Darwin's Bridge Between Microevolution & Macroevolution PDF

NATURE|Vol 457|12 February 2009|doi:10.1038/nature07894 REVIEW INSIGHT Darwin’s bridge between microevolution and macroevolution David N. Reznick1 & Robert E. Ricklefs2 Evolutionary biologist...

NATURE|Vol 457|12 February 2009|doi:10.1038/nature07894 REVIEW INSIGHT Darwin’s bridge between microevolution and macroevolution David N. Reznick1 & Robert E. Ricklefs2 Evolutionary biologists have long sought to understand the relationship between microevolution (adaptation), which can be observed both in nature and in the laboratory, and macroevolution (speciation and the origin of the divisions of the taxonomic hierarchy above the species level, and the development of complex organs), which cannot be witnessed because it occurs over intervals that far exceed the human lifespan. The connection between these processes is also a major source of conflict between science and religious belief. Biologists often forget that Charles Darwin offered a way of resolving this issue, and his proposal is ripe for re-evaluation in the light of recent research. Charles Darwin and Alfred Russel Wallace based their insight that organ- The keys to Darwin’s thinking about macroevolution are the ‘prin- isms evolve by natural selection on four principles1,2: first, that organisms ciple of divergence’ and extinction. In this Review, we consider how have “individual variations” that are faithfully transmitted from parent these principles have fared since the publication of On the Origin of to offspring; second, that all organisms produce more offspring than are Species1, and we discuss whether Darwin’s concept of the relationship required to replace themselves in the next generation; third, that limited between microevolution and macroevolution can provide useful insight resources create a “struggle for existence” that regulates population size, today. This relationship continues to generate controversy both within such that most offspring die without reproducing; and fourth, that the the biological sciences and in the confrontation between science and individuals that survive and reproduce are, on average, by virtue of their religion. On the 200th anniversary of Darwin’s birth, a status report is individual variations, better suited to their local environment than those surely in order. that do not. Given these four principles, evolution by natural selection (Darwin’s Divergence and extinction in 1859 ‘principle of descent with modification’) naturally follows. Such adap- Extinction was a hot topic during Darwin’s formative years. Many fos- tive modifications within populations over time are now referred to as sils had been found that were not identifiable as living organisms, but it microevolution. Darwin anticipated that microevolution would be a was not until the early nineteenth century that Georges Cuvier argued process of continuous and gradual change. that these fossils represented organisms that were extinct. A competing The term macroevolution, by contrast, refers to the origin of new hypothesis was that these creatures lived on in the vast (at that time) species and divisions of the taxonomic hierarchy above the species level, unexplored regions of the globe. When US President Thomas Jefferson and also to the origin of complex adaptations, such as the vertebrate eye. dispatched Meriwether Lewis and William Clark to explore the interior Macroevolution posed a problem to Darwin because his principle of of North America, he expected them to find living mammoths and mas- descent with modification predicts gradual transitions between small- todons, which he knew about from fossils. The French biologist Jean- scale adaptive changes in populations and these larger-scale phenomena, Baptiste Lamarck championed another alternative: that these fossil yet there is little evidence for such transitions in nature. Instead, the organisms, rather than being extinct, had evolved into contemporary natural world is often characterized by gaps, or discontinuities. One forms. Cuvier, who did not believe in evolution, based his thesis of extinc- type of gap relates to the existence of “organs of extreme perfection”, tion on detailed anatomical comparisons that emphasized differences such as the eye, or morphological innovations, such as wings, both of between fossil and living forms3. which are found fully formed in present-day organisms without leav- Darwin embraced Cuvier’s explanation and then extended it by pro- ing evidence of how they evolved. Another category is that species and posing that extinction was a by-product of evolution. Accordingly, as higher ranks in the taxonomic hierarchy are often separated by gaps organisms evolve under the struggle for existence, some species acquire without evidence of a transition between them. These discontinuities, superior adaptations and exclude other species through competition or plus the discontinuous appearance and disappearance of taxa in the fos- exploitation. In this way, extinction reflects the existence of a tipping sil record, form the modern conceptual divide between microevolution point in the ongoing struggle for existence. An increase in the severity and macroevolution (Box 1). of any factors that regulate population size can cause populations to Most evolutionary biologists think that Darwin explained macroevolu- decline in abundance and then disappear. tion simply as microevolution writ large. In fact, Darwin had rather more Darwin argued that the struggle for existence was caused by inter- to say about the relationship between microevolution and macroevolution actions among organisms and was the dominant factor that shaped how and invoked additional principles to define it. It is