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The Strength of Phenotypic Selection in Natural Populations

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The Strength of Phenotypic Selection in Natural Populations vol. 157, no. 3 the american naturalist march 2001 The Strength of Phenotypic Selection in Natural Populations J. G. Kingsolver,1,* H. E. Hoekstra,1 J. M. Hoekstra,1,² D. Berrigan,1,³ S. N. Vignieri,1 C. E. Hill,1,§ A. Hoang,1 P. Gibert,1,k and P. Beerli2 1. Department of Zoology, University of Washington, Seattle, overall median of only 0.10, suggesting that quadratic selection is Washington 98195; typically quite weak. The distribution of g values was symmetric 2. Department of Genetics, University of Washington, Seattle, about 0, providing no evidence that stabilizing selection is stronger Washington 98195 or more common than disruptive selection in nature. Submitted June 9, 2000; Accepted October 31, 2000 Keywords: microevolution, natural populations, natural selection, phenotypic selection, sexual selection. abstract: How strong is phenotypic selection on quantitative traits How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for in nature? Is strong directional selection rare? Is stabilizing studies that estimated the strength of linear and quadratic selection or correlational selection common? Is selection more in- in terms of standardized selection gradients or differentials on natural tense on life history than on morphological traits? What variation in quantitative traits for ®eld populations. We tabulated 63 is the relative importance of direct versus indirect selection published studies of 62 species that reported over 2,500 estimates of on correlated traits? The answers to these and similar ques- linear or quadratic selection. More than 80% of the estimates were tions are fundamental to understanding the role of selec- for morphological traits; there is very little data for behavioral or tion in determining evolutionary changes and adaptation physiological traits. Most published selection studies were unrepli- cated and had sample sizes below 135 individuals, resulting in low in current populations. In his in¯uential book, Natural statistical power to detect selection of the magnitude typically re- Selection in the Wild, Endler (1986) provided a compre- ported for natural populations. The absolute values of linear selection hensive review of published ®eld studies of selection gradients FbF were exponentially distributed with an overall median through 1983. His synthesis documented the abundant of 0.16, suggesting that strong directional selection was uncommon. evidence that selection on quantitative traits occurs fre- The values of FbF for selection on morphological and on life-history/ quently in natural populations. However, quantitative es- phenological traits were signi®cantly different: on average, selection timates of the strength of phenotypic selection on quan- on morphology was stronger than selection on phenology/life history. titative traits were largely lacking at that time (e.g., Endler's Similarly, the values of FbF for selection via aspects of survival, review reports values of directional selection differentials fecundity, and mating success were signi®cantly different: on average, selection on mating success was stronger than on survival. Com- from a total of 25 species). parisons of estimated linear selection gradients and differentials sug- The early 1980s also saw the development and intro- gest that indirect components of phenotypic selection were usually duction of new methods for estimating the strength of modest relative to direct components. The absolute values of qua- selection on multiple quantitative traits (Lande 1979; dratic selection gradients FgF were exponentially distributed with an Lande and Arnold 1983; Arnold and Wade 1984a, 1984b). These methods had two important advantages. First, they * Corresponding author. Present address: Department of Biology, University provided a means of distinguishing the direct and indirect of North Carolina, Chapel Hill, North Carolina 27599-3280; e-mail: jgking@ bio.unc.edu. components of selection on a set of correlated traits. This allowed researchers to use simple statistical methods (par- ² Present address: Department of Ecology and Evolutionary Biology, Univer- sity of Arizona, Tucson, Arizona 20892. tial regression models) to estimate the strength of direct ³ Present address: National Cancer Institute, Bethesda, Maryland 20892. selection on a trait in terms of a common metric, the selection gradient, that represents the relationship of rel- § Present address: Department of Biology, Coastal Carolina University, Con- way, South Carolina 29528. ative ®tness to the variation in a quantitative trait mea- k Present address: Laboratoire Populations, Genetique, et Evolution, Centre sured in standard deviation units. Second, selection gra- National de la Recherche Scienti®que, 91198, Gif Sur Yvette Cedex, France. dients were shown to be directly relevant to quantitative Am. Nat. 2001. Vol. 157, pp. 245±261. q 2001 by The University of Chicago. genetic models for the evolution of multiple, correlated 0003-0147/2001/15703-0001$03.00. All rights reserved. traits (Lande 1979; Lande and Arnold 1983). 