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Macroevolution Is More Than Repeated Rounds of Microevolution

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Macroevolution Is More Than Repeated Rounds of Microevolution EVOLUTION & DEVELOPMENT 2:2, 78–84 (2000) Macroevolution is more than repeated rounds of microevolution Douglas H. Erwin Department of Paleobiology, MRC-121, National Museum of Natural History, Washington, DC 20560, USA Correspondence (email: [email protected]) SUMMARY Arguments over macroevolution versus micro- discontinuities impose a hierarchical structure to evolution evolution have waxed and waned through most of the twenti- and discredit any smooth extrapolation from allelic substitu- eth century. Initially, paleontologists and other evolutionary tion to large-scale evolutionary patterns. Recent develop- biologists advanced a variety of non-Darwinian evolutionary ments in comparative developmental biology suggest a need processes as explanations for patterns found in the fossil to reconsider the possibility that some macroevolutionary dis- record, emphasizing macroevolution as a source of morpho- continuites may be associated with the origination of evolu- logic novelty. Later, paleontologists, from Simpson to Gould, tionary innovation. The attractiveness of macroevolution reflects Stanley, and others, accepted the primacy of natural selec- the exhaustive documentation of large-scale patterns which tion but argued that rapid speciation produced a discontinuity reveal a richness to evolution unexplained by microevolution. between micro- and macroevolution. This second phase em- If the goal of evolutionary biology is to understand the history phasizes the sorting of innovations between species. Other of life, rather than simply document experimental analysis of discontinuities appear in the persistence of trends (differen- evolution, studies from paleontology, phylogenetics, devel- tial success of species within clades), including species sort- opmental biology, and other fields demand the deeper view ing, in the differential success between clades and in the provided by macroevolution. origination and establishment of evolutionary novelties. These INTRODUCTION duced by differential sorting of species within lineages, or differential sorting between lineages, where lineages with Since all evolutionary change involves intraspecific modifi- predation-resistant morphologies are more successful, a cation and speciation, in a trivial sense, macroevolution macroevolutionary process. It is unclear whether a micro- could be reducible to microevolution. The novel associations evolutionary null model should be preferred to a hierarchical of morphological characters and developmental processes one (on any basis but personal preference), and in the ab- recognized as phyla did not arise through some processes of sence of sufficient data there is no way to resolve the issue. “phylization,” but through speciation. At issue is not the ef- The distinction is real, however, and is subject to empirical ficacy of natural selection (contrary to some misunderstand- evaluation. ings, e.g., Dawkins 1996), but whether the larger scale pat- Physicists ignore the actions of individual atoms because terns in the history of life simply reflect the accumulation of the generalities that produce physical laws are exhibited by microevolutionary events over long spans of time, or whether collections of atoms. Similarly, ecologists have recognized a more inclusive view of evolutionary processes is required. that the analysis and experimental perturbation of local com- In particular, paleontologists and other macroevolutionists munities, while useful, blinds them to processes exhibited at point to a range of phenomena that suggest discontinuities broader spatial and temporal scales (e.g., Brown 1995; Mau- between microevolution and some forms of speciation, and rer 1999). These ecological generalities are not apparent at in the interactions within and between clades. more circumscribed levels of analysis, yet they reveal the Vermeij’s (1987, 1994) documentation of the morpho- significance of processes operating beyond the scope of tra- logical changes induced in gastropods since the Jurassic by ditional ecological studies. Patterns of community structure the action of shell-crushing predators, particularly crabs, and regional differences in biodiversity, immigration, and could simply be the manifestation of numerous, individual local extinction each emerge at the level of macroecology. microevolutionary trends. Narrow apertures, spines, and Unlike statistical physics, however, where laws derive from other antipredatory defenses may have become widespread a statistical summation of individual behavior, the emergent while many once common but susceptible morphologies properties of macroecology and macroevolution reflect a hi- vanished through natural