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Reconciling Strong Stabilizing Selection with the 2 Maintenance of Genetic Variation in a Natural Population 3 of Black Field Crickets (Teleogryllus Commodus)

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Reconciling Strong Stabilizing Selection with the 2 Maintenance of Genetic Variation in a Natural Population 3 of Black Field Crickets (Teleogryllus Commodus) Genetics: Published Articles Ahead of Print, published on July 29, 2007 as 10.1534/genetics.107.077057 1 1 Reconciling Strong Stabilizing Selection with the 2 Maintenance of Genetic Variation in a Natural Population 3 of black field crickets (Teleogryllus commodus) 4 John Hunt*†, Mark W. Blows‡, Felix Zajitschek*, Michael D. Jennions§ and Robert Brooks* 5 * Evolution & Ecology Research Centre. The University of New South Wales, Kensington, 6 Sydney, NSW, 2052, Australia. 7 †Centre for Ecology and Conservation, School of Biosciences, University of Exeter, 8 Cornwall Campus, TR10 9EZ, United Kingdom. 9 ‡School of Integrative Biology, University of Queensland, Brisbane, QLD, 4072, Australia. 10 §School of Botany and Zoology, The Australian National University, Canberra ACT, 0200, 11 Australia. 12 13 14 15 2 15 Running Header: Stabilizing selection and genetic variation 16 17 Key words: Stabilizing selection, selection analysis, G matrix, genetic variance, 18 multivariate traits 19 20 Corresponding author: John Hunt, Centre for Ecology and Conservation, School of 21 Biosciences, University of Exeter, Cornwall Campus, TR10 9EZ, United Kingdom. E-mail: 22 [email protected], Phone: +44 (0)1326 371 892, Fax: +44 (0)1326 253 638. 23 24 3 24 ABSTRACT 25 Genetic variation in single traits, including those closely related to fitness, is pervasive and 26 generally high. By contrast, theory predicts that several forms of selection, including 27 stabilizing selection, will eliminate genetic variation. Stabilizing selection in natural 28 populations tends to be stronger than that assumed in theoretical models of the maintenance 29 of genetic variation. The widespread presence of genetic variation in the presence of strong 30 stabilizing selection is a persistent problem in evolutionary genetics that currently has no 31 compelling explanation. The recent insight that stabilizing selection often acts most 32 strongly on trait combinations via correlational selection may reconcile this problem. Here 33 we show that for a set of male call properties in the cricket Teleogryllus commodus, the 34 pattern of multivariate stabilizing sexual selection is closely associated with the degree of 35 additive genetic variance. The multivariate trait combinations experiencing the strongest 36 stabilizing selection harboured very little genetic variation while combinations under weak 37 selection contained most of the genetic variation. Our experiment provides empirical 38 support for the prediction that a small number of trait combinations experiencing strong 39 stabilizing selection will have reduced genetic variance, and that genetically-independent 40 trait combinations experiencing weak selection can simultaneously harbour much higher 41 levels of genetic variance. 42 43 44 4 44 INTRODUCTION 45 The presence of genetic variation in almost all traits has been exhaustively documented in 46 natural populations (LYNCH and WALSH 1998; PARTRIDGE and BARTON 2000), and yet 47 explaining the maintenance of this variation in the presence of selection represents one of 48 the most persistent challenges in evolutionary biology (BARTON and KEIGHTLEY 2002; 49 BARTON and TURELLI 1989; BLOWS and HOFFMANN 2005). Traits strongly associated with 50 fitness tend to show lower heritabilities than those less strongly associated with fitness 51 (GUSTAFSSON 1986; MOUSSEAU and ROFF 1987), but this is a consequence of these traits 52 tending to have higher environmental variances (HOULE 1992). When scaled appropriately, 53 traits closely related to fitness tend to harbour more genetic variation than those more 54 distant from fitness (HOULE 1992). 55 Several forms of selection, particularly stabilizing selection, should deplete genetic 56 variation (BARTON and KEIGHTLEY 2002; BARTON and TURELLI 1989; BÜRGER 2000; ROFF 57 1997). Although stabilizing selection is not more common than other types of nonlinear 58 selection in natural populations (BROOKS et al. 2005; KINGSOLVER et al. 2001), when it 59 occurs it is much stronger than assumed in theoretical models (JOHNSON and BARTON 60 2005). Moreover, stabilizing selection is likely to be a widespread cause of stasis over 61 longer evolutionary timescales (ESTES and ARNOLD 2007). The ubiquity of genetic 62 variation despite the presence of stabilizing selection currently has no compelling 63 explanation (JOHNSON and BARTON 2005). The conflict between these two fundamental 64 observations has provided the impetus for the large body of theory devoted to exploring 65 whether a balance between mutation and stabilizing selection can maintain genetic 66 variation (JOHNSON and BARTON 2005; KONDRASHOV and TURELLI 1992; SLATKIN and 67 FRANK 1990; ZHANG and HILL 2003; ZHANG et al. 2002), or whether other mechanisms are 68 required to maintain genetic variance, such as balancing selection generated by 5 69 environment- or sex-specific effects (TURELLI and BARTON 2004), or frequency- or density- 70 dependent dependent selection (BÜRGER 2005). Our purpose here is not to investigate any 71 one of these potential mechanisms for maintaining genetic variance, but to critically 72 evaluate the fundamental observation of the ubiquity of genetic variance in the presence of 73 stabilizing selection. 