Naturwissenschaften (2005) 92:1–19 DOI 10.1007/s00114-004-0586-9 REVIEW L. D. Martin · T. J. Meehan Extinction may not be forever Published online: 16 November 2004 Springer-Verlag 2004 Abstract Here we review the phenomenon of ecomorph Introduction evolution and the hypothesis of iterative climatic cycles. Although a widely known phenomenon, convergent evo- Here we review the hypothesis of iterative climatic cy- lution has been underappreciated in both its scope and cles, which states that the evolution of faunas and floras commonality. The power of natural selection to override and their extinction has a predictable pattern. South genealogy to create similar morphologies (even among American pollen and North American mammalian as- distantly related organisms) supports classical Darwinian semblages exhibit convergent evolution in repeating A-B- evolution. That this occurs repeatedly in stratigraphically C cycles (van der Hammen 1957, 1965; Martin 1985; closely spaced intervals is one of the most striking features Meehan and Martin 2003), and these consecutive A-B-C of Earth history. Periodic extinctions followed by re- communities form a chronofauna. The stability and then evolution of adaptive types (ecomorphs) are not isolated extinction of these communities have been correlated to occurrences but are embedded within complex ecological cycling sedimentary and temperature profiles. This pat- systems that evolve, become extinct, and repeat them- tern is reflected in simultaneous radiations of convergent selves in temporal synchrony. These complexes of radia- adaptive types (ecomorphs) on separate continents, indi- tion and extinction bundle the biostratigraphic record and cating that it results from natural selection caused by provide the basis for a global stratigraphy. At this scale, global climatic change, as opposed to genetic or com- climatic change is the only mechanism adequate to explain munity biotic factors. An iterative pattern of hierarchical the observed record of repeating faunas and floras. Un- climatic cycles may form the underlying basis for bios- derstanding of the underlying causes may lead to predic- tratigraphy and explain most evolutionary trends and tive theories of global biostratigraphy, evolutionary pro- extinctions. The cycles recognized so far appear to re- cesses, and climatic change. present equal units of time—2.4 Ma for each A, B, and C cycle, and 7.2 Ma for this chronofauna triplet. Whether the cycles represent equal units of time is integral to understanding the cause of these cycles, but is not integral to the main thrust of the argument; repeating ecomorph evolution and extinction among different lineages occurs synchronously, and only climatic change has broad en- ough effects to produce this pattern. L. D. Martin ()) It would be very important to establish that climatic Natural History Museum and Biodiversity Research Center, change and evolutionary processes, including extinction, Department of Ecology and Evolutionary Biology, University of Kansas, are due to random historical accidents, but it would also 1345 Jayhawk Blvd, Lawrence, KS 66045–7561, USA be a scientific dead end. A predictive model of climatic e-mail: [email protected] change and correlated evolutionary processes is obviously Fax: +1-785-8645335 much more desirable, but can such a model be con- structed? While the basis of stratigraphy and almost all T. J. Meehan geology is the Law of Superposition, we must use fossils Division of Science, Chatham College, Buhl Hall, Woodland Rd, Pittsburgh, PA 15232–9987, USA to construct a regional or global stratigraphy. The units of biostratigraphy are unique combinations of last and first T. J. Meehan appearances of organisms. If such events were randomly Research Associate, distributed over the rock column, boundaries would result Carnegie Museum of Natural History, solely from historical accidents, and these boundaries Pittsburgh, Pennsylvania, USA 2 might change with the whims of prevailing academic these changes will have a global signature. Some version politics. It seems obvious that it would be better if a of this scenario must lie at the root of biostratigraphy. boundary corresponded to a recognizable global event. A climatic-evolutionary connection seems fundamental to biostratigraphy, and Krasilov (1974) advocated a climat- Ecomorphs ic-based system in his causal biostratigraphy. He impli- cated overall ecological change as the key to under- The similarities among organisms are a greater theoretical standing biostratigraphy and stated that the succession of problem than differences. Differences can and should ecosystems is controlled by climatic cycles. This implies result from random events over time. Historical accidents that there are bundles of time that can