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Extinction As the Loss of Evolutionary History

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Extinction As the Loss of Evolutionary History Extinction as the loss of evolutionary history Douglas H. Erwin* Department of Paleobiology, MRC-121, National Museum of Natural History, Washington, DC 20013-7013; and Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501 Current plant and animal diversity preserves at most 1–2% of the preservation and correlation make species-level compilations species that have existed over the past 600 million years. But impractical. Conservation biologists have long focused on spe- understanding the evolutionary impact of these extinctions re- cies, an approach enshrined in the U.S. Endangered Species Act. quires a variety of metrics. The traditional measurement is loss of This reliance on taxa tends to assume, implicitly, that taxonomic taxa (species or a higher category) but in the absence of phyloge- entities are a reliable metric to the impact of extinction on netic information it is difficult to distinguish the evolutionary ecosystem structure and function, morphological variability, depth of different patterns of extinction: the same species loss can behavior complexity, and developmental processes. This as- encompass very different losses of evolutionary history. Further- sumption is often far from true. Consequently, conservation more, both taxic and phylogenetic measures are poor metrics of biologists have proposed other metrics for identifying critical morphologic disparity. Other measures of lost diversity include: targets for conservation (4), including biogeographic centers of functional diversity, architectural components, behavioral and so- endemic taxa, or hotspots (5), and the characterization of cial repertoires, and developmental strategies. The canonical five phylogenetic diversity (6, 7) and evolutionary distinctiveness (8). mass extinctions of the Phanerozoic reveals the loss of different, There is, however, a more important reason for considering the albeit sometimes overlapping, aspects of loss of evolutionary loss of other aspects of evolutionary history, and that is the history. The end-Permian mass extinction (252 Ma) reduced all search for mechanisms underlying patterns of extinction and measures of diversity. The same was not true of other episodes, construction of biodiversity. Ecologists increasingly recognize differences that may reflect their duration and structure. The the importance of a network of interactions in generating construction of biodiversity reflects similarly uneven contributions biodiversity, including positive feedback relationships among to each of these metrics. Unraveling these contributions requires biodiversity, productivity, and stability (9, 10). greater attention to feedbacks on biodiversity and the temporal Although paleontologists are aware of the diversity of effects variability in their contribution to evolutionary history. Taxic on evolutionary history caused by past extinctions, particularly diversity increases after mass extinctions, but the response by mass extinctions, we have been slow to develop and apply other aspects of evolutionary history is less well studied. Earlier comparative metrics beyond taxic compilations and estimates of views of postextinction biotic recovery as the refilling of empty geographic range. Enough work has been done to suggest a range ecospace fail to capture the dynamics of this diversity increase. of alternative metrics. Biogeographic structure is an important aspect of evolutionary history that has been considered biodiversity ͉ morphologic disparity ͉ ecosystem engineering elsewhere (11). xtinction is the inevitable fate of organisms, although there Taxic Diversity. The divisions of the geologic time scale are framed Eis considerable variance in both rates of extinction through by biotic crises recognized by early geologists as ‘‘revolutions’’ time and the duration of particular species or clades. By some triggering wholesale changes in the biota. Paleontologists have estimates, extant multicellular biodiversity is but 1–2% of all since compiled records of fluctuations in taxonomic diversity for multicellular species that have existed over the past 600 Ma (1, marine taxa (12, 13), terrestrial plants (14), vertebrates (15), and 2). Paleontologists have long recognized that the relatively various microfossil groups (16). Patterns of extinction and regular overturn of species is occasionally punctuated by more origination have received considerable attention, particularly the severe biotic crises, including at least five events recognized as decline in ‘‘background’’ extinction rates through the Phanero- mass extinctions. Some have claimed that rates of current species zoic for marine families and genera (17) and episodic events of loss exceed those of past mass extinctions. Perhaps the most increased extinction. Curiously, as the English geologist John valuable contribution that paleontologists can make to under- Phillips understood as long ago as the 1840s, extinctions within standing the current biodiversity crisis is to identify the rela- geologic stages appears pulsed, rather than spread out through tionship between attributes of the loss of past evolutionary the stage (18). Within clades paleontologists have also identified history and both the depth of past crises and the speed and intriguing patterns of replacement where successive subclades structure of subsequent biotic recovery. Given that conservation replaced earlier clades. For higher-resolution analyses statistical biologists increasingly face a problem of triage, where not all techniques have been developed to account for sampling prob- species can be saved, can paleontological data provide any lems (see ref. 19 for an application to the end-Permian mass insights into the species, communities, or structures that should extinction). have the highest priority for support? Paleontological data are Several general lessons emerge from these compilations. First, unlikely to be decisive in such decisions, but the unique per- the persistent decline in extinction rates suggests an increased spective provided by the fossil record may provide a useful input. stability in younger taxa, although this may be a statistical artifact Here, I discuss a range of potential metrics for the impact of of increased species/genus and species/family ratios (17). It extinction on the loss of evolutionary history and provide a would be of considerable interest to know whether this apparent preliminary application of them to the five canonical mass extinctions (see also ref. 3). There are, however, relatively few This paper results from the Arthur M. Sackler Colloquium of the National Academy of applications of these metrics to understanding the processes of Sciences, ‘‘In the Light of Evolution II: Biodiversity and Extinction,’’ held December 6–8, postextinction biotic recovery. 2007, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and audio files of most presentations are Metrics for the Loss of Evolutionary History available on the NAS web site at www.nasonline.org/Sackler࿝biodiversity. The traditional accounting method for the loss of evolutionary Author contributions: D.H.E. performed research and wrote the paper. history is taxa: populations and species for biologists, often The author declares no conflict of interest. genera or families for paleontologists because the vagaries of *E-mail: [email protected]. 11520–11527 ͉ PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ suppl. 1 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0801913105 Downloaded by guest on September 25, 2021 simple example demonstrates how knowledge of the phyloge- netic structure is essential to evaluating the amount of evolu- tionary history lost or at risk, and not surprisingly conservation biologists have proposed several different metrics for measuring phylogenetic diversity (6–8). Although some have argued that taxic diversity is a reliable proxy for phylogenetic diversity, empirical studies have convincingly demonstrated the need for phylogenetic analyses. A study of the plants of the fynbos of South Africa, for example, showed that generic richness is strongly decoupled from phylogenetic diversity (34). The most direct demonstration of the importance of a phylogenetic frame- Fig. 1. Similar losses of taxic diversity have very different implications for the work was a study showing that some 80% of the structure of the loss of evolutionary history depending on the phylogenetic distribution of the underlying phylogeny can survive even a 95% loss of species (35), extinctions. Three different scenarios are shown, at levels A, B, and C. (A) Seven if the extinctions are random. When the phylogenetic structure taxa are lost (33% extinction) but the overall structure of the phylogeny is of an extinction is highly clustered, the effects on evolutionary preserved. (B) An entire clade of seven taxa is pruned, but the remaining history can be more severe (36). structure is preserved. (C) Six taxa are lost but this eliminates the deepest Paleontologists have long recognized the unequal impact of branching clades. past biotic crises on the disappearance of particular clades, including archaeocyathid sponges in the Early Cambrian; many increased robustness is real and whether it translates into some trilobite clades and numerous problematica during the various of the other metrics described below. Second, patterns of Cambrian crises; trilobites, blastoids and many smaller clades during the end-Permian mass extinction; conodonts at the subclade replacement can suggest adaptive improvement
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