these additional princi- organisms evolve. He considered the physical environment to be of minor ples that are of interest here because they are often forgotten in discussions importance in evolution. Through his experience as a gardener and his of the relationship between microevolution and macroevolution. visits to the zoological park in London, he observed that organisms from 1 Department of Biology, University of California, Riverside, California 92521, USA. 2Department of Biology, University of Missouri - St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121, USA. 837 © 2009 Macmillan Publishers Limited. All rights reserved INSIGHT REVIEW NATURE|Vol 457|12 February 2009 Box 1 | A brief survey of macroevolution An undercurrent of the debate about the mechanisms of macroevolution It stands in opposition to species selection because macroevolution is whether natural selection (microevolution) is also the cause of emerges from microevolutionary processes. Simpson combined the macroevolution. Charles Darwin argued that, although natural selection idea of key adaptations, or changes that would allow organisms to is the sole mechanism that causes evolution, both divergence and expand into previously underutilized environments, with Sewall Wright’s extinction shape the larger-scale patterns that emerge from this process. theoretical models65 to explain the sudden appearance and expansion of successful lineages. Macromutations The key feature of Wright’s models is the adaptive landscape. Adaptive The initial phase of this debate focused on the expectation that change peaks are defined by a combination of characters that must appear caused by natural selection will cause continuous variation. It was argued together to define a well-adapted phenotype. Peaks are separated from that if natural variation — such as the distinction between species or one another by ‘valleys’, or character combinations that result in reduced ranks above species in the taxonomic hierarchy (for example, genera fitness. Wright’s models invoked the combination of natural selection, and families) — is discontinuous, then the underlying mechanism that genetic drift, mutation and migration, in allowing shifts between peaks. caused that change must also be discontinuous. Some championed Simpson adapted these models to a logical scenario for how a new lineage macromutation: the origination of a new species as a result of a single could be the product of accelerated peak-to-peak evolution. The fact that large mutation61. such evolution is accelerated and happens in a restricted geographical region means that it is unlikely to be seen in the fossil record. Punctuated equilibrium and species sorting Simpson later developed the concept of adaptive radiation17, which Two patterns of evolution revealed in the fossil record have been argued still stands as a competing explanation for species sorting because to be inconsistent with natural selection. such radiations are caused by natural selection and can account for First, Stephen Jay Gould and Niles Eldredge observed that the detailed differences among lineages in the rate of diversification (see the history of individual lineages reveals prolonged intervals with little or no section ‘Update on divergence’). change (equilibrium or stasis) interspersed with intervals of rapid change (punctuations) that are associated with the origin of new species62. They Heterochrony proposed that natural selection could fine-tune organisms during periods Particular types of natural selection and adaptive response have been of stasis but that another mechanism had to account for punctuated credited with the potential to cause rapid morphological evolution. Gould66 change. Second, the fossil record often reveals species sorting, meaning championed heterochrony, or changes in the rate of development of one that some lineages rapidly diversify into new species whereas others component of an organism relative to others, as a mechanism for the rapid decline. Gould argued for species selection as the mechanism to explain evolution of descendent species that are a mixture of juvenile and adult both phenomena63. Species selection treats species as the unit of characters in their ancestors. One hypothesis for the origin of vertebrates selection in the same way that natural selection treats individuals as is that they are derived from a tunicate-like ancestor that had an actively the unit of selection. swimming larval stage with a nerve cord, but then metamorphosed into adults that lost these characters. A common ancestor of the vertebrates Megaevolution and adaptive radiation could evolve from such a tunicate-like ancestor with the deletion George Gaylord Simpson’s proposed mechanism of ‘megaevolution’64 of metamorphosis and the retention of these larval characters into was a modern synthesis (1930s–1950s) proposal for how natural adulthood. The adults of such a descendent species would not be readily selection can combine with other processes to explain species sorting. identifiable as being closely related to the adult life stage of its ancestor. a diversity of climates could survive and reproduce perfectly well when If it is accepted that reproductive isolation between species is a pre- transported to England, so their natural distributions were not limited by requisite for divergence, then Darwin’s principle must be modified their climate tolerance. Instead, their distributions were shaped by their so that the initial stages of diversification do not involve interactions ability to disperse and by the presence of other species. For Darwin, the between individuals or between closely related populations. This con- interactions that define the struggle for existence and shape