Biodiversity and Extinction

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In the light of evolution II: Biodiversity and extinction

John C. Avise*†, Stephen P. Hubbell‡, and Francisco J. Ayala*† *Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697; and ‡Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095

he Earth’s biodiversity is a well- (from species-area curves and other evi- extend to many kinds of terrestrial, spring for scientific curiosity dence) to taxa that undoubtedly are aquatic, and marine organisms. The arti- about nature’s workings. It is disappearing even before they can be cles under this heading, and the next, also a source of joy and inspira- identified and studied. Nevertheless, illustrate some of the challenges of Ttion for inquisitive minds, from poets to they do reveal the general magnitude of quantifying the magnitude of extant philosophers, and provides life-support the ongoing extinction crisis. For many biodiversity and deciphering extinction services. According to Kellert (2), biodi- species that manage to avoid extirpation, rates and patterns in a representative versity affords humanity nine principal local and regional populations are being selection of diverse contemporary types of benefit: utilitarian (direct eco- decimated. biotas. nomic value of nature’s goods and ser- The modern extinction crisis is Oceans cover three-quarters of the vices), scientific (biological insights), prompting scientific efforts on many Earth’s surface, and their inhabitants aesthetic (inspiration from nature’s fronts. Systematists are striving to de- might seem at first thought to be some- beauty), humanistic (feelings deeply scribe biodiversity and reconstruct the what buffered (compared with terrestrial rooted in our inherent attachment to Tree of Life. Ecologists are mapping the and freshwater species) against anthro- other species), dominionistic (physical distributions of biodiversity and global pogenic disturbance. However, Jeremy and mental well-being promoted by hotspots that merit special conservation Jackson (6) compiles evidence from four some kinds of interactions with nature), attention. Paleontologists are placing the major marine realms—estuaries and moralistic (including spiritual uplifting), current crisis in temporal context with coastal areas, continental shelves, open naturalistic (curiosity-driven satisfaction regard to the Earth’s long geological ocean pelagic zone, and coral reefs— from the living world), symbolic (nature- history, and also to the recent history of that marine ecosystems are under ex- stimulated imagination, communication, human impacts on biodiversity across treme duress from the oft-synergistic and thought), and even negativistic timescales ranging from decades to mil- effects of habitat destruction, overfish- (fears and anxieties about nature, which lennia. Educators and concerned scien- ing, introduced species, warming and can actually enrich people’s life experi- tists are striving to alert government acidification, toxins, and nutrient runoff. ence). Whether or not this list properly leaders, policy makers, and the public to One common result has been the degra- characterizes nature’s benefits, the fact the biodiversity crisis. Conservation ef- dation of biodiverse marine ecosystems is that a world diminished in biodiversity forts (including those by many nongov- with complex food webs capped by an would be greatly impoverished. ernment organizations) are underway to abundance of top-echelon predators into Many scientists have argued that, as a slow the pace of biological extinctions. simplified biotic communities increas- consequence of human activities, the However, unless conservation achieve- ingly dominated by smaller animals, al- Earth has entered the sixth mass extinc- ments accelerate quickly, the outlook gae, and microbes. Among the many tion episode (and the only such event for biodiversity in and beyond the 21st ramifications have been the economic precipitated by a biotic agent) in its century remains grim. collapse of numerous marine fisheries 4-billion-year history (3, 4). The last cat- The goals of this Colloquium were to and massive degradation of coral reefs astrophic extinction, which occurred synthesize recent scientific information that formerly rivaled tropical rainforests Ϸ65 million years ago and was the coup- and ideas about the abundance and dis- in terms of spatial coverage and biotic de-grace for non-avian dinosaurs, marine tribution of biodiversity and to compare richness. The data paint a disturbing ammonites, and many other evolution- contemporary biodiversity and extinc- picture about current and projected eco- ary lineages, happened rather suddenly tion patterns with those in the distant after a large asteroid slammed into the and near evolutionary past as well as logical states for the world’s oceans. planet. Today, most of the biotic holo- with those plausible in the near-term David Wake and Vance Vredenburg caust is due—directly or indirectly—to future. Articles from