246 The American Naturalist Table 1: Summary of the database of phenotypic ical Transactions of the Royal Society of London, Proceedings selection studies (1984±1997) of the Royal Society of London, and Science. These represent Number of items the major peer-reviewed outlets for original scienti®c re- in the database search on phenotypic selection. We did not include un- Studies 63 published studies or studies published in book chapters Records 1,582 or technical reports, for which it is more dif®cult to assess Species 62 quality control. Genera 51 We used four main criteria for including studies in our Taxon type: analyses. First, the studies involved quantitative traits Invertebrates (I) 534 records (19 studies) showing continuous phenotypic variation within the study Plants (P) 587 records (18 studies) population: studies of discrete and categorical traits were Vertebrates (V) 461 records (27 studies) not considered. Second, the studies examined natural Study type: phenotypic variation within populations: studies involving Cross-sectional (C) 14 studies Longitudinal (L) 51 studies genetically or phenotypically manipulated traits, highly in- bred or experimental genetic lines, or domesticated species were not considered. Third, the studies were conducted in natural conditions in the ®eld: studies in the lab, green- These and other advances led to an explosion of ®eld house, experimental plots, or other controlled environ- studies of selection on quantitative traits in a variety of mental conditions were not considered. systems during the ensuing 15 yr. These studies have been The fourth criterion concerns the metrics used to es- important for exploring the role of selection for evolution timate selection. We included only those studies that re- of particular traits in many speci®c model systems of in- ported one or more of the following metrics: standardized terest. However, while aspects of these studies have been linear selection gradients (b), standardized quadratic se- reviewed with respect to speci®c issues or taxa (Primack lection gradients (g), standardized linear selection differ- and Kang 1989; Travis 1989; Gontard-Danek and Mùller entials (i), or standardized quadratic selection differentials 1999), no synthesis of this literature has emerged that (Lande and Arnold 1983; Arnold and Wade 1984a, 1984b). examines the strength of selection in natural systems more These metrics estimate selection on a trait in terms of the generally. effects on relative ®tness in units of (phenotypic) standard In this report, we describe such a synthesis. We have deviations of the trait, allowing direct comparisons among reviewed the published literature from 1984 through 1997 traits, ®tness components, and study systems. Selection that reported standardized selection gradients and/or se- gradients estimate the selection directly on the trait of lection differentials on natural variation in quantitative traits within ®eld populations. Using the resulting data- interest, whereas selection differentials estimate total se- base, we explore how the strength of directional and qua- lection on the trait acting both directly and indirectly via dratic selection varies across systems, traits, and ®tness selection on other, correlated traits (Lande and Arnold components and examine the power of these studies for 1983). Linear selection gradients and differentials estimate detecting selection on quantitative traits. the strength of directional selection; quadratic selection gradients and differentials estimate the curvature of the selection function. Note that stabilizing selection on a trait implies that the quadratic selection gradient and differ- Methods ential are negative, and disruptive selection on a trait im- plies that the quadratic selection gradient and differential General Considerations are positive. However, the converse is not true: a negative We started our literature review with 1984 because Endler's quadratic selection gradient or differential is not suf®cient monograph (1986) reviewed the literature on selection, to demonstrate stabilizing selection (Mitchell-Olds and including estimates of selection differentials, published by Shaw 1987). the end of 1983. We examined all studies published from These criteria exclude many important and interesting 1984 through 1997 in 15 peer-reviewed journals: American studies of selectionÐwe estimate that more than half of Journal of Botany, American
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