how organ- dition does not invalidate Darwin’s principle that divergence and extinc- isms evolve were diverse, including competition, predation, parasitism, tion are often a consequence of interactions among close relatives; it disease and pollination. This same range of interactions can therefore merely delays the action of the principle until the reproductively isolated contribute to extinction. descendants of a common ancestral lineage begin to interact. Darwin’s principle of divergence derives from what he thought to be one Darwin illustrated the combined action of his principle of descent of the most potent components of the struggle for existence. He argued that with modification, the principle of divergence, and extinction in the strongest interactions would be among individuals within a population the only figure in On the Origin of Species (Fig. 1). It showed the link or among closely related populations or species, because these organisms between microevolution and macroevolution. Each branch in the evo- have the most similar requirements. Darwin’s principle of divergence pre- lutionary tree of life is seen as sprouting ‘buds’ that are emerging var- dicts that the individuals, populations or species most likely to succeed in ieties or locally distinct populations. These buds are the consequence the struggle are those that differ most from their close relatives in the way of the overproduction of offspring whose individual variations allow they achieve their needs for survival and reproduction. them to outcompete others or to probe the environment for open eco- The principle of divergence has had strong detractors. Ernst Mayr logical space. Most of these buds go extinct, but some persist, becom- singled it out as a failed theory4. His reasoning paralleled his argument ing modified and improved descendants that tend to drive their close that On the Origin of Species is not about the origin of species5. Darwin relatives to extinction, or to fill the unoccupied ecological space. saw each species as an arbitrary point on a continuum of populations According to Darwin, this combination of replacement and diver- that are diverging from one another as a consequence of evolution by gence causes cladogenesis: the splitting of one ancestral species into natural selection. For this reason, he saw the principle of divergence as more than one descendant. Continued divergence of form and function acting among individuals within a population or among populations or between genetically isolated species causes the branches of the tree of species. He did not distinguish between these levels of interaction. The life to grow ever farther apart, separated from one another by what crucial contribution of Theodosius Dobzhansky6 and Mayr5 to the mod- seem to be unbridgeable gaps. Darwin argued that the processes of ern synthesis was to recognize that speciation involves both divergence diversification and extinction can explain the gaps that are seen and the origin of discontinuity, or reproductive isolation. Mayr argued among living species. Divergence pushes lineages apart, and extinc- that individuals within a population cannot diverge from one another tion erases the bridge that once joined them, creating the appearance of because they are part of an interbreeding gene pool4. discontinuity. 838 © 2009 Macmillan Publishers Limited. All rights reserved NATURE|Vol 457|12 February 2009 REVIEW INSIGHT How has Darwin’s proposal for the relationship between microevolution phenotypic diversity within a rapidly multiplying lineage. It occurs when a and macroevolution fared since its publication in On the Origin of Species? single ancestor diverges into a host of species that use a variety of environ- Here we evaluate three conditions necessary for the structural integrity of ments and that differ in traits used to exploit those environments.” Adap- Darwin’s proposed bridge between microevolution and macroevolution. tive radiations are commonly associated with diversification in sparsely First, some speciation events should be associated with the divergence of occupied ecological space, for example following the colonization of a ecologically relevant characteristics among descendent lineages; second, remote island, the survival of a mass extinction event, or the crossing of an at least some extinction events should be attributed to interactions among adaptive barrier to open new evolutionary opportunities. Competition for closely related species; and third, extinction of some lineages should be resources has been shown to have had a dominant role in some adaptive linked to the diversification of closely related lineages. radiations12,16. Perhaps the most famous is the evolution of 13 species of geospizine finches (Darwin’s finches) within the Galapagos archipelago. Update on divergence The birds’ diverse body sizes, beak shapes and diets are all derived from The principle of divergence has never been an explicit subject of analysis, a single common ancestor that colonized an almost bird-free island12,13. but its imprint can be found in the early development of evolutionary ecol- Diversification within the much larger areas of continents undoubtedly ogy, when it was established that closely related organisms could inhabit proceeds in the same way for many types of organism. the same environment only if they differed in morphology, habitat use or In the absence of a fossil record, the radiation of any living group some other characteristics that reduced their ecological similarity7. Such of organisms can be visualized by reconstructing the evolutionary rel- observations fostered the idea that competition among close relatives had ationships among the living species in a lineage to create