the Colloquium (7) describe a similarly gloomy scenario local, regional, and global environmen- address biodiversity and extinction in for the global status of amphibians. Of tal impacts from a burgeoning human four contexts: Contemporary Patterns population. The first phase of the cur- and Processes in Animals; Contemporary Ϸ This paper serves as an introduction to this PNAS supple- rent extinction episode started 50,000– Patterns and Processes in Plants and ment, which resulted from the Arthur M. Sackler Collo- 100,000 years ago, when modern Microbes; Trends and Processes in the quium of the National Academy of Sciences, ‘‘In the Light of humans began dispersing around the Paleontological Past; and Prospects for Evolution II: Biodiversity and Extinction,’’ held December planet. The second phase started 10,000 the Future. 6–8, 2007, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, years ago with further population in- CA. It is the second in a series of colloquia under the general creases and land-use changes associated Contemporary Patterns and Processes title ‘‘In the Light of Evolution’’ (see Box 1). The complete with the invention of agriculture. A in Animals program and audio files of most presentations are avail- third phase of environmental alteration There is no doubt that humans are the able on the NAS web site at www.nasonline.org/ Sackler࿝biodiversity. Papers from the first colloquium in the and biodiversity loss was ushered in by root cause of most ecosystem stresses series, titled ‘‘In the Light of Evolution I: Adaptation and the industrial revolution. E. O. Wilson and biotic extinctions in the modern Complex Design,’’ appeared in ref. 1. (5) estimated that the Earth is currently world. Negative human pressures on Author contributions: J.C.A., S.P.H., and F.J.A. wrote the losing Ϸ0.25% of its remaining species biodiversity occur via pollution, intro- paper. per year (such that at least 12,000 spe- ductions of alien species, overexploita- The authors declare no conflict of interest. cies may be going extinct annually). tion, landscape transformations, and †To whom correspondence may be addressed. E-mail: Such estimates are educated guesses be- other factors. Like the asteroid impact [email protected] or [email protected]. cause they represent extrapolations 65 million years ago, human impacts © 2008 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802504105 PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ suppl. 1 ͉ 11453–11457 Downloaded by guest on September 30, 2021 the Ϸ6,300 extant species of frogs, extant biodiversity that is parasitic. The and Steven Gaines (11) examine histori- salamanders, and caecilians, at least authors conclude that Ϸ10–15% of par- cal records from islands around the one-third are currently threatened with asitic helminthes (Trematoda, Cestoda, world to ask whether native plant spe- extinction, and many more are likely to Acanthocephala, and Nematoda) are at cies likewise often have gone extinct become so in the near future. A dra- risk of extinction by virtue of being de- when exotic plants were introduced and matic worldwide decline in amphibian pendent on threatened or endangered became naturalized. The answer seems populations was first noticed in the late species of vertebrate host. They also to be a clear no, at least yet. One possi- 1980s. Several ecological factors includ- conclude that parasite species diversity bility is that native plant species on is- ing habitat degradation and climatic does not map linearly onto host species lands are accumulating an extinction changes probably are involved, but so diversity and that approximately three- debt that will be paid in future species too is an unanticipated, recently uncov- quarters of all links in food webs involve losses; alternatively, the number of na- ered threat: an emerging virulent dis- a parasitic species. These findings pro- tive plus exotic plants on islands may ease (chytridiomycosis) caused by a vide a sobering reminder that the cur- reach a stable equilibrium or saturation pathogenic fungus. The source of this rent extinction pulse is affecting many point that is much higher than the en- fungus and its mode of spread are kinds of organisms (not just the conspic- demics alone had been able to achieve. poorly understood, but the disease (per- uous megafauna) and that extinction The authors examine the evidence perhaps in synergy with other ecological processes could therefore have many taining to these competing hypotheses factors) has devastated amphibian popu- unforeseen ramifications for ecosystem and explore the ramifications for future lations in such distant sites as the Amer- operations. plant biodiversity on islands depending icas and tropical Australia. Whatever on which scenario proves to be more the proximate and ultimate causes of Contemporary Patterns and Processes in nearly correct. the ongoing amphibian extinctions, the Plants and Microbes trend is especially disturbing because The task of tallying extant species and amphibians otherwise