Losing history: how extinctions prune features from the tree of life

Biodiversity provides many valuable services to humanity; however, rapid expansion of the human population has placed increasing pressure on natural systems, and it has been suggested that we may be entering a sixth mass extinction. There is an urgent need, therefore, to prioritize conservation efforts if we are to maintain the provisioning of such service in the future. Phylogenetic diversity (PD), the summed branch lengths that connect species on the tree-of-life, might provide a valuable metric for conservation prioritization because it has been argued to capture feature diversity. Frequently, PD is estimated in millions of years, and therefore implicitly assumes an evolutionary model in which features diverge gradually over time. Here, I explore the expected loss of feature diversity when this assumption is violated. If evolution tends to slow down over time, as might be the case following adaptive radiations, losses of feature diversity might be relatively small. However, if evolution occurs in rapid bursts, following a punctuated model, impacts of extinctions might be much greater. PD captures many important properties, but if we use it as a proxy for feature diversity, we first need to ensure that we have the correct evolutionary model.     

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.     

Branch lengths on birth-death trees and the expected loss of phylogenetic diversity

Diversification is nested, and early models suggested this could lead to a great deal of evolutionary redundancy in the Tree of Life. This result is based on a particular set of branch lengths produced by the common coalescent, where pendant branches leading to tips can be very short compared with branches deeper in the tree. Here, we analyze alternative and more realistic Yule and birth-death models. We show how censoring at the present both makes average branches one half what we might expect and makes pendant and interior branches roughly equal in length. Although dependent on whether we condition on the size of the tree, its age, or both, these results hold both for the Yule model and for birth-death models with moderate extinction. Importantly, the rough equivalency in interior and exterior branch lengths means that the loss of evolutionary history with loss of species can be roughly linear. Under these models, the Tree of Life may offer limited redundancy in the face of ongoing species loss.     

Phylogenetic extinction rates and comparative methodology

Species are not independent points for comparative analyses because closely related species share more evolutionary history and are therefore more similar to each other than distantly related species. The extent to which independent-contrast analysis reduces type I and type II statistical error in comparison with cross-species analysis depends on the relative branch lengths in the phylogenetic tree: as deeper branches get relatively long, cross-species analyses have more statistical type I and type II error. Phylogenetic trees reconstructed from extant species, under the assumptions of a branching process with speciation (branching) and extinction rates remaining constant through time, will have relatively longer deep branches as the extinction rate increases relative to the speciation rate. We compare the statistical performance of cross-species and independent-contrast analyses with varying relative extinction rates, and conclude that cross-species comparisons have unacceptable statistical performance, particularly when extinction rates are relatively high.     

Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions

If we are to plan conservation strategies that minimize the loss of evolutionary history through human-caused extinctions, we must understand how this loss is related to phylogenetic patterns in current extinction risks and past speciation rates. Nee & May (1997, Science 278, 692-694) showed that for a randomly evolving clade (i) a single round of random extinction removed relatively little evolutionary history, and (ii) extinction management (choosing which taxa to sacrifice) offered only marginal improvement. However, both speciation rates and extinction risks vary across lineages within real clades. We simulated evolutionary trees with phylogenetically patterned speciation rates and extinction risks (closely related lineages having similar rates and risks) and then subjected them to several biologically informed models of extinction. Increasing speciation rate variation increases the extinction-management pay-off. When extinction risks vary among lineages but are uncorrelated with speciation rates, extinction removes more history (compared with random trees), but the difference is small. When extinction risks vary and are correlated with speciation rates, history loss can dramatically increase (negative correlation) or decrease (positive correlation) with speciation rate variation. The loss of evolutionary history via human-caused extinctions may therefore be more severe, yet more manageable, than first suggested.     

Phylogenetically clustered extinction risks do not substantially prune the Tree of Life

Anthropogenic activities have increased the rate of biological extinction many-fold. Recent empirical studies suggest that projected extinction may lead to extensive loss to the Tree of Life, much more than if extinction were random. One suggested cause is that extinction risk is heritable (phylogenetically patterned), such that entire higher groups will be lost. We show here with simulation that phylogenetically clustered extinction risks are necessary but not sufficient for the extensive loss of phylogenetic diversity (PD) compared to random extinction. We simulated Yule trees and evolved extinction risks at various levels of heritability (measured using Pagel's λ). At most levels of heritability (λ in range of 0 to 10), mean values of extinction risk (range 0.25 to 0.75), tree sizes (64 to 128 tips), tree balance and temporal heterogeneity of diversification rates (Yule and coalescent trees), extinction risks do not substantially increase the loss of PD in these trees when compared to random extinction. The maximum loss of PD (20% above random) was only associated with the combination of extremely excessive values of phylogenetic signal, high mean species' extinction probabilities, and extreme (coalescent) tree shapes. Interestingly, we also observed a decline in the rate of increase in the loss of PD at high phylogenetic clustering (λ → 10) of extinction risks. Our results suggest that the interplay between various aspects of tree shape and a predisposition of higher extinction risks in species-poor clades is required to explain the substantial pruning of the Tree of Life.     

