through competitive evolution, by a rapid succession of increasingly better adapted species that can be classified into different genera and higher taxa (“macroevolution”). Equilibrium is largely re-established within a few million years. Competitive and extinctive evolution combine into a unified model of evolution.     

Introductions do not compensate for functional and phylogenetic losses following extinctions in insular bird assemblages

The ratio of species extinctions to introductions has been comparable for many insular assemblages, suggesting that introductions could have ‘compensated’ for extinctions. However, the capacity for introduced species to replace ecological roles and evolutionary history lost following extinction is unclear. We investigated changes in bird functional and phylogenetic diversity in the wake of extinctions and introductions across a sample of 32 islands worldwide. We found that extinct and introduced species have comparable functional and phylogenetic alpha diversity. However, this was distributed at different positions in functional space and in the phylogeny, indicating a ‘false compensation’. Introduced and extinct species did not have equivalent functional roles nor belong to similar lineages. This makes it unlikely that novel island biotas composed of introduced taxa will be able to maintain ecological roles and represent the evolutionary histories of pre‐disturbance assemblages and highlights the importance of evaluating changes in alpha and beta diversity concurrently.     

Were Phanerozoic mass extinctions among brachiopod superfamilies selective by taxa longevity?

All mass extinctions are characterized by certain kind of selectivity. An analysis of stratigraphic ranges of 112 brachiopod superfamilies implies that some Phanerozoic mass extinctions (Late Ordovician, Frasnian/Famennian and Devonian/Carboniferous, Early Jurassic, and Cretaceous/Paleogene) were selective by taxa longevity. They preferentially affected relatively old superfamilies and favoured a survival of relatively young superfamilies. No explanation of this selectivity as an apparent phenomenon is fully satisfactory. The Permian/Triassic mass extinction did not favour a survival of “young” superfamilies because of abnormally low rate of origination established since the Pennsylvanian and the absence of these “young” taxa. This study confirms tentatively a difference between Paleozoic and post-Paleozoic times by the importance of post-extinction recovery intervals for taxa longevity.     

Microbes and mass extinctions: paleoenvironmental distribution of microbialites during times of biotic crisis

Widespread development of microbialites characterizes the substrate and ecological response during the aftermath of two of the 'big five' mass extinctions of the Phanerozoic. This study reviews the microbial response recorded by macroscopic microbial structures to these events to examine how extinction mechanism may be linked to the style of microbialite development. Two main styles of response are recognized: (i) the expansion of microbialites into environments not previously occupied during the pre-extinction interval and (ii) increases in microbialite abundance and attainment of ecological dominance within environments occupied prior to the extinction. The Late Devonian biotic crisis contributed toward the decimation of platform margin reef taxa and was followed by increases in microbialite abundance in Famennian and earliest Carboniferous platform interior, margin, and slope settings. The end-Permian event records the suppression of infaunal activity and an elimination of metazoan-dominated reefs. The aftermath of this mass extinction is characterized by the expansion of microbialites into new environments including offshore and nearshore ramp, platform interior, and slope settings. The mass extinctions at the end of the Triassic and Cretaceous have not yet been associated with a macroscopic microbial response, although one has been suggested for the end-Ordovician event. The case for microbialites behaving as 'disaster forms' in the aftermath of mass extinctions accurately describes the response following the Late Devonian and end-Permian events, and this may be because each is marked by the reduction of reef communities in addition to a suppression of bioturbation related to the development of shallow-water anoxia.     

