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Adaptations and History Historically Through the Action of George V TREE vol. 8, no. 8, August 1993 I4 Doiman, A.J., Gash, J.H.C., Roberts, J. and 22 ldso, S.B., Alien, SC. and Choudhury. Plant Cell Environ. 13, 383-388 Shuttleworth, W.J. (1991) Agric. For. B.I. (1988) Agric. For. Meteoml. 43, 49-58 31 Meinzer, F.C., Grantz, D.A., and Smit, B. Meteorol. 54, 303-3 I8 23 Monteith, I.L. (1990) Agrk Fo‘or. ( I99 I ) Amt. I. Plant Physiol. 18, 329-338 15 Kim, J. and Verma, S.B. (1991) Agric, For Meteorol. 49, 155-167 32 Meinzer, F.C. and Grantz, D.A. ( I991 ) Meteorol. 57, 187-208 24 Kostner, B.M.M. etal. ( 1992) Oecologia Physiol. Plant. 83, 324-329 I6 Cohen, Y., Fuchs, M. and Green, G.C. 91,350-359 33 Monteith, J.L. (1988) /. Hydrol. 100, 57-68 ( I98 1) Plant Cell Environ. 4, 39 I-397 25 Aphaio, P.J. and Jarvis, P.G. (1991) Plant 34 Tyree, M.T. and Sperry, IS. 11988) Plant I7 Cermak, I., Demi, M. and Penka, M. CellEnviron. 14, 127-132 Physiol. 88, 574-580 (1973) Biol. Plant. 15, 171-178 26 Mott, K.A. and Parkhurst, D.F. (1991) 35 Meinzer, F.C., Goldstein, G., Neufeid. 18 Baker, I.M. and Van Bavel, C.H.M. (1987) Plant Cell Environ. 14, 509-5 I5 H.S., Grantz, D.A. and Crisosto, G.M. (1992) Plant Cell Environ. 10, 777-782 27 Davies, W.)., Mansfield, T.A. and Plant Cell Environ. 15, 471-477 I9 Grantz, D.A. ( 1990) P/ant Cell Environ. Hetherington, A.M. (1990) Plant Cell 36 lones, H.G. and Sutherland, R.A. (1991) I3,667-679 Environ. 13, 709-7 I9 Plant Cell Environ. 14, 607-612 20 Idso, S.B., Clawson, K.L. and Anderson, 28 Davies, W.J. and Zhang, 1. (1991) Annu. 37 Idso, S.B. (I 983) Agrk. Meteorol. 29, M.G. (1986) WaterResour. Res. 22, 1702-1716 Rev. Plant Physiol. Molec. Biol. 42, 55-76 213-217 21 Idso, S.B. (1987) Agric. For. Meteorol. 40, 29 Chapin, F.S. (1991) BioScience41, 29-36 38 Coilatz, G.J., Bail, LT., Grivet, C. and Berry, 105-106 30 Meinzer, F.C. and Grantz, D.A. (1990) LA. (I 99 I ) Agric. For. Meteorol. 54, 107-l 36 Adaptations and History historically through the action of George V. Lauder, Armand M. Leroi and Michael R. Rose natural selection for its current bio- logical role’14. This definition, or some version of it, is now widely accepted9J3r15-‘7, and for the sake The historical definition of adaptations has With this rise in comparative of brevity we refer to it as the his- come into wide use as comparative biol- studies has come an emphasis on torical definition of adaptations. ogists have applied methods of phylogen- the concept of adaptation as having Central to this definition, as to etic analysis to a variety of evolutionary an important historical component. many other (but not a11r8) defi- problems. Here we point out a number of Gould and Vrba’* codified this view nitions of adaptations, is the notion difficulties in applying historical methods by developing a terminology that that selection is the evolutionary to the study of adaptation, especially in distinguished between the current process that produced the trait cases where a trait has arisen but once. utility of a character and its histori- under consideration’9s20; traits that In particular, the potential complexity of cal origin. For Gould and Vrba, are considered to be adaptive thus the genetic correlations among phenotypic an adaptation was a trait whose evolve under selection for that traits, performance variables and fitness ‘historical genesis’ was due to the trait. makes inferring past patterns of selection same selective pressure as that This definition of adaptations from comparative data difficult. A given which currently maintains the trait. leads naturally to a research meth- pattern of character distribution may A trait whose origins in a clade were odology that aims to reveal the way support many alternative hypotheses of due to selective pressures other in which historical changes in selec- mechanism. While phylogenetic data are than those that currently maintain tive regimes or environments have limited in their ability to reveal evolution- it was labeled an ‘exaptation’. shaped the evolution of clades13,‘4. ary mechanisms, they have always been Gould and Vrba’s’* definition of A centerpiece of the method is the an important source of adaptive hypoth- adaptations has had considerable role given to measuring organismal esesand will continue to be so. influence on other workers who have performance. The method, sum- elaborated on the historical defi- marized in Box I, consists of four The last five years have witnessed nition of adaptation. For example, steps. First, historical changes in a virtual explosion in comparative Coddingtonr3 defined an adap- environmental circumstances or in studies of organismal design. Fueled tation in cladistic terms as an a ‘selective regime’r4 that might in part by the increasing accept- ‘apomorphic function promoted by have plausibly influenced the evol- ance