a phylogeny19, a significant role in shaping communities8–10. Character displacement, or usually from DNA sequence data. This approach derives from models the evolution of increased dissimilarity among species whose geographi- for lineage diversification that were originally developed in the palae- cal ranges overlap11, provides a natural experimental test of the hypothesis ontological literature20. As well as defining the patterns of relatedness that selection favours individuals in each species that diverge further from among species, phylogenies can yield more specific information about the ecological requirements of the other species. Such displacement has the tempo and possible mode of evolution that underlies contemporary now been well characterized in a variety of organisms12–16. diversity19,21–24. The baseline for such analyses is the temporal distribu- Darwin’s principle of divergence also figures prominently in the process tion of branching points in the phylogeny, which allows certain inferen- of adaptive radiation, as originally proposed by George Gaylord Simpson17 ces about rates of speciation and extinction in the past19,25, although there and as defined by Dolph Schluter18 as “the evolution of ecological and are sources of uncertainty and bias in doing this26,27. Figure 1 | Darwin’s view of the link between microevolution and labelled with lower-case letters and numerical superscripts, represent macroevolution. This figure appears in chapter 4 of Darwin’s On the distinct descendent subspecies or species. The descendants seen at each Origin of Species. The x axis represents a hypothetical ecological variable. time horizon are not simply modified versions of their immediate ancestor The y axis represents time. Each horizontal line, associated with roman but new and improved organisms that outcompeted their parental lineage numerals I to XIV, represents a long but unspecified interval of time. A to and drove it to extinction. Thus a2 is not just a1 1,000 generations later; it is L are 11 species in a hypothetical genus. Two of these species (A and I) a daughter lineage that outcompeted a1. If there is more than one surviving diversify over time, whereas eight become extinct. One species (F) does lineage at a node, the survivors tend to be the ones most different from one not diversify but has surviving descendants, and it represents what Darwin another. For example, a1 and m1 are the most divergent populations derived described as “living fossils” — slowly evolving lineages that survived from A at the end of the first time interval, and these are the ones that in marginal habitats where they were shielded from interactions with survive. As each lineage diversifies, its descendants fan out along the x axis, more rapidly diversifying lineages. At each intersection between the occupying progressively more ecological space. They do so at the expense diversifying lineages and the divisions in time, the lineage is represented of the species that lie closest to them on the x axis, which become extinct, by diverging dashed lines, which are varieties that differ from one another presumably because they lost out in competition for resources. (Figure in characteristics and habitat use. Most of these become extinct. Some, reproduced from ref. 1.) 839 © 2009 Macmillan Publishers Limited. All rights reserved INSIGHT REVIEW NATURE|Vol 457|12 February 2009 a One common pattern is for a lineage to diversify rapidly early in W. citrina S. ruticilla its history, followed by a progressive slowing in the rate of diversifi- D. kirtlandii cation21,28–30 (Fig. 2). Such a density-dependent cladogenesis21,24 stems 0.74 D. tigrina from an initial rapid adaptive radiation that fills the ecological space * D. cerulea left open by a mass extinction, for example, or from a spread into a new * P. americana adaptive zone facilitated by the evolution of some trait that makes the 0.75 * P. pitiayumi D. magnolia zone more accessible17,31. The resultant decline in available ecological D. fusca space constrains further diversification. 0.71 0.35 * D. castanea As Darwin envisaged in his principle of divergence, rapid diversific- * D. petechia ation often ensues when a lineage evolves adaptations that enable it to D. striata *0.82 D. pensylvanica breach an ecological barrier32. Examples include the repeated invasion 0.72 D. caerulescens of brackish water environments by the ancestors of the different lineages of D. palmarum mangrove plants33, the invasion of temperate environments by lineages of * D. coronata trees that evolved freezing tolerance34–36, and the radiation of skinks that * * D. dominica D. pinus occupied the expanding deserts of Australia as the climate became more * 0.84 D. discolor arid37. Timothy Barraclough and colleagues summarize other radiations * D. nigrescens that have been associated with the evolution of key innovations38. Such * D. graciae radiations also occur on a much grander scale: for example, bats diversi- D. virens * * D. chrysoparia fied from a single ancestor that evolved flight into the largest order of * D. occidentalis mammals with more than 1,100 species39. * D. townsendi Analyses of diversification sometimes reveal other details that are con- sistent with Darwin’s macroevolution theory. For example, the passerine birds include many depauperate lineages that occupy ecologically or geographically marginal habitats40,41. These lineages seem to have diver- b 32 sification and extinction rates that are an order of magnitude lower than those of more species-rich clades of passerines, and thus correspond to Darwin’s lineage F (Fig. 1), a slowly diversifying lineage isolated from interactions with more rapidly diversifying lineages. Certainly, Darwin’s