selection extended through the Me- erarchical structure and the importance of different scales of sozoic. The same trend, however, could also have been pro- process and analysis. © BLACKWELL SCIENCE, INC. 78 Erwin Macroevolution versus microevolution 79 Paleontologists have proposed a number of patterns and poration of paleontology into the Modern Synthesis. Reject- processes that suggest a hierarchical structure to the evolu- ing the macromutationist views of Goldshmidt, Schinde- tionary process, with explicit discontinuities between levels wolf, and others, Simpson noted: “Macro-evolution involves (see particularly Gould 1985; Bennett 1997). Such disconti- the rise and divergence of discontinuous groups, and it is still nuities may exist at the level of speciation, with the most debatable whether it differs in kind or only in degree from widely discussed example being punctuated equilibrium, micro-evolution. If the two proved to be basically different, and in the generation of trends, particularly those within the innumerable studies of micro-evolution would become clades through differential success of species. The formation relatively unimportant and would have minor value in the of larger-scale patterns of differential success of clades study of evolution as a whole.” (1944, p. 97) through long spans of time may constitute a further disconti- Simpson’s macroevolution emphasized the origin of spe- nuity. Finally, the empirical distribution of evolutionary cies and genera, while he coined the term mega-evolution for novelties through time suggests that the origin of evolution- the origin of higher taxonomic categories. In his view, the ary innovation may be distinct from much of traditional mi- discontinuities between larger groups were of far greater croevolution. I begin with a brief discussion of macroevolu- evolutionary significance than between species and genera. tion and then consider each of the discontinuities noted Simpson also defined quantum evolution as a rapid shift above, and the generation of evolutionary novelties. from one adaptive zone to another through genetic drift, dif- fering in both rate and kind from speciation and phyletic evo- lution. Yet in 1953 he rejected this view, suggesting that WHAT IS MACROEVOLUTION? quantum evolution is simply a rapid form of phyletic evolu- tion (see Gould 1980, 1994). Simpson’s views remained the The term macroevolution was introduced by Iurii Fil- major statement on macroevolution for the following two de- ipchenko, a Russian geneticist and developmental biologist cades, although the subject received relatively little attention and mentor of Theodosius Dobzhansky. Filipchenko distin- during the 1960s. guished between Mendelian inheritance within species and The concept of punctuated equilibrium led to a renewal of non-Mendelian, cytoplasmic inheritance responsible for the interest in macroevolution with the claim that speciation of- formation of taxa above the species level. In contrast to latter ten imposed a fundamental discontinuity between phyletic views, speciation was not seen as the crux of the distinction evolution and the formation of species. Since Cuvier in the between micro- and macroevolution, since Filipchenko saw 1820s and Phillips in the 1840s, paleontologists had recog- speciation as continuous with microevolutionary change nized that species appear suddenly in the fossil record, often (Alexandrov 1994). The discontinuity lay above this level: show no directional morphologic change during their exist- “. the origin of the characters [that differentiate the] higher ence, and then disappear, frequently to be replaced by systematic categories [requires] some other factors than does closely related species. Paleontologists had discounted the the origin of the lower taxonomic units” (Filipchenko 1927, evolutionary significance of these observations by invoking p. 91, cited by Burian 1994, p. 134). Filipchenko’s views the incompleteness of the fossil record, slavishly following meshed with the later efforts of such macromutationists as the example of Darwin in the Origin of Species. But El- Osborne and Goldschmidt. dredge and Gould (1972) asserted that the fossil record was Dobzhansky (1937) introduced macroevolution to En- not sufficiently incomplete to produce the observed pattern glish-speaking evolutionists but decisively rejected any dis- as an artifact (since confirmed by many analyses, e.g., Hol- continuity between micro- and macroevolution. Dobzhansky land and Patzkowsky 1999; Foote et al. 1999). They argued appears to have been agnostic about the potential of macro- that speciation occurred rapidly, in events, and that any mor- evolution and in an oft-cited passage wrote: “. there is no phological change between events had little influence on way toward an understanding of the mechanisms of macro- speciation (see Erwin and
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