be recognized on come into full play when we examine how organisms the basis of unique biological compositions and the im- differ, but how are we to explain characters that are pact of climate on the sedimentary record. There is a conserved over vast intervals of geologic time? We see school of thought that claims that there is no visible ev- immense amounts of conserved similarity in genetic idence for climatic impact on evolution (e.g., Prothero composition and cellular processes over the hundreds of 1999; Alroy 2000), but most workers see a clear con- millions of years that organisms have inhabited Earth. nection, and Darwinian evolution seems to demand such a Without the action of natural selection, such similarities result. There are numerous studies of modern organisms would soon have fallen prey to random processes. There correlating climate and adaptation, and natural selection are also not an infinite number of solutions to biological resulting from climatic change has been observed in a problems. In fact the number of solutions seems to be three-decade study of Darwin’s finches (Grant and Grant quite small judging from the number of times that the 2002). From the fossil record, we have empirical evidence same solution is evolved independently. A computer that climate changes over time and that biota are directly simulation of “organisms” shows that with strong selec- affected. For instance, Europe was fully tropical in the tion, convergent evolution of even a complex trait is Middle Eocene, as evidenced by the famous deposits at common (Lenski et al. 2003). Natural selection produces Messel where we find rainforest trees and animals whose suites of coordinated similarity resulting from shared closest analogues are in Africa today (Schaal and Ziegler activities, rather than shared phylogeny. If the shared 1988), while fossils of 18,000 years ago indicate a tundra activity is an integral part of an “ecological occupation,” flora and fauna (von Koenigswald and Hahn 1981). The it may predict other similarities related to that occupation. overall global trend during the past 55 Ma has been to- Cuvier’s great contribution to comparative anatomy was wards cooling, but we are presently experiencing a re- the principle of correlation—the idea that changes in one versal of that trend. There is relatively little evidence of anatomical suite required concordant changes in others long periods of climatic stasis, and all long-term patterns and that a lifestyle could be predicted from a subset of are interrupted by periodic fluctuations where the general correlated structures. It is this ability of ecological posi- trend is reversed. tion to predict anatomy independent of phylogeny that is The usual measures for climatic regime are tempera- the basis of the ecomorph concept (Martin and Naples ture and its effects as expressed in terms of water. Hot 2002). worlds are wet worlds because of increased energy and Convergent organisms have been called ecomorphs water surface area for evaporation, while cold worlds are (ecological morphotypes; Williams 1972), which can be dry. Wet worlds favor canopy strategists (trees) and cold correlated to Van Valen’s (1971) adaptive zone—an or- worlds pioneering plants and open vegetational structures ganism’s resource space together with relevant predation (Martin 1994). Wet worlds favor sedimentary deposition and parasitism. An important property of adaptive zones with increased plant cover and a higher base level, is that they exist as opportunities within the ecological whereas dry worlds are characterized by increased ero- framework and are defined by specific resources. The sion. Climate is mediated locally, and it is possible for a existence of an adaptive zone creates an opportunity for local region to be dry when global averages are wetter. the development of a specialized organism to occupy it, Ultimately weather patterns are interconnected, and cli- but does not require or imply that such an organism exists mate cannot change greatly over any large region without (Martin and Naples 2002). Simpson (1953:161) antici- affecting all regions. Usually environmental change is bad pated this view: “Possible ways of life are always re- for established organisms. Changing rainforest to grass- stricted in two ways: the environment must offer the land may be bad for monkeys, while changing grassland opportunity and a group of organisms must have the to forest may be bad for wildebeest. Global change is possibility of seizing this opportunity.” Ecologies contain likely to have a negative impact on organisms best opportunities that define circumscribed morphologies, adapted to the status quo. On the other hand, organisms including physiology and behavior. Convergent forms that occupy marginal