principle of divergence has been supported by a range of what are now well-characterized and generally accepted 10 evolutionary phenomena. Lineages Update on extinction Analyses of extinction in the fossil record have been dominated by the discovery of mass extinction events and the later realization that the mass 3.1 extinctions represent the tail of a distribution of mostly smaller events. Mass extinctions have external causes, including bolide (large crater- forming projectile) impacts, major tectonic events and global climate change42,43. These extinctions appear as discrete events involving multiple species and are unrelated to Darwin’s proposed mechanism of extinction. Indeed, Darwin’s interactive extinctions lie hidden in the background 1 of these events. Modern analyses also almost invariably deal with the 5 4 3 2 1 0 appearance and disappearance of genera or families in the fossil record, as Time before present (million years) species can rarely be distinguished among fossils, although it is the extinc- Figure 2 | A plot of lineage through time. This ‘lineage through time’ tion of populations or species that is most relevant to Darwin’s principle (LTT) plot is based on the temporal distribution of branch points in a of divergence. However, even though the fossil record may not be fertile phylogenetic tree. a, Phylogenetic tree for North American wood warblers ground for evaluating Darwin’s proposed mechanism, species-level origi- based on more than 9 kb of mitochondrial and nuclear intron DNA nations and extinctions can be identified for some periods and some taxa, sequence. Species are mainly Dendroica spp. but are also from the genera such as the recent fossil record for marine bivalves44, and inferences can Parula, Wilsonia and Setophaga. The branch lengths are proportional be drawn about Darwin’s proposed mechanism of extinction. to absolute time. Branch points marked with asterisks are supported by Analyses of extinction in living organisms fall almost exclusively in the a posterior probability (Bayes’ theorem) of >0.95. Numbers at the other province of conservation biology. Primary causes of extinction in this branch points are exact probabilities. b, The LTT plot derived from this phylogeny. The y axis shows the number of lineages; the x axis shows the context include introduced predators and competitors, climate change, estimated time before present. The solid line represents the absolute value and habitat destruction, with the consequent subdivision of once- of the log of the number of ancestral lineages (different branches) present widespread populations into small isolates. Current research focuses at each time interval. The shading is the 95% confidence interval for the on defining those properties of species that can predict susceptibility to number of lineages. The dashed line is what would be seen if the existing extinction, such as geographical range, population density, life history species were the product of a constant rate of diversification with no and trophic level45–47. Many of the causes and correlates of contemporary extinction. Note that the rate of accumulation of new lineages is initially extinctions have the signature of Darwin’s emphasis on biotic interac- high and then levels off. The slope of the lineage-accumulation curve tions and the tipping of the balance of factors that regulate population represents the net rate of diversification, which is the rate of formation size. For example, small geographical range, low population density and of new lineages minus the rate of loss of lineages by extinction. Dan occupation of a high trophic level often figure as significant correlates Rabosky and Irby Lovette show that this pattern can be explained only by a high initial speciation rate followed by a deceleration in the rate of a high risk of extinction. Small changes in the factors that normally of diversification60. This pattern is consistent with density-dependent regulate population size can tip the balance towards extinction for species speciation, or the early diversification of the lineage as it filled the available that are already less abundant or have restricted distributions. Many of ecological space before being constrained by resource limitation. (Figure these factors involve interactions with other species. Although the causes reproduced, with permission, from ref. 30.) of current extinctions often lie outside the natural processes envisaged 840 © 2009 Macmillan Publishers Limited. All rights reserved NATURE|Vol 457|12 February 2009 REVIEW INSIGHT by Darwin, many of them, such as the impact of invasive species, are taxa27,58. This pattern suggests an underlying equilibrium between spe- enhanced versions of natural processes. ciation and extinction during these intervals24,29. Perhaps speciation and Recent work on West Indian birds provides an unusual opportunity extinction are random, unconnected events that balance out over time. to observe progressive stages of ecological and geographical contrac- However, models of random speciation and extinction processes suggest tion leading to extinction, using inferences from current geographical that the average time required for the complete replacement of species ranges and DNA-based phylogenies. Birds that colonize islands embark is approximately the product of the number of species and the average on sequential phases of range expansion and contraction, referred to duration of individual species. The duration of species can be estimated as a taxon cycle48,49. Recent colonists are genetically indistinguishable directly from the fossil record31 and, more recently, from the analysis of from their mainland source populations, occupy wide geographical dis- phylogenies24,26. These