Extinction risk and diversification are linked in a plant biodiversity hotspot

It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny--opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.     

Extinction vulnerability of coral reef fishes

With rapidly increasing rates of contemporary extinction, predicting extinction vulnerability and identifying how multiple stressors drive non-random species loss have become key challenges in ecology. These assessments are crucial for avoiding the loss of key functional groups that sustain ecosystem processes and services. We developed a novel predictive framework of species extinction vulnerability and applied it to coral reef fishes. Although relatively few coral reef fishes are at risk of global extinction from climate disturbances, a negative convex relationship between fish species locally vulnerable to climate change vs. fisheries exploitation indicates that the entire community is vulnerable on the many reefs where both stressors co-occur. Fishes involved in maintaining key ecosystem functions are more at risk from fishing than climate disturbances. This finding is encouraging as local and regional commitment to fisheries management action can maintain reef ecosystem functions pending progress towards the more complex global problem of stabilizing the climate.     

The Butterflies of Barro Colorado Island,Panama: Local Extinction since the 1930s

Few data are available about the regional or local extinction of tropical butterfly species. When confirmed, local extinction was often due to the loss of host-plant species. We used published lists and recent monitoring programs to evaluate changes in butterfly composition on Barro Colorado Island (BCI, Panama) between an old (1923–1943) and a recent (1993–2013) period. Although 601 butterfly species have been recorded from BCI during the 1923–2013 period, we estimate that 390 species are currently breeding on the island, including 34 cryptic species, currently only known by their DNA Barcode Index Number. Twenty-three butterfly species that were considered abundant during the old period could not be collected during the recent period, despite a much higher sampling effort in recent times. We consider these species locally extinct from BCI and they conservatively represent 6% of the estimated local pool of resident species. Extinct species represent distant phylogenetic branches and several families. The butterfly traits most likely to influence the probability of extinction were host growth form, wing size and host specificity, independently of the phylogenetic relationships among butterfly species. On BCI, most likely candidates for extinction were small hesperiids feeding on herbs (35% of extinct species). However, contrary to our working hypothesis, extinction of these species on BCI cannot be attributed to loss of host plants. In most cases these host plants remain extant, but they probably subsist at lower or more fragmented densities. Coupled with low dispersal power, this reduced availability of host plants has probably caused the local extinction of some butterfly species. Many more bird than butterfly species have been lost from BCI recently, confirming that small preserves may be far more effective at conserving invertebrates than vertebrates and, therefore, should not necessarily be neglected from a conservation viewpoint.     

Extinction order and altered community structure rapidly disrupt ecosystem functioning

By causing extinctions and altering community structure, anthropogenic disturbances can disrupt processes that maintain ecosystem integrity. However, the relationship between community structure and ecosystem functioning in natural systems is poorly understood. Here we show that habitat loss appeared to disrupt ecosystem functioning by affecting extinction order, species richness and abundance. We studied pollination by bees in a mosaic of agricultural and natural habitats in California and dung burial by dung beetles on recently created islands in Venezuela. We found that large-bodied bee and beetle species tended to be both most extinction-prone and most functionally efficient, contributing to rapid functional loss. Simulations confirmed that extinction order led to greater disruption of function than predicted by random species loss. Total abundance declined with richness and also appeared to contribute to loss of function. We demonstrate conceptually and empirically how the non-random response of communities to disturbance can have unexpectedly large functional consequences.     

Anthropogenic extinction threats and future loss of evolutionary history in reef corals

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.     

Habitat loss and mammalian extinction patterns: are the reserves in the Quadrilátero Ferrífero, southeastern Brazil, effective in conserving mammals?

