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The Evolution of Maladaptation

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The Evolution of Maladaptation Heredity 84 (2000) 623±629 Received 6 March 1999, accepted 11 April 2000 Short Review The evolution of maladaptation BERNARD J. CRESPI* Department of Biological Science, Simon Fraser University, 8888 University Drive, Burnaby BC V5A 1S6, Canada This review contains a description of a research program for using studies of natural selection and teleonomy; (2) deter- the study of maladaptation, de®ned here in terms of deviation mination of the causes of the deviation, using analyses of from adaptive peaks. Maladaptation has many genetic causes, genetics, development, or other methods. Conditions for including mutation, inbreeding, drift, gene ¯ow, heterozygote unambiguously identifying maladaptation are considerably advantage and pleiotropy. Degrees of maladaptation are more stringent than those for demonstrating adaptation and determined by genetic architecture and the relationship remarkably few studies have clearly identi®ed and character- between the rates of selective, environmental change and the ised maladaptative traits. A thorough understanding of the nature and extent of genetic responses to selection. The nature of phenotypic variation will never be achieved without empirical analysis of maladaptation requires: (1) recognition of an analysis of the scope and usual causes of maladaptation. putative maladaptation, using methods from phylogenetics, teleonomy, development and genetics, followed by an assess- Keywords: adaptation, adaptive peaks, evolution, maladap- ment of the nature and degree of deviation from adaptation, tation. `But by far the most important consideration is that the chief `maladaptation' and discussed the usefulness of these de®ni- part of the organization of every being is simply due to tions for addressing various questions. Secondly, I have inheritance; and consequently, though each being assuredly is discussed the causes of maladaptation at dierent levels in the well ®tted for its place in nature, many structures now have no hierarchy of biological information (Arnold, 1992). Thirdly, I direct relation to the habits of life of each species'. Darwin have focused on methods for identifying and analysing (1859; p. 199). maladaptation, drawing on approaches that have developed independently in dierent ®elds and seeking to reconcile the often-acrimonious opinions of geneticists and ecologists Introduction regarding the usefulness of their research methods. The study of phenotypic adaptation and its genetic basis is central to evolutionary biology. The term `adaptation' has accumulated myriad de®nitions (reviews in Reeve & Sher- De®ning adaptation and maladaptation man, 1993; Rose & Lauder, 1996) but adaptations are forms Our primary criterion for choosing a de®nition should be its of traits that are always construed as the result of natural utility for answering questions of interest. De®nitions of selection, whereas individuals with variant traits that are less adaptation can be categorized into four main types: (1) well ®t to the environment exhibit lower reproductive success. teleonomic; (2) phylogenetic; (3) population genetic; (4) quan- However, the ®t of traits to environments epitomized in the titative genetic. term adaptation (`®t for', from the Greek `ad aptos') can Teleonomic de®nitions of adaptation developed in evolu- never be perfect, partly because organisms are always tionary and behavioural ecology (Thornhill, 1990) and focus adapted to at least one generation in the past. Thus, some on the functional design of phenotypic traits ± how they have degree of deviation from the maximal possible degree of been `designed' by the blind watchmaker of selection to adaptation is always expected. Such deviations have been `function' in some environmental context. These de®nitions analysed under a variety of rubrics, using the tools of emphasize the selective maintenance of traits, and involve population and quantitative genetics, developmental biology, identi®cation and quanti®cation of the ®t between form and behavioural and evolutionary ecology. The purpose of and function (Reeve & Sherman, 1993). The implementation this review is to synthesize perspectives and information from of teleonomic de®nitions into a research program requires these disparate disciplines and to analyse the nature and speci®cation of a strategy set (a range of possible trait forms), causes of maladaptation. Firstly, I have categorized de®ni- an application of some ®tness criterion (what is maximized, tions of `adaptation', translated them into de®nitions of such as performance of some task or a component of ®tness) and deliniation of constraints (®xed parameters that bound *Correspondence. Tel.: +1 604 291 3533, Fax: +1 604 291 3496, the analyses and link the strategy set with the ®tness E-mail: [email protected] criterion). This research program is based on the premise Ó 2000 The Genetical Society of Great Britain. 