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Key Innovations and the Ecology of Macroevolution

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Key Innovations and the Ecology of Macroevolution PERSPECTIVES tata (aardvarks) are not and probably never have been particularly diverse Key innovations and the ecology of either morphologically or taxonomically; nevertheless, aardvarks possess key char- macroevolution acters that have essentially committed them to eating colonial insects, a way of John P. Hunter life quite different from other ‘subungu- lates’5. Traditional (‘evolutionary’) sys- The origin or evolutionary ‘success’ of taxa is often attributed to key innovations – tematists would recognize the distinctive- aspects of organismal phenotype that promote diversification. Different ways of ness of aardvarks by placing them in their delimiting taxa and measuring ‘success’ (i.e. number or longevity of species, own order. If macroevolution is con- morphological variety or differential control of energy) give rise to different ideas of cerned with such ‘character-state transi- how key innovations might operate. Key innovations may enhance competitive tions that diagnose evolutionary differ- ability, relax adaptive trade-offs or permit exploitation of a new productive resource ences of major taxonomic rank’6 (e.g. base. Recent key innovation studies comparing species richness in extant sister between the order Tubulidentata and clades may miss important observations possible only with consideration of the fossil other mammalian orders), then key inno- record, traditional higher taxa and phenotypic diversity. vations should occupy a central place in the study of macroevolution. John P. Hunter is at the Dept of Anatomy, New York College of Osteopathic Medicine, Historically, the rug might have been Old Westbury, NY 11568, USA. pulled out from under the key innovation concept with the decline of evolutionary systematics and the rise of phylogenetic ey innovations are aspects of organis- taxa3,4, specifically to explain how higher systematics. When systematists began to K mal phenotype important to the ori- taxa arise in terms of population level pro- group species into holophyletic (mono- gin or subsequent success of a taxonomic cesses. Miller3 used the origin of ground- phyletic sensu stricto) clades rather than group. This concept is controversial, how- foraging thrashers from among tree- higher taxa, investigators of macroevolu- ever, because it is difficult to test hy- foraging mockingbirds as a case study of a tion shifted their focus from the biological pothesized key innovations1 and because taxon (genus Toxostoma) originating from differences between groups to the differ- researchers understand the concept in within another (genus Mimus) and de- ential performance of clades, most easily different ways (see Box 1). Nevertheless, scribed the differentiation in digging ability measured as numbers of species. Because the various definitions of key innovation among thrashers as a possible ‘genus in many traditional higher taxa are paraphy- share the basic idea that some attributes of the making’. The acquisition of simple, but letic, unacceptable within phylogenetic sys- organisms have been important over evolu- functionally important, changes in beak tematics, many macroevolutionists viewed tionary time. The concept links autecology form makes possible the appearance of the biological distinctiveness of higher taxa and macroevolution, or more specifically, sets of birds (thrashers and mockingbirds) as a partial result of an arbitrary classifi- the summed performance of individuals with different functional abilities and eco- cation7. On the other hand, differences in and the performance of a taxonomic group logical tendencies. Traditional systemati- the number of species between clades to which the individuals belong. When cists would recognize the adaptive and could be investigated as the result of properly investigated (Boxes 2 and 3), key ecological distinction between these birds innovations can potentially link evolu- by placing them in different taxa. tionary processes acting on different hier- These taxa are, of course, those of archical levels. Nevertheless, key inno- evolutionary systematics. The differences Box 1. Contrasting definitions of key innovation vation hypotheses are not attempts to between such taxa can be large, whereas reduce the causes of biological expansion Miller saw natural selection as capable of Miller (1949): ‘… key adjustments in the mor- phological and physiological mechanism which down to a single factor. only incremental change and felt that ex- are essential to the origin of new major groups’3. Historically, researchers have meas- tinction is insufficient to account for the 3 Van Valen (1971): ‘A key character, in the adap- ured evolutionary ‘success’ by the appear- distinctiveness