Habitat loss is considered to be the principal cause of the local extinction of mammals worldwide. We assessed the extinction pattern of medium- and large-sized mammals caused by the effects of habitat loss in reserves in the Quadrilátero Ferrífero, southeastern Brazil, and discussed the effectiveness of these natural remnants for conserving mammals. A literature review and field collections were conducted from 2006 to 2011 to estimate the composition and richness of mammals in nine remnants of different sizes, including reserves and non-protected areas. A species–area relation and a nested subset analysis were performed, and a degree of sensitivity to habitat loss was obtained for each species according to its frequency of occurrence. Forty-five species of mammals were recorded. There was a strong species–area relation involving the legal size of reserves. High species richness was associated with large reserves, and the z value was within the range of very isolated continental remnants. The mammalian community exhibited a nested occurrence pattern, suggesting that most species were part of a more continuous ecosystem and that non-random extinction caused by habitat loss occurred in southeastern Brazil. The negative relation found between species frequencies and body weights suggested that selective species loss is associated with decreases in the size of the reserves. The estimated viable size required to conserve all of the sensitive species is greater than the size of the largest reserve inventoried. We recommend the aggregation of neighboring natural remnants and the creation of new reserves to reduce extinction risks.     

Climate‐driven extinctions shape the phylogenetic structure of temperate tree floras

When taxa go extinct, unique evolutionary history is lost. If extinction is selective, and the intrinsic vulnerabilities of taxa show phylogenetic signal, more evolutionary history may be lost than expected under random extinction. Under what conditions this occurs is insufficiently known. We show that late Cenozoic climate change induced phylogenetically selective regional extinction of northern temperate trees because of phylogenetic signal in cold tolerance, leading to significantly and substantially larger than random losses of phylogenetic diversity (PD). The surviving floras in regions that experienced stronger extinction are phylogenetically more clustered, indicating that non‐random losses of PD are of increasing concern with increasing extinction severity. Using simulations, we show that a simple threshold model of survival given a physiological trait with phylogenetic signal reproduces our findings. Our results send a strong warning that we may expect future assemblages to be phylogenetically and possibly functionally depauperate if anthropogenic climate change affects taxa similarly.     

Extinction of retinol-binding protein gene expression in somatic cell-hybrids: identification of the target sequences.

The Retinol-Binding Protein (RBP) is expressed primarily in the liver. The regulatory elements involved in its tissue-specific expression have been identified and mapped to the 5' flanking region of the RBP gene. In this paper heterokaryons and somatic cell-hybrids have been produced and analysed in order to demonstrate that the RBP gene is subject to extinction and to identify the target sequences of this phenomenon. We show here that the gene is extinguished in fusions of hepatoma with a variety of cells of different species and embryonic lineages. The repression is not due to loss of the gene and occurs also when chromosome 10, where the gene is located, is inherited from the expressing parental cell-type. Hybrid clones were transfected with constructs carrying DNA segments of different lengths from the 5' flanking region of the RBP gene fused to a reporter gene. We demonstrate that extinction takes place also on an exogenous RBP-CAT gene, mimicking the phenomenon observed with the endogenous gene in its chromosomal location. Moreover, we identify and map the target sequences of the putative extinguishing function. Our data thus show that extinction of RBP is mediated through the DNA segment that is involved in its tissue-specific expression.     

Macroevolution and climate change influence phylogenetic community assembly of North American hoofed mammals

Animal richness, community composition, and phylogenetic community structure (PCS) vary across the modern landscape. Animal communities vary from phylogenetically clustered (i.e. higher relatedness amongst co‐occurring species than is expected by chance) to phylogenetically even (i.e. co‐occurring taxa are more distantly related than expected by chance), which is explained by abiotic or climatic filtering and competitive exclusion, respectively. Under this model, the contribution of historical origination and extinction events to modern animal PCS remains relatively unknown. Because origination and extinction determine the make‐up of the terrestrial community, the study of historical changes in animal PCS is tantamount to understanding formation of modern communities. In the present study, we test the effects of macroevolution and climate changes on ‘hoofed mammals’ (i.e. perissodactyl and artiodactyl) PCS from the late Cenozoic of North America because they experience large, phylogenetically dispersed extinctions of browsing species and phylogenetically dispersed originations of grazing species associated with the evolution of grassland ecosystems during the late Miocene. We show that the loss of numerically dominant nonhypsodont (putatively browsing and mixed feeding) clades and phylogenetically dispersed origination of less speciose clades following the mid Miocene climatic optimum led to an increase in phylogenetic evenness at the regional scale that is well explained by global climate changes. Phylogenetic evenness and a reduced richness during the late Cenozoic may have facilitated reduced niche overlap among co‐occurring hoofed mammal species as global climates cooled. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 485–494.     