have been quint- The anthropogenic introduction of alien estimating extinction risks can be daunt- essential evolutionary survivors that species is perhaps second only to habitat ing even for relatively well studied bio- managed to persist across several earlier loss as a cause of recent and ongoing tas. Such scientific exercises can also be mass extinction events in the Earth’s species extinctions. The problem is espe- highly informative, as Stephen Hubbell history. cially acute on oceanic islands, where et al. (12) illustrate by applying neutral Biodiverse coral reefs are among the countless native animals have gone ex- biodiversity theory (13) to estimate the most threatened ecological systems on tinct after the arrival of humans and number, abundance, range size, and ex- Earth. Approximately 70% of coral their hitchhiking associates. Dov Sax tinction risk (under alternative scenarios reefs globally have been degraded beyond recognition in recent years (20%), are in imminent danger of collapse (24%), or are under longer-term threat Box 1. In the Light of Evolution. In 1973, ture, pharmacology, and biotechnol- of demise (26%) (8). Marjorie Reaka et Theodosius Dobzhansky penned a ogy. The ramifications of evolutionary al. (9) survey reef-dwelling stomatopods short commentary titled ‘‘Nothing in thought extend into learned realms tra- (a large group of marine crustaceans) as biology makes sense except in the light ditionally reserved for philosophy and a model taxon to assess global hotspots of evolution’’ (25). Most scientists religion. The central goal of the In the of extant biodiversity, endemism, and agree that evolution provides the uni- Light of Evolution series will be to extinction risk, the intent being to iden- fying framework for interpreting bio- promote the evolutionary sciences tify evolutionary sources and sinks of logical phenomena that otherwise can through state-of-the-art colloquia and stomatopod diversity, infer driving often seem unrelated and perhaps un- their published proceedings. Each in- mechanisms, and provide an additional intelligible. Given the central position stallment will explore evolutionary focus for conservation and management of evolutionary thought in biology, it is perspectives on a particular biological efforts on coral reefs. Stomatopod spe- sadly ironic that evolutionary perspec- topic that is scientifically intriguing but cies diversity (like that of several other tives outside the sciences have often also has special relevance to contem- reef-dwelling marine taxa) is highest in been neglected, misunderstood, or pur- porary societal issues or challenges. the Indo-Australian Archipelago, gradu- posefully misrepresented. Biodiver- Individually and collectively, the In the ally declines eastward across the central sity—the genetic variety of life—is an Light of Evolution series will aim to Pacific, and shows a secondary peak of exuberant product of the evolutionary interpret phenomena in various areas species richness in the southwestern In- past, a vast human-supportive resource of biology through the lens of evolu- dian Ocean. From these and other data (aesthetic, intellectual, and material) tion, address some of the most intel- (related to body size, ecology, and spa- of the present, and a rich legacy to lectually engaging as well as pragmat- tial pattern of endemism), the authors cherish and preserve for the future. ically important societal issues of our explain how a ‘‘merry-go-round’’ evolu- Two challenges, as well as opportuni- times, and foster a greater appreciation tionary model might account for the ties, for 21st-century science are to gain of evolutionary biology as a consoli- differential dynamics of species origin deeper insights into the evolutionary dating foundation for the life sciences. and extinction in different ocean regions. processes that foster biotic diversity The organizers and founding editors Extinctions in the ongoing biodiversity and to translate that understanding of this effort (J.C.A. and F.J.A.) are the crisis apply not only to free-living organ- into workable solutions for the regional academic grandson and son, respectively, isms but also to their parasites. Andy and global crises that biodiversity cur- of Theodosius Dobzhansky, to whose Dobson et al. (10) address the possible rently faces. A grasp of evolutionary fond memory this In the Light of Evolu- magnitude of this problem by reviewing principles and processes is important in tion series is dedicated. May Dobzhan- estimates of the total number of para- other societal arenas as well, such as sky’s words and insights continue to in- sitic species on Earth (with special education, medicine, sociology, and spire rational scientific inquiry into reference to helminthes that parasitize other applied fields including agricul- nature’s marvelous operations. vertebrate animals) and the fraction of