estimates, which typically fall between 1 million tributions and live mainly in lowland habitats50. Older, genetically dif- and 10 million years, are far too long for random speciation and extinc- ferentiated, populations occur on one or a few islands, often restricted tion to account for observed species turnover rates27. Instead, more to forested environments at higher elevations. Each species provides a rapid turnover of species can be reconciled only when some lineages snapshot of this process, leading from the initial occupation of open, exhibit an excess of speciation and others an excess of extinction. Only lowland habitats, to expansion into forested montane environments and a direct link between the two is needed to support Darwin’s mechanism exclusion from lowland habitats by new colonists. As they adapt to island of macroevolution. interiors, older taxa also become isolated into small populations that are susceptible to local extinction. This process of cycling, with a con- Conclusions sequent increase in the probability of extinction, fits well with Darwin’s Although Darwin might have erred in some of the details of his prin- concept of extinction being driven by biotic interactions. Such support ciple of divergence, particularly the generally agreed starting point of from the study of contemporary extinctions is understandably limited, reproductively isolated species, his basic idea has merit. The fundamen- but evidence should begin to accumulate more rapidly with the recent tal truth of his principle of divergence has emerged in different facets of availability of molecular tools for investigating population history. evolutionary ecology, a field in which the same principle, in the form Darwin’s proposal for the cause of extinction has yet to be fairly evalu- of character displacement or some models of sympatric speciation, was ated. He suggested that many taxa are driven to extinction by competi- discovered independently in different contexts over a century after the tion from ecologically similar but adaptively superior groups undergoing publication of On the Origin of Species. Darwin’s linking of extinction diversification. This core assumption of Darwin’s explanation for macro- to diversification did not re-emerge as the study of extinction rose to evolution has little empirical support, mainly because the search for prominence in conservation biology. Competitive replacement leading appropriate evidence has fallen through the gap between evolution and to extinction was once generally and uncritically accepted by palaeon- ecology; of course, pertinent evidence would strongly resist discovery tologists before fading into the background after the discovery of mass under any circumstance. extinctions. There is compelling evidence, however, of a role for biotic interactions in at least some extinction events, and a complementary Bringing divergence and extinction together relationship between divergence and extinction finds enough support Central to Darwin’s explanation for macroevolution is that the suc- for Darwin’s proposal to merit further consideration as a viable link cess of one group is gained at the expense of another. Palaeontological between microevolution and macroevolution. studies often reveal replacements in the fossil record, but their tem- Darwin’s proposal carries a more general message for contemporary poral, spatial and taxonomic resolution is generally limited. Research discussions of macroevolution, namely that microevolution alone can- on faunal replacements tends to focus on biotic changes associated with not explain macroevolution. Understanding macroevolution requires major changes in the Earth’s environment, such as the mid-Tertiary the integration of ecology, evolution and the role of history in shaping the temperature decrease and the increasing aridity at temperate latitudes. diversification or decline of lineages. Other investigators, most recently For example, Christine Janis and co-workers documented the Miocene David Jablonski59, have conveyed similar messages. Jablonski’s vision is replacement of browsing mammals by grazers in North America and more complex than Darwin’s and reflects the growth of ecology, evolu- attributed it to replacement of forest by grasslands51. Jin Meng and Mal- tion and palaeontology as disciplines since 1859, but it retains Darwin’s colm McKenna documented a similar Eocene–Oligocene replacement emphasis on the presence of a biological filter that lies between micro- on the Mongolian plateau — where a perissodactyl-dominated mam- evolution and macroevolution and shapes the long-term consequences malian fauna occupying a forested landscape was replaced by a rodent- of evolutionary change. Jablonski concludes by calling for increased and lagomorph-dominated grassland fauna — in association with the integration between fields to build a bridge between microevolution uplift of the Himalayas and the Tibetan plateau52. and macroevolution, and we concur with him. Mass extinctions and More direct evidence of continual background replacement of species the large-scale expansions and contractions of clades in the fossil record comes from long fossil sequences with reasonable taxonomic resolution, are captivating but are only part of the story. Background extinctions such as the 40-million-year Palaeocene-to-Miocene record of pollen are more elusive, but they must be considered in order to understand morphotypes from northwestern South America documented by Carlos Darwin’s mechanism of the turnover of species resulting from their Jaramillo and colleagues53. Although environment and overall diversity evolution and interactions. Studies of extant populations — including both varied over this period, the