Nestedness-resultant community disassembly process of extinction debt in a highly fragmented semi-natural grassland

There are two major processes of species disassembly after landscape changes: non-random loss of species resulting in nested assemblages and species replacement resulting in spatial species turnover. Although time-lagged responses of species to landscape change have been widely recognized, few studies have empirically evaluated which of these two processes is more closely related to extinction debt (i.e., postponed species extinction following habitat loss). This study aimed to understand the underlying processes of extinction debt by partitioning β-diversity into components of species nestedness and species turnover. We measured grassland species richness at three spatial extents in a highly fragmented semi-natural grassland landscape in Japan. Dissimilarity-based β-diversity was partitioned into two components (i.e., nestedness-resultant dissimilarity [β_sne] and turnover-resultant dissimilarity [β_sim]), which were further analyzed using principal coordinates analyses (PCoA). The relationships between the variability of PCoA axis 1 scores and the current and past habitat proportions were evaluated. A significant positive relationship between current grassland species richness and past (i.e., the 1910s) grassland proportion was found at the largest spatial extent. The first axis of PCoA based on β_sne showed significant correlation with past habitat proportions, whereas the PCoA axis based on β_sim showed no significant correlation with either the current or past habitat proportions. A non-random loss of grassland species represented by nestedness underlay the extinction debt found at the landscape level. There is a chance of predicting the loss of species from the nested ranks of species which likely reflects the gradient of species vulnerability to historical landscape changes.     

How do habitat amount and habitat fragmentation drive time-delayed responses of biodiversity to land-use change?

Land-use change is a root cause of the extinction crisis, but links between habitat change and biodiversity loss are not fully understood. While there is evidence that habitat loss is an important extinction driver, the relevance of habitat fragmentation remains debated. Moreover, while time delays of biodiversity responses to habitat transformation are well-documented, time-delayed effects have been ignored in the habitat loss versus fragmentation debate. Here, using a hierarchical Bayesian multi-species occupancy framework, we systematically tested for time-delayed responses of bird and mammal communities to habitat loss and to habitat fragmentation. We focused on the Argentine Chaco, where deforestation has been widespread recently. We used an extensive field dataset on birds and mammals, along with a time series of annual woodland maps from 1985 to 2016 covering recent and historical habitat transformations. Contemporary habitat amount explained bird and mammal occupancy better than past habitat amount. However, occupancy was affected more by the past rather than recent fragmentation, indicating a time-delayed response to fragmentation. Considering past landscape patterns is therefore crucial for understanding current biodiversity patterns. Not accounting for land-use history ignores the possibility of extinction debt and can thus obscure impacts of fragmentation, potentially explaining contrasting findings of habitat loss versus fragmentation studies.     

Testing the effects of plant species loss on multiple ecosystem functions based on extinction scenarios

Ecosystem functions are threatened by continuing global loss of biodiversity. We simultaneously investigated three ecosystem functions and forage nutrient values following potential species extinction scenarios (dominant species removal, rare species removal, end-member species removal and random species removal) in a Mongolian grassland. ANPP, forage nutrient values, litter decomposition, and soil respiration were measured one and/or two years after plant removal. DNA samples of microorganisms extracted from the soil were subjected to metagenomics analysis. Finally, we calculated the multifunctionality, and examined the relationship of multifunctionality with plant and microorganism diversity. Among ecosystem functions, ANPP and litter decomposition rate decreased under random and rare species extinction scenarios, respectively, and forage quality increased when only dominant species had been removed. Diversity and species composition of soil microorganism were not affected by plant species richness or removal scenario. Only genus-level diversity of bacteria and ANPP were significantly and positively correlated with microbial diversity. Taken together, decreasing species richness of plants and soil organisms rarely impaired multifunctionality. Ecosystem functions were relatively robust to realistic disturbances and species extinction in natural grasslands. However, as each function responded differently to the different sets of species removed, the consequences of a realistic non-random extinction scenario for multiple ecosystem functions should be critical to the management of biodiversity loss caused by different disturbances.     

Taxonomic selectivity in amphibians: ignorance, geography or biology?

Many taxa, including amphibians, have been shown to have a taxonomically non-random distribution of threatened species. There are three possible non-exclusive reasons for this selectivity: non-random knowledge of species conservation status, clades endemic to different regions experiencing different intensities of threatening process and the effects of clade-specific biological attributes on the susceptibility of species to these processes. This paper tests the sufficiency of the first two explanations using extinction risk evaluations from the 2004 Global Amphibian Assessment. Our results indicate that they cannot alone account for the degree of non-randomness in extinction risk among amphibian families. The overall distribution of threatened amphibians remained taxonomically non-random when species of unknown conservation status were omitted, and significant selectivity was detected not only at a global geographic scale but also in country- and site-specific data sets. Furthermore, the same families tend to be over- or underthreatened within different countries. Together, these results suggest that biological differences among amphibian families play an important role in determining species' susceptibility to anthropogenic threatening processes.