Of isopods and Hollywood stars: the measure of sexual selection
Article first published online: 4 APR 2005
Journal of Evolutionary Biology
Volume 18, Issue 1, pages 243–244, January 2005
How to Cite
Pizzari, T. (2005), Of isopods and Hollywood stars: the measure of sexual selection. Journal of Evolutionary Biology, 18: 243–244. doi: 10.1111/j.1420-9101.2004.00800.x
- Issue published online: 4 APR 2005
- Article first published online: 4 APR 2005
A review by Tommaso Pizzari
A review of ‘Mating Systems and Strategies; Monographs in Behavior and Ecology’ . By & . Princeton University Press , NJ, USA . 2003 . ISBN 0-691-04931-9 , price $35.00 / £22.95 .
Sexual selection is an intriguing force. Operating on variance in reproductive success, it is limited almost exclusively to adult males, and yet its action is one of the most powerful evolutionary forces, underlying rapid inter-sexual coevolution, speciation and much of the phenotypic exuberance observed in sexual organisms. Following Darwin (1871), the study of sexual selection got off to a slow start, partly because of the lack of a formal genetic framework and the scepticism surrounding the idea of female choice (Mayr, 1982). However, in the past 20 years or so, interest in sexual selection has gathered tremendous momentum thanks to the synthesis between genetics and Darwinian theory, and a cultural shift towards female strategies, to become one of the most rapidly-growing subjects in evolutionary biology. This intense interest has focussed primarily on the evolution of female preference for specific partners, resulting in a wealth of theoretical models and empirical tests of their predictions (Andersson, 1994).
More recently, mechanisms of post-insemination sexual selection have also attracted intense attention, following the realization that females of many species obtain sperm from multiple males, prolonging sexual selection after insemination through sperm competition and cryptic female choice. Finally, the growing evidence that reproductive partners pursue divergent fitness interests at each other's expense (sexual conflict) is generating much interest on the extent to which sexual selection is driven by sexual conflict. All these efforts attempt to elucidate potential mechanisms of sexual selection but do not measure the intensity with which it operates. In nature, the strength of sexual selection and the male traits that it targets depend ultimately on the availability of receptive females in time and space, determined by ecological and life-history constraints. To understand how sexual selection promotes a diversity of mating strategies across different ecological and life-history constraints we must be able to measure and compare the intensity of sexual selection across different species and populations. Despite isolated, and mostly verbal, efforts linking mating system diversity with the operation of sexual selection (e.g. Emlen & Oring, 1977), there has been a dire need for a comprehensive statistical framework to relate the intensity of sexual selection to patterns of spatio-temporal female availability. Shuster & Wade's (2003) book achieves this ambitious goal brilliantly.
The book builds a framework to measure sexual selection across mating systems, based on quantitative genetics and the analysis of variances and covariances. The first chapter lays the foundation of this framework, identifying the variance in number of sexual partners secured by males, Imates, as a crucial measure of the intensity of sexual selection. When variances in male and female fitness are considered, the solution to the apparent paradox of sexual selection (stronger than natural selection, yet limited to adult males) becomes clear: competition among males over females results in consistently high variance in male mating success and generates relatively high intensity of sexual selection. The next eight chapters formalize, critically review and build on previous models to develop a statistical framework that measures the effects of female spatio-temporal dispersion, life history and re-mating rates on variance in male and female reproductive success, and thus on the opportunity of sexual selection on males (Imates) arising from a mating system. The beauty of this approach is that it generates a dimensionless measure of the intensity of sexual selection that can be readily quantified in the field (provided parentage can be assigned correctly!) and compared across a variety of different taxa: from isopods to Hollywood film stars (chapter five). The other great advantage of this approach is that it allows the comparison between the opportunity of sexual selection on males and natural selection on females. Therefore, chapters six, eight and nine analyse variation in the difference between the opportunity of selection on males and females (ΔI), due to ecological and life-history factors, to propose a precise classification of the bewildering diversity of mating systems (chapter nine). Chapter ten shifts the subject to provide a useful reminder of Darwin's (1871) phenomenal intuition and advanced understanding of the operation of sexual selection (or of the frustrating little progress made ever since!) which, if somewhat disjointed from the previous chapters, introduces nicely the issue of alternative mating strategies, often overlooked in reviews of mating systems, that is discussed fully in the following, final two chapters.
Shuster and Wade's framework has unprecedented predictive power because it generates quantitative, testable predictions about the extent to which different ecological and life-history constraints catalyse or buffer sexual selection. But this book does more than delivering a statistical tool. While they are at it, Shuster and Wade address several outstanding issues in sexual selection. For example, embedded in chapter five is a discussion of the pitfalls of mate choice trials, based on quantitative arguments that lucidly illustrate the problems of using this experimental approach. A whole chapter (seven) is dedicated to conceptually problematic issues in sexual selection. Put in this quantitative perspective (i.e. when one starts quantifying the effects of different sexual selection mechanisms), some important patterns begin to emerge. For example, the fact that viability selection is unlikely to drive female preference unless variances in male and female fitness are similar, seems to undermine pervasive ‘good genes’ explanations for highly skewed mating systems (e.g. leks). Similarly, because variance in male fitness is typically higher than variance in female fitness, viability selection on females is unlikely to counteract sexual selection for male traits even if these traits reduce female fitness, thus emphasizing potential difficulties associated with recent theories of sexual selection via sexual conflict.
The book is a success: it is clear and strikes the right balance between theory and biological examples. Each chapter starts with clear aims and plan, and ends with a very useful summary. I found that equations were often accompanied by clear verbal explanations. Despite these efforts, some empiricists may still be intimidated by the theory of this book. The wealth of equations in the first chapters is crucial to lay the foundations of the quantitative framework. However, as a minor point, complementing or replacing some equations with verbal explanations (perhaps including the necessary mathematical steps in appendixes, without forcing readers to plough through equations) may have improved readability. This may also have reduced the risk of confusions associated with some symbols (e.g. Vw = variance in fitness before reproduction, and Vw = variance in relative fitness) and ambiguities generated by typos. For example, in chapter one, page 26, third line from bottom, should be k > 1, not <1 for each k class of males: these ‘one-character substitutions’ are more likely to result in ‘deleterious mutations’ distorting the meaning of a period when they arise in symbols rather than in multi-character words. Similarly, chapter titles such as ‘The ΔI surface’ (chapter six) may discourage readers, particularly the ones interested in the empirical study of sexual selection. This would be a shame because it is crucial that the importance of going ‘quantitative’, so convincingly advocated by the book, reaches theoreticians and empiricists alike. Evolutionary biology has often suffered from a lack of feedback between theoretical and empirical approaches, starting from the early days when biologists interested in evolution were not prepared to recognize the theoretical importance of Mendel's (1866) paper, stalling evolutionary theory for quite some time (Fisher, 1930).
Shuster and Wade's book is a tremendous effort to move the empirical study of sexual selection from ‘just-so’ stories to robust quantitative tests, and a powerful demonstration that even in our ‘post-genomics’ age, the contribution of standard multivariate statistics remains priceless. This book will have an important long term influence. It will provoke discussion and further theoretical refinements of this quantitative approach. It will force people to consider empirical quantitative approaches, based on the measure of variance in fitness, to complement current approaches based on the description of sexual selection mechanisms. The dimensionless property of Shuster and Wade's measure of the intensity of sexual selection should make this approach particularly amenable to comparative studies, which are currently based on approximate measures of sexual selection such as sexual dimorphism and relative testis mass. This book is a must for any biologist seriously interested in the operation of sexual selection in any organism: from isopods to Hollywood stars.
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