11454 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802504105 Avise et al. Downloaded by guest on September 30, 2021 of future habitat loss) for medium- and community functionally redundant to associated with the size of the geo- large-sized trees in the Amazon Basin. the original? Based on the authors’ liter- graphic range of genus-level clades. Their quantitative analysis suggests that ature review, the answers to these ques- From this and other evidence, the au- Ͼ11,000 tree species inhabit this ex- tions usually seem to be ‘‘no,’’ ‘‘no,’’ and thor’s take-home message is that spatial traordinarily biodiverse region. The ‘‘no.’’ Allison and Martiny emphasize that considerations are fundamental to un- good news for biodiversity conservation all such conclusions remain provisional derstanding the evolutionary dynamics is that Ͼ3,000 of these species have pending further research of this nature, of biodiversity, including a clade’s sus- large population sizes and therefore are and they suggest several promising empiri- ceptibility to extinction and its potential likely to persist well into the future cal and conceptual approaches. for recovery and expansion after a mass (barring catastrophic climatic or other extinction event. These findings have environmental changes). The bad news Trends and Processes in the ramifications for the current biodiversity is that for the large class of rare Amazo- Paleontological Past crisis because human activities are alter- nian trees (Ͼ5,000 species likely to con- Extinction has always been a part of life ing the geographic distributions of many sist of Ͻ10,000 individuals each) esti- on Earth and is the ultimate fate of all taxa around the world. mated near-term extinction rates are species. Rates of extinction have varied John Alroy (18) uses information 37% and 50%, respectively, under opti- across time, from standard or ‘‘back- from a recent web-based ‘‘Paleobiology mistic and nonoptimistic projections ground’’ rates to occasional mass events. Database’’ to revisit classical questions concerning ongoing deforestation prac- The articles in this section place the cur- about the marine fossil record, such as: tices by humans. rent biodiversity crisis in temporal per- Do biotic turnovers occur in pulses that With regard to tallying numbers of taxa spective by scrutinizing the fossil record coincide with the boundaries between and characterizing local, regional, or for patterns and processes of extinction geological intervals? Did extinction rates global patterns of biodiversity, microbes in the distant and near past. decline during the Phanerozoic? Are offer even stiffer challenges than many The fossil record traditionally has been biotic extinction rates more volatile than plant and animal taxa. Jessica Bryant and interpreted to register five episodes of origination rates? Do large-scale extinc- colleagues associated with Jessica Green wholesale biotic change so severe as to tions exhibit a 26-myr periodicity as (14) tackle such problems on a mesogeo- qualify as mass extinctions: at the end of some have claimed? Were the ‘‘Big graphic scale by applying DNA sequence the Ordovician (Ϸ440 mya), Devonian Five’’ mass extinction events qualita- data (from the 16S ribosomal gene) and (370 mya), Permian (245 mya), Triassic tively distinct from lesser extinction epi- other information to questions about mi- (210 mya), and Cretaceous (65 mya). sodes? Alroy’s provisional answers to crobial biodiversity along an elevational Each was characterized (indeed identified) some of these questions are unorthodox. habitat gradient in the Colorado Rocky by a substantial loss of then-extant taxa. For example, he suggests that the Big Mountains. Bacterial taxon richness along Douglas Erwin (16) reexamines these five Five are merely the upper end of a con- their climatic-zone transect decreases mass extinction events in terms of the re- tinuous spectrum of extinction intensi- monotonically from lower to higher alti- spective impacts on each of seven metrics ties, such that it is ‘‘a matter of taste tudes, and detectable phylogenetic struc- of biodiversity—taxonomic diversity, phy- whether to speak of the Big Five, the ture (nonrandom spatial clustering of logenetic diversity, morphologic disparity, Big Three, or just the Big One. . . ’’. The related taxa) occurs at all elevations. In functional diversity, architectural diversity, analyses yield empirical estimates of typi- comparable analyses of plants along the behavioral complexity, and developmental cal recovery times from mass extinctions. same gradient, the authors uncovered diversity—which potentially capture differ- Alroy concludes that the rebound from qualitatively different outcomes with re- ent aspects of the loss of evolutionary his- the ongoing mass extinction will probably gard to both taxon richness and species tory. Erwin reports that the canonical take between 15 and 30 million years, if assemblage. These findings indicate that mass extinctions differed with respect to past mass extinction events are any guide. whatever ecological and evolutionary their impacts on these various metrics. For Moving closer to the present time, forces shape microbial