A sexually-selected male weapon characterised by strong additive genetic variance and no evidence for sexually antagonistic polyphenic maintenance

Sexual selection and sexual antagonism are important drivers of eco-evolutionary processes. The evolution of traits shaped by these processes depends on their genetic architecture, which remains poorly studied. Here, implementing a quantitative genetics approach using diallel crosses of the bulb mite, Rhizoglyphus robini, we investigated the genetic variance that underlies a sexually-selected weapon that is dimorphic among males and female fecundity. Previous studies indicated that a negative genetic correlation between these two traits likely exists. We found male morph showed considerable additive genetic variance, which is unlikely to be explained solely by mutation-selection balance, indicating the likely presence of large-effect loci. However, a significant magnitude of inbreeding depression also indicates that morph expression is likely to be condition-dependent to some degree and that deleterious recessives can simultaneously contribute to morph expression. Female fecundity also showed a high degree of inbreeding depression, but variance in female fecundity was mostly explained by epistatic effects, with very little contribution from additive effects. We found no significant genetic correlation, nor any evidence for dominance reversal, between male morph and female fecundity. The complex genetic architecture underlying male morph and female fecundity in this system has important implications for our understanding of the evolutionary interplay between purifying selection and sexually antagonistic selection.

Methods
Inbred lines of the bulb mite, Rhizoglyphus robini, were established from wild-caught individuals using full sib x sib mating for 14 generations. Males of the species are dimorphic, with fighter males expressing an enlarged and thickened third pair of legs which are used in combat with other males, in contrast, scrambler males have legs with all approximately equal thickness. The morph of each P-generation male was recorded and in subsequent generations of inbreeding, the same male morph was used, thus giving inbred lines fixed for fighter and scrambler alleles.

Using diallel crossing, males and females from each inbred line were crossed with other inbred lines. The offspring produced by each cross were either 1) individually isolated and the fecundity of F1 females determined or 2) reared in small groups and the frequency of each male morph recorded.

Using a Bayesian modeling approach, we partitioned the variance of each trait into additive effects, parental-sex effects, dominance effects and epistatic effects, plus noise. Furthermore, we investigated dominance relationships of these traits by calculating array covariances.

性选择与性拮抗作用是生态进化过程的关键驱动因子。由这些过程塑造的性状演化，取决于其遗传架构，目前相关研究仍较为匮乏。本研究以罗宾根螨（Rhizoglyphus robini）为研究对象，采用双列杂交（diallel crosses）的数量遗传学方法，探究了雄性二态性性选择武器以及雌性繁殖力的遗传变异基础。既往研究提示，这两种性状间可能存在负遗传相关。
我们发现，雄性形态具有显著的加性遗传方差（additive genetic variance），且该方差难以仅由突变-选择平衡解释，提示可能存在大效应基因座。不过，近交衰退（inbreeding depression）的显著程度也表明，雄性形态的表达在一定程度上依赖于个体条件，且有害隐性等位基因可同时参与形态调控。雌性繁殖力同样表现出较强的近交衰退现象，但该性状的变异主要由上位效应（epistatic effects）解释，加性效应的贡献极小。我们未发现雄性形态与雌性繁殖力间存在显著遗传相关，也未找到性状显性逆转的相关证据。本系统中雄性形态与雌性繁殖力背后的复杂遗传架构，有助于我们深入理解净化选择与性拮抗选择间的进化互作关系。

方法
本研究通过全同胞兄妹交配14代，从野生捕获的个体中建立了罗宾根螨（Rhizoglyphus robini）的近交系。该物种的雄性存在二态性：战斗型雄性具有特化膨大且增厚的第三对足，用于与其他雄性争斗；而漫游型雄性的各对足厚度均一。我们记录了亲本代（P代）每只雄性的形态类型，并在后续近交世代中保留相同的雄性形态，由此获得固定为战斗型等位基因与漫游型等位基因的近交系。
通过双列杂交实验，我们将每个近交系的雄性与雌性与其他近交系进行交配。每一组杂交产生的后代分为两类：1）单独隔离饲养，测定F1代雌性的繁殖力；2）小群体饲养，记录各雄性形态的出现频率。
本研究采用贝叶斯建模方法，将每种性状的方差分解为加性效应、亲本性别效应、显性效应、上位效应以及随机噪声。此外，我们通过计算杂交阵列协方差，探究了这些性状的显性关系。