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Extinction and the Spatial Dynamics of Biodiversity

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Extinction and the Spatial Dynamics of Biodiversity Extinction and the spatial dynamics of biodiversity David Jablonski* Department of Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, IL 60637 The fossil record amply shows that the spatial fabric of extinction extinctions of the geologic past are a separate class of intensities has profoundly shaped the biosphere; this spatial dimension pro- from the ‘‘background’’ extinction that constitutes the great bulk vides a powerful context for integration of paleontological and of geologic time (and the bulk of total extinction; ref. 5), but this neontological approaches. Mass extinctions evidently alter extinc- is a secondary issue that can probably be resolved by factoring tion selectivity, with many factors losing effectiveness except for out the well known secular decline in background extinction a positive relation between survivorship and geographic range at rates (6–8). As discussed below, extinction selectivities evidently the clade level (confirmed in reanalyses of end-Cretaceous extinc- shift between episodes of low and high extinction rates, and this tion data). This relation probably also holds during ‘‘normal’’ times, selectivity is the more important issue for understanding the role but changes both slope and intercept with increasing extinction. of extinction in shaping past and future biotas. I will corroborate The strong geographical component to clade dynamics can obscure previous evidence for a strong spatial component to survivorship causation in the extinction of a feature or a clade, owing to during major extinction events, present a multifactorial analysis hitchhiking effects on geographic range, so that multifactorial of the end-Cretaceous (K-T) mass extinction in which geo- analyses are needed. Some extinctions are spatially complex, and graphic range emerges as the best predictor of survivorship in regional extinctions might either reset a diversity ceiling or create marine bivalves, and argue that such indirect effects are probably a diversification debt open to further diversification or invasion. more important than generally appreciated. I will also discuss Evolutionary recoveries also exhibit spatial dynamics, including regional variations in the balance of invasions and local origi- regional differences in invasibilty, and expansion of clades from nation in the aftermath of the K-T event, which are somewhat the tropics fuels at least some recoveries, as well as biodiversity unexpected given that the extinction itself tended to increase dynamics during normal times. Incumbency effects apparently biotic homogenization on a global scale by preferentially remov- correlate more closely with extinction intensities than with stand- ing the more localized taxa. Invasions and extinctions are also ing diversities, so that regions with higher local and global extinc- important during times of ‘‘normal’’ extinction intensities, as I tions are more subject to invasion; the latest Cenozoic temperate will illustrate with reference to the dynamics of the latitudinal zones evidently received more invaders than the tropics or poles, diversity gradient. I will conclude with some implications for but this dynamic could shift dramatically if tropical diversity is integrating insights for past and present-day extinctions and strongly depleted. The fossil record can provide valuable insights, suggest that a powerful approach might involve comparative and their application to present-day issues will be enhanced by dissection in extinction patterns according to likely drivers. partitioning past and present-day extinctions by driving mecha- Throughout I will note gaps in our understanding that would nism rather than emphasizing intensity. benefit from combined study of modern and ancient systems. In this article, I will focus mainly on marine bivalves such as biogeography ͉ macroevolution ͉ recovery mussels, scallops, and cockles. Bivalves are becoming a model system for the analysis of large-scale biogeographic and evolu- he inventory of life on Earth has always been determined at tionary patterns (4, 9–14) for several reasons. They are taxo- Tthe most basic level by the difference between origination nomically rich but not unmanageable (Ϸ3,000 living and fossil and extinction. This fundamental macroevolutionary equation, ϭ Ϫ genera), and their systematics are increasingly understood, so richness origination extinction, has been formally applied in that taxonomic standardization and phylogenetic treatment of many ways and with many elaborations, but takes on special heterogeneous data are feasible. They have diverse life habits, consequence when attempting to evaluate the processes shaping from filter-feeding to photosymbiosis