communities, the example, the end-Permian extinction had late-Quaternary extinctions heavily im- biodiversity patterns will not always mirror major consequences for essentially all di- pacted large mammals especially. The those in macrobiota. mensions of global biodiversity whereas last 50,000 years were witness to the ex- An important follow-up issue for mi- the end-Ordovician extinction heavily im- tinction of approximately two-thirds of crobial (or other) taxa is whether the pacted morphologic disparity but had low all genera and one-half of all species of composition of natural communities pre- or medium effects on several other biodi- mammal weighing Ͼ44 kg (about the dictably influences the responses of versity measures. The biodiversity fallout size of a sheep). Causal factors for this those communities to environmental from mass extinction events can vary both megafaunal extinction have been much alteration. Traditionally, microbial com- quantitatively and qualitatively, and the debated, with a leading hypothesis being munities often have been treated as nature of each extinction influences the human hunting (overkill) arguably aug- ‘‘black boxes’’ in functional ecological rate and pattern of evolutionary recovery mented by habitat alteration and climate models, a situation that Steve Allison from the catastrophe. change. Anthony Barnosky (19) exam- and Jennifer Martiny (15) would like to David Jablonski (17) develops a ines the situation from the fresh per- see rectified. These authors review ex- somewhat similar theme by emphasizing spective of historical tradeoffs in bio- periments and observations from the the selectivity of mass extinctions with mass. An inverse relationship between scientific literature to address questions respect to potential risk factors such as human biomass and nonhuman about the composition of a microbial body size, species richness, and geo- megafaunal biomass indicates that be- community after exposure to environ- graphic range. From a consideration of fore the mass extinction the energy mental perturbations. Is the microbial the fossil record for marine organisms needed to construct large animals was community resistant to the disturbance (especially bivalve mollusks), the author divided among many species, whereas (tend not to change in taxonomic com- concludes that every mass extinction after the extinction much more of the position)? Is it resilient (change in event seems to show some degree of planet’s total supply of energy became makeup but then return quickly to the selectivity, but also that disproportion- concentrated in one species (Homo sapi- predisturbance condition)? If an altered ately high clade survivorship during ens) and its domesticates. Based on the composition is sustained, is the new mass extinction episodes is consistently historical chronologies of biomass transi-

Avise et al. PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ suppl. 1 ͉ 11455 Downloaded by guest on September 30, 2021 tions in various parts of the world, Bar- logenetic information from a recently been slow to materialize and inadequate nosky draws several biological implica- completed Tree of Life for mammals to steward global biodiversity through tions, including how the current with ecological, life history, and geo- the crucial 21st century. One major rea- depletion of fossil fuels as an energy graphic data to examine the origins and son is the general lack of understanding source may translate into near-future current distributions of mammalian and engagement on biodiversity issues challenges for global biodiversity. biodiversity. Results from the analysis by the public, which in polls typically indicate that evolutionary cradles of ori- ranks environmental concerns below Prospects for the Future gin have shifted over time and that ex- other challenges such as terrorism, the Armed with evidence from the past and tinction risks vary according to the type economy, and family values. Novacek present about global patterns and pro- of mammal (e.g., large-bodied versus analyzes this state of affairs and argues cesses of extinction, what can be pro- small-bodied) and also to spatial and tem- that effective ways must be found to tailor jected for global biodiversity in the near poral differences (often region-specific) in biodiversity messages to each target au- and distant future? Articles in this section threat intensity. The authors discuss rami- dience. Enlightened environmental mea- address several of the many challenges fications of such phylogenetic findings for sures by corporations and democratic presented by the ongoing extinction cri- the near- and long-term future of mam- governments will be achieved only if the sis, both for the biodiversity sciences per malian biodiversity, including how alter- ‘‘power of the people’’ is marshaled in se and for efforts to translate the science native criteria (different ‘‘currencies of favor of conservation efforts. into an enhanced societal awareness that conservation’’) might be used in setting