of major groups . Instead, tive sense, is a structure or element of physiology ance of higher taxa, the proliferation of small changes in form can have a large func- that makes a taxon more or less committed to species or the generation of new mor- tional significance (i.e. key innovations) a way of life different from, or appreciably more phologies. Each measures a different as- and bring a lineage into a new ecological efficient than, that of its ancestors’5. pect of expansion in the use and control of sphere where it can diverge free from com- Levinton (1988): ‘key innovation is necessary, energy2, and key innovations may promote petition with related incumbent species3. but not sufficient for a subsequent radiation’6. this expansion. Recent investigators have This connection between key inno- Baum & Larson (1991): ‘… a trait that greatly tended to focus on taxonomic diversifi- vations and the origin of higher taxa made modifies the selective regime of the lineage in cation, usually the number of species in a biological sense to early workers. Invasion which it evolves’15. group, whereas older literature was more of new adaptive zones (i.e. a set of related Rosenzweig & McCord (1991): ‘A key adaptation concerned with major adaptive shifts rec- ecological niches) was seen to precede the is a change in the mathematical rule governing a trade-off constraint so that after the change, ognized by the appearance of higher taxa. origin and diversification of (and within) the trade-off is less severe’13. Here, I outline how the key innovation con- higher taxa, and key innovations were cept has itself evolved, explain what can be seen to facilitate a transition into a new Erwin (1992): ‘[K]ey innovations characterize particular clades and are both necessary and learned from older approaches, indicate adaptive zone. Historically, studies of key sufficient to explain diversification within the problems in current analytical methods, innovations have focused on characters clade’39. and offer some alternatives. that diagnose higher taxa and set them Heard & Hauser (1995): ‘an evolutionary change apart adaptively from their close rela- in individual trait(s) that is causally linked to an Key innovations and higher taxa tives5 as opposed to characters that pro- increased diversification rate in the resulting The key innovation concept has al- mote diversification per se. For example, clade (for which it is a synapomorphy)’9. ways been linked to the origin of higher among mammalian orders, the Tubuliden- TREE vol. 13, no. 1 January 1998 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00 PII: S0169-5347(97)01273-1 31 PERSPECTIVES In some cases, the connection between innovation and taxonomic diversification is (a) direct, in others less so. If speciation results from divergence in the same characters on Bunodont (human) which natural selection acts, as in ecologi- cal11 or competitive12,13 speciation, then a key innovation that facilitates ecological Bilophodont (kangaroo) Trilophodont (rhinoceros) divergence might also directly influence taxonomic diversification as well. Evidence for these controversial speciation modes, however, is rare in nature. In theory, eco- logical or competitive speciation should be Quadritubercular most common at the base of adaptive radi- ations11,12 or during biotic replacements13 Hypocone Lamellar (elephant) Selenodont (deer) when key innovations may have most influ- ence on diversification rate14. Lateral In other cases the connection between Anterior innovation and taxonomic diversification is indirect or unclear. Heard and Hauser9 hy- Tritubercular pothesized that on an ecological time scale key innovations might work by one of the (b) following three mechanisms: (1) by allow- ing escape from competition via invasion hypocone into a new adaptive zone, (2) by decreasing 200 hypocone shelf the probability of extinction by increasing (intermediate) population density via increased individ- no hypocone ual fitness, or (3) by favoring reproductive 150 or ecological specialization. Invasion of a new adaptive zone may re- 100 sult in a change in the selection pressures acting on a lineage15, which may result in 50 evolutionary changes of a magnitude that Number of species traditional systematists would recognize by naming a new taxon for the derived 0 forms4,6. Whether the change in adaptation Plio. Paleocene Eocene Oligocene Miocene Plei. also results in a proliferation of new spe- cies depends as much on the adaptive zone itself as the lineage invading it. Adopting Fig. 1. The evolution of the hypocone and herbivory in mammals. The hypocone, a cusp on the postero- medial corner of mammalian upper molars, is believed to have evolved in at least 20 lineages of mammals herbivorous habits seems to offer many during the Cenozoic, most of these appearing by
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