Evolutionary genetics of life-history traits in a haplodiploid mite

Two-spotted spider mites hide against predatory mites in a web of self-produced sticky silk. The proteins invested in this shelter may reduce investment in reproduction. Do spider mite populations harbour genetic variation for web production, thereby enabling a response to selection by predation? Is adaptation affected by genetic trade-offs with life-history traits? The data were also used to test a central hypothesis in quantitative genetics, that heritability indicates a trait’s importance for fitness and is positively correlated with the amount of additive genetic variation across traits. Using a mother–daughter breeding design, we determined the narrow-sense heritability and coefficients of additive genetic and residual variation (CVA and CVR) for web production and six life-history traits. In addition, we examined correlations between heritable traits for genetic trade-offs. Web production exhibited heritability of 50% and a high CVA. Thus, web production is not a fixed defence-related trait, and probably has the potential to evolve. Two life-history traits (oviposition rate and total adult offspring) revealed significant heritable variation. Results were inconclusive regarding genetic trade-off with web production. The life-history data demonstrate a positive relationship between heritability and CVA, which supports the hypothesis that the relationship of traits with fitness influences their amount of heritable variation. M species of spider mites in the subfamily Tetranychinae produce silken threads, but the quantity produced and the way in which silk is used differ markedly among species (Saito 1985). The two-spotted spider mite, Tetranychus urticae, has one of the highest rates of silk production, spinning silken threads whenever it moves around (Saito 1985). The adults and their offspring live within the web, which has been shown to be successful as a defence against predatory mites (Sabelis 1985; Sabelis and Bakker 1992). The sticky and chaotic web impedes the movement of predatory mites, which may even become stuck and die. Some predator species cannot enter an area with T. urticae webbing (such as Amblyseius andersoni), whereas others (such as the specialist predator of T. urticae, Phytoseiulus persimilis AthiasHenriot) are less hindered unless the web has become very dense, which occurs when spider mites over-exploit their host plant (Sabelis 1985). 2 We assume that the fitness effects of producing silk depend on the level of predation. Thus, when predation is high, good defensive abilities will contribute greatly to individual fitness. Hence, selection on web production may be strong. The first question to arise is whether there is potential for web production to evolve. A second, related question is whether the evolution of web production is influenced by genetic trade-offs. The production of silk to create a web requires mites to metabolize large amounts of amino acids (Hazan et al. 1975). Given the limited amount of resources an individual can procure and utilize, production of silk may come at a cost to other fitness-determining traits, such as growth and reproduction. Amino acids are metabolized via different biochemical pathways. The determination of the flux of amino acids through these pathways may have a genetic basis and this may generate a genetic trade-off between traits (Zera and Zhao 2006). The questions above can be addressed by a quantitative genetic approach (Falconer and Mackay 1996). To address whether web production has the potential to adapt to predation pressure, we assessed the similarity between parent and offspring and calculated two measures of the amount of additive genetic variation (VA) in the population: the narrow-sense heritability and the coefficient of additive genetic variation. The narrow-sense heritability, h2, estimates the share of the phenotypic variation in a population that is additive genetic and thereby the potential strength of a response to selection (Falconer and Mackay 1996), since selection acts on the total phenotypic variation, whereas adaptation emerges from selection on genetic variation only. The coefficient of additive genetic variation, CVA, estimates VA scaled by the trait mean, which enables comparison between traits (Houle 1992). To examine the second question, whether genetic trade-offs exist between web production and life-history traits, the correlations between traits with heritable variation were determined (Falconer and Mackay 1996). A final issue that we investigated relates to a controversy in quantitative genetics about the relationship between fitness and VA (Stirling et al. 2002). Classical theory states that natural selection shapes the amount of VA of a trait: if a trait is important for fitness, selection acts strongly on that trait and consequently erodes much of the VA in the population (Falconer and Mackay 1996). In that case, across traits both heritability and CVA are negatively correlated with the trait’s importance for fitness and positively correlated to each other. This mechanism is known as the ‘eliminationselection hypothesis’ (Stirling et al. 2002). In contrast, the amount of VA in a trait can also be shaped by how integrated the trait is (Price and Schluter 1991; Houle 1992). This so-called ‘variance compounding hypothesis’ (Stirling et al. 2002) states that a trait further down the causal pathway from genes to phenotype (Price and Schluter 1991) (and thus more highly integrated) accumulates more genetic variation and also more environmental variation. However, how integrated the trait is affects VA less