623 624 B. J. CRESPI that a history of natural selection leads to forms of traits subject to unfavourable environmental change, or (2) the (adaptations) that are optimal in a given environmental degree to which the ®tness of the current genotype lags be- context, within the range of the strategy set. Quanti®cation of hind the optimal genotype in a changing environment (see current selection is not necessary under this program, because also Kirkpatrick, 1996). Gillespie (1991; p. 63 and p. 305) current selection need not re¯ect the selective pressures concludes that such loads are often heavy as populations are 1during the trait's evolution (Thornhill, 1990). This optimiza- usually far from allelic equilibrium, apparently; this is because tion approach to adaptation has been useful in characterising genotypic adaptive peaks outrun responses to selection. the nature and causes of associations between traits, and Load-based metrics of maladaptation require estimating the between traits and environments, especially for aspects of relation between alleles or genotypes and ®tness, and where behaviour and life history. feasible they provide a strong link from maladaptation to its Under a teleonomic research program, `maladaptation' can causes. be de®ned as prevalence in a population of a `strategy' (a form Quantitative geneticists normally discuss adaptation in the of a phenotype), that does not lead to the highest relative context of phenotypic adaptive topologies, where local and ®tness of the strategies in the allowed set. This viewpoint has global peaks represent optimal population states (Schluter & often been dicult to implement, due to the diculties 2Nychka, 1994). For quantitative traits, approaches to these involved in de®ning a complete and accurate set of strategies peaks are governed by the form and strength of multivariate and constraints, the complex selective pressures on many traits selection and response to selection which can be predicted (at and the challenge of measuring ®tness in an evolutionari- least in the short term) using the genetic variance-covariance ly meaningful way (Lewontin, 1979). Moreover, if a formerly matrix (Shaw et al., 1995). By this perspective, maladaptation neutral trait (e.g. red vs. yellow ¯owers) comes under selection, can be quanti®ed as the distance of a population from the such that plants with red ¯owers have higher reproductive nearest adaptive peak (Loeschcke, 1987; Bjorklund, 1996). success (e.g. their pollen fertilizes more ovules), then red This distance is largely a function of the degree to which the ¯owers will be called an adaptation under some teleonomic population does not exactly track the vector of directional de®nitions (e.g. Reeve & Sherman, 1993), even before there has selection, as a result of aspects of genetic response to selection been any genetic response to selection. that prevent the largest possible selection-driven step up- Phylogenetic de®nitions of adaptation require the use of a wards. Stabilizing selection serves to de®ne the optimal, phylogeny to infer the origin of a trait, inference of the `adapted' state or peak, though a population may spread `selective regime' under which the trait arose, and an analysis more or less widely down its sides. As we can measure of performance of the trait under its ancestral and current selection in the ®eld, construct adaptive surfaces and estimate selective regime (Baum & Larson, 1991 and references G in the ®eld or laboratory, this measure of maladaptation is therein). If the trait arose under its current selective regime feasible to employ. Moreover, it provides a bridge between and exhibits higher performance than its antecedent, then it is genetic mechanisms of microevolutionary change, notably considered an adaptation. This de®nition focuses on joint additive genetic variance, pleiotropy, and linkage disequilib- analyses of the origin and maintenance of traits, under the rium, and aspects of ecology, as depicted in adaptive presumption that traits changing in function over the speci®c landscapes. To the extent that adaptive topologies move time period considered should be categorized dierently from across generations, or populations are displaced downhill by traits that do not. Baum & Larson (1991) provide explicit genetic happenstance, populations will be o their peaks and criteria for identifying maladaptation under this phylogenetic thus, to some quanti®able degree, maladapted. perspective; a trait is maladaptive (a.k.a. `disadapted', in their I have purposefully avoided the term `constraint' in the lexicon) if it exhibits lower utility (performance at some task) exposition above as most authors
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