and chemosymbiosis to present-day biodiversity, where neither term in the right side of carnivory. They occur at all depths from the intertidal zone to the equation can be observed directly. Some progress has been deep-sea trenches and from the tropics to the poles. They are made in modeling these parameters, but most approaches in- abundant and often well preserved as fossils (although not all volve strong assumptions, require very large datasets and carry habitats and clades are equally represented; ref. 13). and they large uncertainties (e.g., refs. 1–3). The spatially explicit form of have diverse shell mineralogies and microstructures, which al- this equation, where richness is a local or regional pool of species lows analyses to control statistically for, and thus factor out, or higher taxa, and immigration and emigration terms enter the right side of the equation (4), is important in many situations, some, although not all, of the biases in the fossil record (12, 13). from the biotic response to Pleistocene climate cycles and These favorable attributes do not mean that the bivalve fossil ongoing climate changes to the recovery from mass extinctions. record is perfect, and preservation and sampling biases must However, this form is even more difficult to apply rigorously always be considered in large-scale analyses (see, for example, without historical data, and my emphasis here will be on the the variety of approaches in refs. 4 and 15–19). However, our fossil record. Few would argue against the idea that the spatial growing knowledge of living and fossil bivalves, including the fabric of extinction has shaped, and will continue to shape, the taxonomic, preservational, and geographic factors that can dis- biosphere in profound ways, but spatial effects have been neglected relative to temporal patterns (partly because docu- This paper results from the Arthur M. Sackler Colloquium of the National Academy of mentation is so challenging). I will argue that the insights Sciences, ‘‘In the Light of Evolution II: Biodiversity and Extinction,’’ held December 6–8, beginning to emerge from spatially explicit approaches to an- 2007, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and cient extinctions have significant implications for the dynamics of Engineering in Irvine, CA. The complete program and audio files of most presentations are diversity of the past and in the future. available on the NAS web site at www.nasonline.org/Sackler࿝biodiversity. This discussion will encompass a range of extinction intensities Author contributions: D.J. designed research, performed research, and wrote the paper. and focus on marine systems, where the fossil record is richest: The author declares no conflict of interest. application of these generalizations to terrestrial realms requires *E-mail: [email protected]. more study. Opinions are divided on whether the handful of mass © 2008 by The National Academy of Sciences of the USA 11528–11535 ͉ PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ suppl. 1 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0801919105 tort their fossil record, makes this group an excellent vehicle for 70 30 A Victims B integrating present-day and paleontological diversity dynamics. 60 25 Survivors 50 n=172 n=117 20 Extinction Selectivity Changes at the Most Extreme Events 40 15 30 A broad array of organismic and clade-level traits enter into 10 Frequency extinction risk for present-day species. For example, in evaluat- 20 Frequency 10 5 ing extinction risk in present-day terrestrial vertebrates, Purvis 0 0 and colleagues (20, 21, 22) found mixed, but significant, effects 13579111315 1 3 5 7 9 111315 for body size, a consistent inverse relation between both abun- Number of Provinces Number of Provinces dance and geographic range and extinction risk and either a C 0.8 D 35 positive relation or no effect for habitat specialization. Similar 0.7 2007 30 Rudists patterns are seen in the fossil record. For example, the geo- 0.6 25 (=pachyodont hinge) 0.5 graphic range is a significant determinant of Cretaceous and 20 0.4 Cenozoic molluscan species duration or survivorship (refs. 23 15 0.3 1995 and 24 and references therein), and Paleozoic crinoids show a 0.2 Frequency 10 significant positive relation between habitat breadth and species 0.1 5 Extinxtion Intensity Extinxtion 0 0 duration (25). Predictable interactions among factors can also be 12345678 13579111315 seen, although this aspect needs much more work. Molluscan Number of Provinces Number of Provinces genera containing many widespread species tend to be more Fig. 1. Spatial effects in the end-Cretaceous (K-T) mass extinction for marine extinction-resistant, with a median duration of 130 million years bivalve genera. (A, B, and D) Victims of the K-T extinction (A) tended to be (Myr), than genera having just a
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