74 Direct empirical tests of the effect of stabilizing selection on the genetic variance in 75 natural populations are difficult because genetic variances, estimates of the strength of 76 stabilizing selection, and mutation rates must be quantified simultaneously (ZHANG et al. 77 2002). A first step, however, is to determine the association between the strength of 78 stabilizing selection and the magnitude of genetic variance in natural populations (BARTON 79 and TURELLI 1989). There are two key difficulties in implementing this approach. First, 80 quantifying true stabilizing selection on a set of traits, as distinct from apparent stabilizing 81 selection generated by unmeasured traits, requires the focal traits to be manipulated in 82 isolation from all other traits (JOHNSON and BARTON 2005; ROBERTSON 1967). Second, 83 almost all single traits tend to display substantial heritabilities (BLOWS and HOFFMANN 84 2005; LYNCH and WALSH 1998; PARTRIDGE and BARTON 2000; ROFF 1997) and theory 85 shows that many traits cannot be under true stabilizing selection simultaneously (BARTON 86 1990). Simply associating single-trait heritabilities or estimates of genetic variance with 87 measures of stabilizing selection on each trait is an inadequate approach to test this 88 hypothesis (JOHNSON and BARTON 2005), because stabilizing selection often acts most 89 strongly on trait combinations via correlational selection (BLOWS and BROOKS 2003; 90 LANDE and ARNOLD 1983; PHILLIPS and ARNOLD 1989). Here we use an example of true 91 multivariate stabilizing selection on a set of traits, which was quantified in a manipulative 92 experiment (BROOKS et al. 2005), to test the prediction that trait combinations under 93 stronger stabilizing selection will display lower genetic variance. 6 94 95 METHODS 96 Study system 97 Acoustic sexual signals in species like frogs (GERHARDT 1991; POLAKOW et al. 98 1995; RYAN and WILCZYNSKI 1988) and crickets (BROOKS et al. 2005; LOFTUS-HILLS et al. 99 1972; LOHER 1979) are often under stabilizing sexual selection due to sensory tuning or 100 neuronal processing by females. Such traits provide exceptional opportunities to study 101 stabilizing sexual selection because call properties can be manipulated independently from 102 all other aspects of the phenotype using computer software to artificially construct calls and 103 then measuring the attractiveness of these calls in acoustic playback trials. Previously 104 (BROOKS et al. 2005), we independently manipulated five acoustic call properties; trill 105 number (TN); inter-call duration (ICD): chirp inter-pulse duration (CIPD) and dominant 106 frequency (DF)) of the advertisement call of male Australian black field crickets (T. 107 commodus). We showed that these five call properties are under strong multivariate 108 stabilizing sexual selection in controlled laboratory phonotaxis trials (BROOKS et al. 2005) 109 and in the field (BENTSEN et al. 2006). Moreover, the population mean call properties of 110 four independent samples of males, representing two different field collections and four 111 different diet regimes, resided near the multivariate adaptive peak (BROOKS et al. 2005). 112 This experiment therefore provided support for the important prediction that populations 113 should converge on the peak of an adaptive landscape that is characterized by stabilizing 114 selection (ARNOLD 2003; LANDE 1976; SIMPSON 1953). 115 7 116 Breeding design 117 The laboratory stock we used originated from Smith’s Lake (32° 22’S, 152° 30’E), 118 New South Wales, Australia. After capture, the stock was bred for four generations in 119 captivity before the start of this experiment. We mated 52 stock males to 7 dams each. This 120 produced 301 full-sib families, as 63 dams failed to produce offspring. For each family we 121 collected 12 offspring, at random, and reared them to adulthood in individual plastic 122 containers (5 x 5 x 5 cm) in a constant temperature room set to 28° C ± 1° C with a 123 10D:14L light regime. All offspring were provided with food (Friskies Go-Cat® Senior) 124 and water ad libitum and a small piece of egg carton for shelter. Containers were cleaned 125 and fresh food and water provided weekly. 126 127 Measuring call properties 128 At 10 days post-eclosion, males were set up in a constant
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