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Genic Capture and Resolving the Lek Paradox

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Genic Capture and Resolving the Lek Paradox Review TRENDS in Ecology and Evolution Vol.19 No.6 June 2004 Genic capture and resolving the lek paradox Joseph L. Tomkins1, Jacek Radwan2, Janne S. Kotiaho3 and Tom Tregenza4 1Environmental and Evolutionary Biology, Dyer’s Brae House, The Mitchell Building, University of St Andrews, Fife, UK, KY16 9TH 2Institute of Environmental Sciences, Jagiellonian University, ul. Ingardena 6, 30-060 Cracow, Poland 3Department of Biological and Environmental Science, University of Jyva¨ skyla¨ , PO Box 35, 40014 Jyva¨ skyla¨ , Finland 4Ecology and Evolution Group, School of Biology, University of Leeds, UK, LS2 9JT The genic capture hypothesis offers a resolution to the sexual display traits mean that mutations can indeed question of how genetic variation in male sexually maintain variation in the face of DIRECTIONAL SELECTION selected traits is maintained in the face of strong female created by female mate choice. preferences. The hypothesis is that male display traits Houle [14] argued that the relatively high genetic are costly to produce and hence depend upon overall variance of fitness-related life-history traits could be condition, which itself is dependent upon genes at explained by their dependence on many underlying many loci. Few attempts have been made to test the physiological and morphological traits, such that they assumptions and predictions of the genic capture sum genetic variation over many loci. This multitude of hypothesis rigorously and, in particular, little attention loci provides a large mutational target [15] that is resistant has been paid to determining the genetic basis of con- to erosion through directional selection. Similar to life- dition. Such tests are crucial to our understanding of history traits, sexually selected traits also have relatively the maintenance of genetic variation and in the evalu- high coefficients of additive genetic variation [4]. Pomian- ation of recent models that propose a role for sexual kowski and Møller [4] argued that this pattern could be selection in the maintenance of sex. Here, we review explained if selection on sexual traits was an increasing approaches to testing the link between genetically function of trait size (e.g. [16]), because this would favour determined condition and levels of sexual trait increased trait variance and select for an increase in the expression and consider the probable importance of number and/or contribution of loci involved in trait deleterious mutations. expression. This mechanism has been criticized because, after initial spread, trait expression at any given level of The ‘LEK PARADOX’ (see Glossary) has long haunted the condition is likely to be subject to stabilizing, rather than study of sexual selection. If females prefer certain male escalating, non-linear selection [2]. The hypothesis also traits that indicate VIABILITY, then the increased mating fails to provide a mechanism for the positive genetic success of males bearing them should rapidly exhaust covariance between sexual trait expression and viability, genetic variation for viability and drive the traits to required in ‘GOOD GENES’ models [17,18]. fixation. This is the paradox [1–4]: female choice depletes Andersson [19] suggested that the phenotypic quality of genetic variation, thus leaving little room for choice to an individual will be influenced by most of its genome and, result in genetic benefits, and yet the genetic benefits to consequently, that the size of sexual ornaments will offspring are the explanation for that choice. depend on the overall genetic quality of the individual The lek paradox is, in fact, just a prominent example of rather than on a few major genes (see also [20]). Population one of the major unresolved issues in evolutionary biology genetic models of this concept show that the key to the [5,6]: what maintains ADDITIVE GENETIC VARIANCE in origin and maintenance of the genetic variance in sexually fitness-related traits [7]? This question continues to be a source of debate [8,9], with two broad and complimentary explanations based either on fluctuating selection or on Glossary mutation–selection balance. Fluctuating selection argu- Additive genetic variance: genetic variance associated with average additive ments depend on the idea that the optimal phenotype effects of alleles. Causes offspring to resemble their parents. Directional selection: selection that favours extreme trait values. varies in either space [10,11] or time, for instance because Genic capture: female preferences for costly male traits results in the evolution parasites are continually evolving to overcome host of a genetic covariance between condition and trait expression (condition dependence). defences [12,13]. Mutation–selection balance arguments Good genes: models of sexual selection that assume extreme ornaments address the question of whether mutations can generate indicate the genetic quality of the bearer, defined as breeding value for fitness. new genetic variation as quickly as it is eroded by Lek paradox: persistent female choice for particular male trait values should erode genetic variance in male traits and thereby remove the benefits of selection. Here, we discuss recent theoretical develop- choice; and yet choice persists. Most obvious in lekking species where females ments that suggest that the condition-dependent nature of gain no material benefits or parental care from males. Viability: the capacity of an individual to survive, grow and develop. Corresponding author: Tom Tregenza ([email protected]). www.sciencedirect.com 0169-5347/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.03.029 324 Review TRENDS in Ecology and Evolution Vol.19 No.6 June 2004 selected traits does lie in the number of loci involved in their condition-dependent expression [2,17,18]. Sexually Box 1. Predictions of the genic capture hypothesis selected traits are expected to show strong condition The fundamental prediction of good genes models of sexual dependence because they are costly to produce. Crucially, selection, that offspring of preferred males will have higher fitness, the ability of a male to overcome the costs of trait is reasonably well supported [58] (but see [59]). Genic capture makes expression [21] and reap the benefits of female preference explicit the mechanism that is expected to lead to positive covariance between sexual traits and offspring fitness. It rests on the assump- depends upon his viability or ‘condition’. This being so, any tions of condition dependence that arise from the costliness of sexual mutation that affects the overall condition of a male will traits (predictions i and ii) and makes unique predictions (iii–vii). consequently affect his sexually selected traits. Rowe and References are to works from which these predictions arise, Houle [2] called this process GENIC CAPTURE and empha- although, frequently, they are not explicitly stated. sized that it requires only that secondary sexual traits are (i) Expression of sexually selected traits should be strongly dependent upon condition [2,17,18,20,60]. costly and, furthermore, that condition has high genetic (ii) Individuals freed from the costs of producing sexually selected variance. The latter requirement is likely to be met traits should have improved naturally selected fitness components because, as Andersson noticed [19,20], condition will be [2,61]. influenced by any allele that affects the ability of an (iii) Condition should have a high coefficient of genetic variation [2]. individual to acquire and utilize resources. This will (iv) Sexually selected traits should be genetically correlated with condition [21]. include alleles that have environmentally dependent (v) Condition and condition-dependent sexually selected traits effects on fitness, as proposed in the fluctuating selection should be affected by many loci [2,17,18,20,60]. arguments discussed above, and will also mean that the (vi) By increasing the strength of selection on overall condition, total number of loci affecting condition represent a large sexual selection should enable populations to adapt more rapidly to target for mutations [15]. Thus, condition should show changes in environment [23] or to purge genetic load [49,50] (vii) Traits that are more costly capture more condition-dependent large genetic variance and be closely associated with variation [2,17]. fitness. Genic capture is the concept that a large proportion of the genome will become involved in determining the expression of sexually selected traits. This has been storage and expenditure of resources. However, the crucial explicitly modelled in two ways: first, using a quantitative question is what net effect does that trait have on the genetic approach [22] with deleterious mutations as a resource dynamic? Non-reproductive traits are generally source of variance; and second, using an individual-based selected for their ability to increase resource acquisition genetic simulation [23], allowing for changes in the ability, which requires keeping the individual healthy and environment to provide additional genetic variance in alive. The notion of the net effect of many independent condition. Both models lead to the evolution of costly male traits and, ultimately, many loci controlling net resource sexual traits and female preferences (but see [24]). The acquisition ability [27] is central to our understanding of models show that, if males can enhance their sexually the concept of genic capture. Storage of resources promotes selected traits by increased
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