of cladistic approaches to in- natural selection’. Furthermore, the ution of a clade are identified. It is ferring relationships among taxa, elaboration of an historical dimen- assumed that environmental charac- comparative biologists have begun sion to the concept of adaptation teristics relevant to fitness can be to attack a wide range of evolution- has led to another definitional ex- mapped onto a phylogenetic tree ary problems. Sexual dimorphism, pansion, namely, that the only much like any other character. life history, ecology, muscle function traits that should be called adap- Second, the performance attributes and insect-plant coevolution are tations are those which confer en- that might have possibly conferred but a few of the many issues that hanced performance in the current increased fitness under a given have been investigated by com- environment relative to the traits selective regime are identified. parative phylogenetic methods’-“. that preceded them evolutionarily: Third, the historical changes in or- ‘To constitute an adaptation, a ganismal traits (be they behavioral, George Lauder, Armand Leroi and Michael Rose are character must be shown to pro- morphological or physiological) that at the Dept of Ecology and Evolutionary Biology, vide current utility to the organism might have plausibly influenced such University of California, Irvine, CA 92717, USA. and to have been generated performance traits are identified. 294 0 1993, Else&v Science Publishers Ltd TREE vol. 8, no. 8, August 7993 And fourth, the relative perform- ance of these organismal traits in ancestral (plesiomorphic) and derived (apomorphic) states is measured. If the derived trait has a superior performance relative to its ancestor, and arose after historical change in the ‘selective regime’, then, and only then, is the trait an adaptation (Box I). The historical method for ana- lysing characters outlined in Box 1 promises two key advances. First, under this methodology, a trait need not have evolved numerous (phylo- genetically independent) times to be deemed an adaptation. Instead, even a trait that has evolved only once might be analysed for en- vironmental and performance cor- relates and pass the requisite tests appropriate to be labelled an adap- tation (Box 1). Second, the com- parative phylogenetic method sug- gests that one will be able to inventory characters within a clade the trait under consideration should circumstance E’), but also of A’ due to determine which traits are adap- not be genetically correlated with to the positive genetic correlation tations, which are disaptations and others that might influence fitness, of A and B. A’ would be identified which are nonaptations without and that fitness should be deter- as an adaptation given the phylo- having to measure directly the ac- mined by the performance variable genetic pattern shown in Case 2 tion of selection on each trait (Box 1). under consideration. (Box 21, under the historical defini- Our purpose here is to examine Box 2 (Case 1) illustrates these tion of adaptation. But in fact selec- the mechanistic assumptions that relations, and how they might ap- tion would not have operated di- underly the historical approach to pear on a phylogeny. In this rectly for character A’, and thus it adaptations, to illustrate potential example, the common ancestor of should not be classified as an ad- difficulties with inferring the past the three species has a particular aptation. The phylogenetic pattern action of selection solely from trait (A), performance (a), and is in this case is misleading as to the comparative data on traits, environ- subject to environment E. In the underlying mechanistic cause of ments and performance, and to in- course of cladogenesis, a change character evolution. dicate the value that such compara- in environmental circumstance (E’) A second situation in which a tive data still have in suggesting imposes a novel selection pressure phylogenetic pattern might be mis- mechanistic hypotheses and in test- for performance attribute a’ and leading is shown in Case 3 of Box 2. ing proposed scenarios. hence trait A’. Trait A’, then, is an If a single trait A is positively adaptation because its evolution is genetically correlated with two dif- The historical approach to adaptation: directly due to its superior perform- ferent performance variables (for genetic and environmental complexities ance in E’ relative to the ancestral example, locomotor endurance and Identifying adaptations using the condition (A). feeding rate), then fixation of trait method outlined in Box 1 requires But the relationship among traits, A’ may result from the fitness conse- that assumptions be made concern- performance and fitness in organ- quences of performance trait p in ing the genetic relationships among isms is rarely as simple as this2’-23.
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