The evolution of diversity in ancient ecosystems: a review

On a perfect planet, such as might be acceptable to a physicist, one might predict that from its origin the diversity of life would grow exponentially until the carrying capacity, however defined, was reached. The fossil record of the Earth, however, tells a very different story. One of the most striking aspects of this record is the apparent evolutionary longueur, marked by the Precambrian record of prokaryotes and primitive eukaryotes, although our estimates of microbial diversity may be seriously incomplete. Subsequently there were various dramatic increases in diversity, including the Cambrian ''explosion'' and the radiation of Palaeozoic-style faunas in the Ordovician. The causes of these events are far from resolved. It has also long been appreciated that the history of diversity has been punctuated by important extinctions. The subtleties and nuances of extinction as well as the survival of particular clades have to date, however, received rather too little attention, and there is still a tendency towards blanket assertions rather than a dissection of these extraordinary events. In addition, some but perhaps not all mass extinctions are characterized by long lag-times of recovery, which may reflect the slowing waning of extrinsic forcing factors or alternatively the incoherence associated with biological reassembly of stable ecosystems. The intervening periods between the identified mass extinctions may be less stable and benign than popularly thought, and in particular the frequency of extraterrestrial impacts leads to predictions of recurrent disturbance on timescales significantly shorter than the intervals separating the largest extinction events. Even at times of quietude it is far from clear whether biological communities enjoy stability and interlocked stasis or are dynamically reconstituted at regular intervals. Finally, can we yet rely on the present depictions of the rise and falls in the levels of ancient diversity? Existing data is almost entirely based on Linnean taxa, and the application of phylogenetic systematics to this problem is still in its infancy. Not only that, but even more intriguingly the pronounced divergence in estimates of origination times of groups as diverse as angiosperms, diatoms and mammals in terms of the fossil record as against molecular data point to the possibilities of protracted intervals of geological time with a cryptic diversity. If this is correct, and there are alternative explanations, then some of the mystery of adaptive radiations may be dispelled, in as much as the assembly of key features in the stem groups could be placed in a gradualistic framework of local adaptive response punctuated by intervals of opportunity.     

Some remarks on the structure and function of refugia in ecology and palaeoecology

Studies of processes connected with various Phanerozoic mass extinctions suggest that although these events differ in details from each other, they manifest certain global mutual similarities. There is a number of detailed data on the mass extinction phases but only scarce information on the survival and recovery intervals directly following the crises. In connection with the biota crises studies also the problem of refugia started to be discussed very intensively, because namely fossil refugia can contain fossils representing important connecting links getting over boundaries of mass extinctions. The aim of this article is to join some general considerations of possible refugia structures, functions and spatial and temporal changes to the discussion being in progress.     

Trophic network models explain instability of Early Triassic terrestrial communities

Studies of the end-Permian mass extinction have emphasized potential abiotic causes and their direct biotic effects. Less attention has been devoted to secondary extinctions resulting from ecological crises and the effect of community structure on such extinctions. Here we use a trophic network model that combines topological and dynamic approaches to simulate disruptions of primary productivity in palaeocommunities. We apply the model to Permian and Triassic communities of the Karoo Basin, South Africa, and show that while Permian communities bear no evidence of being especially susceptible to extinction, Early Triassic communities appear to have been inherently less stable. Much of the instability results from the faster post-extinction diversification of amphibian guilds relative to amniotes. The resulting communities differed fundamentally in structure from their Permian predecessors. Additionally, our results imply that changing community structures over time may explain long-term trends like declining rates of Phanerozoic background extinction.     

The ghosts of mammals past: biological and geographical patterns of global mammalian extinction across the Holocene

Although the recent historical period is usually treated as a temporal base-line for understanding patterns of mammal extinction, mammalian biodiversity loss has also taken place throughout the Late Quaternary. We explore the spatial, taxonomic and phylogenetic patterns of 241 mammal species extinctions known to have occurred during the Holocene up to the present day. To assess whether our understanding of mammalian threat processes has been affected by excluding these taxa, we incorporate extinct species data into analyses of the impact of body mass on extinction risk. We find that Holocene extinctions have been phylogenetically and spatially concentrated in specific taxa and geographical regions, which are often not congruent with those disproportionately at risk today. Large-bodied mammals have also been more extinction-prone in most geographical regions across the Holocene. Our data support the extinction filter hypothesis, whereby regional faunas from which susceptible species have already become extinct now appear less threatened; they may also suggest that different processes are responsible for driving past and present extinctions. We also find overall incompleteness and inter-regional biases in extinction data from the recent fossil record. Although direct use of fossil data in future projections of extinction risk is therefore not straightforward, insights into extinction processes from the Holocene record are still useful in understanding mammalian threat.