In the closing article of this Collo- might spawn effective conservation poli- preservation priorities. quium, Paul Ehrlich and Robert Pringle cies and actions. Before the mid-20th century, scientific (24) remind us that ‘‘the fate of biologi- Conventional wisdom has been that analyses of biodiversity rested on ap- cal diversity for the next ten million ecologically important traits (such as an praisals of organismal phenotypes. That years will be determined during the next ability to withstand cold climates) are situation changed dramatically when 50–100 years by the activities of a single too evolutionarily labile to be of much molecular techniques were introduced species’’ (Homo sapiens). With the pro- utility in phylogenetic inference. Michael that permitted direct assays of geno- jected increase by mid-century of 2.6 Donoghue (20) challenges this paradigm types. The molecular revolution in evo- billion people to an already over- by reviewing several cases in which lutionary biology has provided powerful crowded planet, the prospects for preserving substantial biodiversity are dim, higher plant taxa have retained, for long tools for biodiversity assessments ranging unless societal mindsets and comport- periods of evolutionary time, particular from species identifications and phylog- ments change dramatically and quickly. traits that impact their geographic distri- eny reconstructions to genetic dissec- The authors issue a pluralistic call for butions. Donoghue calls this phenome- tions of ontogeny. Projecting forward, action on seven fronts: combat the non ‘‘phylogenetic niche conservatism.’’ John Avise (22) describes three oppor- underlying drivers of biodiversity loss His basic idea is that the geography of tunities for the field of biodiversity ge- (notably human population growth, biodiversity at any horizon in time re- netics that seem not to have been widely overconsumption, and the use of malign flects an interaction between phyloge- appreciated or discussed: use informa- technologies); promote permanent na- netic legacy (as registered in the evolved tion from the emerging phylogenetic ture reserves; provide social and eco- ecological characteristics of particular Tree of Life to erect the first-ever uni- nomic incentives to preserve wild lineages) and contemporary ecological versally standardized scheme of biologi- populations; better align economies selection pressures. This worldview im- cal classification; identify biogeographic with conservation; restore biodiversity plies that evolutionary shifts from one hotspots and centers of origin (including on currently degraded lands; vest human ecological setting to another cannot be those tracing to the late-Tertiary) for occupants of a region with the desire readily accomplished by many plant various extant biotas; and engage in ed- and capacity to protect nature; and, in taxa, especially if substantial genetic ad- ucational outreach by conveying to stu- general, fundamentally transform human justments in physiology are required. dents and the public a sense of wonder attitudes toward nature and biodiversity. Thus, newly opened niches are more likely and appreciation for the marvelous work- These calls are ambitious, but positive to be filled by immigrants from ecologi- ings of nature, many of which are being societal responses to them are not yet cally similar zones than by in situ evolu- revealed for the first time by genetic ap- beyond the realm of possibility. tion of local populations. Donoghue praisals. Capitalizing on these opportuni- The current extinction crisis is of hu- addresses some ramifications of phyloge- ties should be instructive for basic science man making, and any favorable resolu- netic niche conservatism for the future of and also helpful in conservation efforts. tion of that biodiversity crisis—among plant biodiversity in the face of global cli- Michael Novacek (23) expands on the the most dire in the 4-billion-year his- mate change and habitat fragmentation. public-outreach mission for conservation tory of the Earth—will have to be initi- In a somewhat similar vein, Jonathan biology by emphasizing the need to ated by mankind. Preserving biodiversity Davies and colleagues associated with awaken a broad audience to the ongoing is undeniably in humanity’s enlightened the Andy Purvis group (21) show how a biodiversity crisis. Despite the urgency self-interest, but the tragic irony is that phylogenetic modeling approach can of current environmental problems, and a majority of humanity is not yet en- help to identify mammalian taxa whose committed efforts (albeit by relatively lightened to this fact. Little time re- intrinsic biology might make them espe- small segments of society) over the past mains for the public, corporations, and cially vulnerable to environmental 20 years to find solutions, national and governments to awaken to the magni- pressures. They begin by combining phy- international responses to date have tude of what is at stake.

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