morphospecies composition of the flora mechanisms of population regulation, the contemporary causes of turned over continually, even during periods of relative climate stabil- extinction and the causes of adaptive radiations — can yield important ity. More marked examples of such changes in the fossil record include clues to factors that shape the history of life. Finally, information about the low-latitude replacement of gymnosperms by angiosperms dur- the historical patterns of diversification of lineages can now be mined ing the mid-Cretaceous54,55, and the post-Eocene replacement of non- from molecular phylogenies, shedding light on the underlying causes passerine birds by passerines in Europe56. In both cases, older groups of these patterns. It is the integration of information from the fossil were replaced almost completely by more modern groups, leaving only record, the population and evolutionary dynamics of extant organisms, sporadic relicts of the biotas — the Podocarpaceae and Gnetum in the and phylogenetics that will provide the ultimate test of Darwin’s bridge case of gymnosperms, and swifts and woodpeckers, among others, in between microevolution and macroevolution. the case of European birds. Many people see On the Origin of Species as a beautiful fossil, but Additional indirect evidence for Darwin’s theory of diversification and we view it as a living document that continues to offer insights and extinction comes from the observation that, following recovery from to enlighten modern research. It contains a wealth of ideas that have mass extinction events, species richness remains relatively stable. This slipped through the cracks of the modern synthesis and, when appropri- pattern appears in the fossil record57 and is evident in the absence of a ately updated, can provide inspiration for addressing some of the major correlation between clade age and contemporary diversity in several unanswered questions in evolutionary biology. 841 © 2009 Macmillan Publishers Limited. All rights reserved INSIGHT REVIEW NATURE|Vol 457|12 February 2009 1. Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of 37. Rabosky, D. L., Donnellan, S. C., Talaba, A. L. & Lovette, I. J. Exceptional among-lineage Favoured Races in the Struggle for Life (John Murray, 1859). variation in diversification rates during the radiation of Australia’s most diverse vertebrate This book is essential reading for those who wish not only to understand evolution in clade. Proc. R. Soc. B 274, 2915–2923 (2007). general but also to see the wealth of Darwin’s original ideas that have yet to be tested. 38. Barraclough, T. G., Vogler, A. P. & Harvey, P. H. Revealing the factors that promote 2. Wallace, A. R. On the tendency of varieties to depart indefinitely from the original type. speciation. Phil. Trans. R. Soc. Lond. B 353, 241–249 (1998). J. Proc. Linn. Soc. (Zool.) 3, 53–62 (1858). 39. Freeman, P. W. Macroevolution in Microchiroptera: recoupling morphology and ecology 3. Rudwick, M. J. S. Bursting the Limits of Time (Univ. Chicago Press, 2005). with phylogeny. Evol. Ecol. Res. 2, 317–335 (2000). This book provides the best explanation for how it became evident that fossils represent 40. Ricklefs, R. E. Global diversification rates of passerine birds. Proc. R. Soc. Lond. B 270, the history of life and how the geological timescale was developed. 2285–2291 (2003). 4. Mayr, E. Reasons for the failure of theories. Phil. Sci. 61, 529–533 (1994). 41. Ricklefs, R. E. Small clades at the periphery of passerine morphological space. Am. Nat. 165, 5. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, 1942). 651–659 (2005). 6. Dobzhansky, T. Genetics and the Origin of Species (Columbia Univ. Press, 1937). 42. Raup, D. M. & Sepkoski, J. J. Mass extinctions in the marine fossil record. Science 215, 7. MacArthur, R. H. Geographical Ecology (Princeton Univ. Press, 1972). 1501–1503 (1982). 8. MacArthur, R. H. & Levins, R. The limiting similarity, convergence, and divergence of 43. Raup, D. M. A kill curve for Phanerozoic marine species. Paleobiology 17, 37–48 (1991). coexisting species. Am. Nat. 101, 377–386 (1967). Reference 42 presents the discovery of the most dramatic mass extinctions, whereas 9. Vandermeer, J. H. Niche theory. Annu. Rev. Ecol. Syst. 3, 107–132 (1972). reference 43 presents a more general analysis of the distribution of extinction events 10. Chase, J. M. & Leibold, M. A. Ecological Niches. Linking Classical and Contemporary throughout the fossil record. Approaches (Univ. Chicago Press, 2003). 44. Smith, J. T. & Roy, K. Selectivity during background extinction: Plio-Pleistocene scallops in 11. Brown, W. L. & Wilson, E. O. Character displacement. Syst. Zool. 5, 49–65 (1956). California. Paleobiology 32, 408–416 (2006). This paper is a benchmark in the birth of evolutionary ecology and the first formal 45. Owens, I. P. F. & Bennett, P. M. Ecological basis of extinction risk in birds: habitat loss versus restatement of Darwin’s principle of divergence. human persecution and introduced predators. Proc. Natl Acad. Sci. USA 97, 12144–12148 12. Lack, D. Darwin’s Finches (Cambridge Univ. Press, 1947). (2000). 13. Grant, P. R. Convergent and divergent character displacement. Biol. J. Linn. Soc. 4, 39–68 46. Jones, K. E., Purvis, A. & Gittleman, J. L. Biological correlates of extinction risk in bats. (1972). Am. Nat. 161, 601–614 (2003). 14. Losos, J. B. A phylogenetic analysis of character displacement in the Caribbean Anolis 47. Cardillo, M. et al. The predictability of extinction: biological and external correlates of lizards. Evolution 44, 558–569 (1990). decline in mammals. Proc. R. Soc. Lond. B 275, 1441–1448 (2008). 15. Schluter, D. & McPhail, J. D. Ecological character displacement and speciation in 48. Wilson, E. O. The nature of the taxon cycle in the Melanesian ant fauna. Am. Nat. 95, sticklebacks. Am. Nat. 140, 85–108 (1992). 169–193 (1961). 16. Losos, J. B. Ecological character displacement and the study of adaptation. Proc. Natl Acad. 49. Ricklefs, R. E. & Cox, G. W. Taxon cycles in the West Indian avifauna. Am. Nat. 106, 195–219 Sci. USA 97, 5693–5695 (2000). (1972). 17. Simpson, G. G. The Major Features of Evolution (Columbia Univ. Press, 1953). 50. Ricklefs, R. E. & Bermingham, E. The concept of the taxon cycle in biogeography. Glob. Ecol. 18. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000). Biogeogr. 11, 353–361 (2002). In this paper, Schluter updates Simpson’s concept of adaptive radiation and integrates it 51. Janis, C. M., Damuth, J. & Theodor, J. M. Miocene ungulates and terrestrial primary with the modern evidence for such radiations. productivity: where have all the browsers gone? Proc. Natl Acad. Sci. USA 97, 7899–7904 19. Harvey, P. H., May, R. M. & Nee, S. Phylogenies without fossils. Evolution 48, 523–529 (2000). (1994). 52. Meng, J. & McKenna, M. C. Faunal turnovers of Palaeogene mammals from the Mongolian 20. Raup, D. M., Gould, S. J., Schopf, T. J. M. & Simberloff, D. S. Stochastic models of phylogeny plateau. Nature 394, 364–367 (1998). and evolution of diversity. J. Geol. 81, 525–542 (1973). 53. Jaramillo, C., Rueda, M. J. & Mora, G. Cenozoic plant diversity in the Neotropics. Science 21. Nee, S., Mooers, A. O. & Harvey, P. H. Tempo and mode of evolution revealed from 311, 1893–1896 (2006). molecular phylogenies. Proc. Natl Acad. Sci. USA 89, 8322–8326 (1992). 54. Crane, P. R. & Lidgard, S. Angiosperm diversification and paleolatitudinal gradients in 22. Nee, S., May, R. M. & Harvey, P. H. The reconstructed evolutionary process. Phil. Trans. R. Cretaceous floristic diversity. Science 246, 675–678 (1989). Soc. Lond. B 344, 305–311 (1994). 55. Lidgard, S. & Crane, P. R. Angiosperm diversification and Cretaceous floristic trends; 23. Pybus, O. G. & Harvey, P. H. Testing macro-evolutionary models using incomplete a comparison of palynofloras and leaf macrofloras. Paleobiology 16, 77–93 (1990). molecular phylogenies. Proc. R. Soc. Lond. B 267, 2267–2272 (2000). 56. Mayr, G. The Paleogene fossil record of birds in Europe. Biol. Rev. 80, 515–542 (2007). 24. Nee, S. Birth–death models in macroevolution. Annu. Rev. Ecol. Syst. 37, 1–17 (2006). 57. Alroy, J. et al. Phanerozoic trends in the global diversity of marine invertebrates. Science 25. Harvey, P. H., Holmes, E. C. & Nee, S. Model phylogenies to explain the real world. Bioessays 321, 97–100 (2008). 16, 767–770 (1994). 58. Magallón, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. 26. Ricklefs, R. E. Estimating diversification rates from phylogenetic information. Trends Ecol. Evolution 55, 1762–1780 (2001). Evol. 22, 601–610 (2007). 59. Jablonski, D. Biotic interactions and macroevolution: extensions and mismatches across 27. Ricklefs, R. E. in Speciation and Patterns of Diversity (eds Butlin, R., Bridle, J. & Schluter, D.) scales and levels. Evolution 62, 715–739 (2008). 257–277 (Cambridge Univ. Press, 2009). 60. Rabosky, D. L. & Lovette, I. J. Explosive evolutionary radiations: decreasing speciation or 28. Ricklefs, R. E. Evolutionary diversification and the origin of the diversity–environment increasing extinction through time? Evolution 62, 1866–1875 (2008). relationship. Ecology 87, S3–S13 (2006). 61. Mayr, E. The Growth of Biological Thought (Harvard Univ. Press, 1982). 29. Phillimore, A. B. & Price, T. D. Density-dependent cladogenesis in birds. PLoS Biol. 6, 62. Gould, S. J. & Eldredge, N. Punctuated equilibria: the tempo and mode of evolution 483–489 (2008). reconsidered. Paleobiology 3, 115–151 (1977). 30. Rabosky, D. L. & Lovette, I. J. Density-dependent diversification in North American wood 63. Gould, S. J. The Structure of Evolutionary Theory (Harvard Univ. Press, 2002). warblers. Proc. R. Soc. Lond. B 275, 2363–2371 (2008). 64. Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1944). 31. Stanley, S. M. Macroevolution, Pattern and Process (Freeman, 1979). 65. Wright, S. Character, change, speciation and higher taxa. Evolution 36, 427–443 (1982). 32. Wiens, J. J. & Donoghue, M. J. Historical biogeography, ecology, and species richness. This paper is ideal reading for those who wish to learn more about the debate on the Trends Ecol. Evol. 19, 639–644 (2004). relationship between microevolution and macroevolution. 33. Ricklefs, R. E., Schwarzbach, A. E. & Renner, S. S. Rate of lineage origin explains the diversity 66. Gould, S. J. Ontongeny and Phylogeny (Harvard Univ. Press, 1977). anomaly in the world’s mangrove vegetation. Am. Nat. 168, 805–810 (2006). 34. Latham, R. E. & Ricklefs, R. E. Global patterns of tree species richness in moist forests: Acknowledgements We thank M. Clark, N. Hughes, D. Rabosky and J. Sachs for energy-diversity theory does not account for variation in species richness. Oikos 67, comments on the manuscript. D.N.R. is supported by grants from the National 325–333 (1993). Science Foundation (grant numbers DEB-0416085 and DEB-0623632). 35. Judd, W. S., Sanders, R. W. & Donoghue, M. J. Angiosperm family pairs: preliminary phylogenetic analyses. Harv. Pap. Bot. 5, 1–51 (1994). Author Information Reprints and permissions information is available at 36. Ricklefs, R. E. in Tropical Rainforests: Past, Present, and Future (eds Bermingham, E., www.nature.com/reprints. The authors declare no competing financial interests. Dick, C. W. & Moritz, C.) 16–40 (Univ. Chicago Press, 2005). Correspondence should be addressed to D.N.R. ([email protected]). 842 View publication stats © 2009 Macmillan Publishers Limited. All rights reserved