Genetic basis of female sexual preference in a stalk-eyed fly

公众和科学家们对男性夸张的性装饰是如何通过女性的配偶偏好进化而来的非常感兴趣。最近，人们对性选择的兴趣主要集中在理解男性装饰物变异的原因，包括遗传和环境因素，以及这些特征的信号价值。相比之下，对女性性偏好变化的深入研究一直被忽视。这在一定程度上反映了准确量化偏好的困难——这需要反复测量女性对各种男性刺激的反应，而这通常很难在实验室条件下进行研究。这也反映了对女性偏好行为的可变性和复杂性普遍认识不足。我们已经开发了一个很好的系统来量化非洲柄眼蝇的雌性配偶偏好的变化。在这个物种中，雌性会主动拒绝不想要的雄性交配。这使我们能够制定出精确测量雌性个体择偶偏好的方案。我们之前已经证明，偏好的强度与雌性眼距和雌性繁殖力的表型变异呈正相关。要解决的一个关键问题是女性择偶偏好变异的遗传基础。没有遗传变异，女性偏好就无法进化。我们将首次开展择优遗传学的QTL（数量性状位点）研究。这将揭示潜在的偏好变化的可分离遗传因素的数量。可能有一两个遗传因素具有主要影响，或者在整个基因组中基因的影响大小分布更为均匀。它还将揭示偏好基因的连锁模式，以及是否像某些理论预测的那样，存在对x染色体的偏爱。我们将研究的另一个关键问题是偏好依赖于条件的证据。最近的几项研究表明，在优质资源可自由获得的良好条件下饲养的雌性与在劣质资源下饲养的雌性有不同的偏好。例如，在我们之前的工作中，我们已经表明，能够获得更好的幼虫或成虫资源的雌性柄眼蝇对具有较大性装饰物的雄性具有更强的定向偏好。这对性选择的强度有广泛的影响，如果条件最高的雌性不仅对配偶表现出最大的歧视，而且也是最多产的。我们将使用定量遗传研究来研究条件依赖偏好的遗传学。基因相关的家庭将在三种食物质量不同的环境中长大。环境的变化可能会压倒遗传信号。但从我们之前测量男性特征对环境压力的反应的研究来看，我们并没有预料到这一点。相反，我们认为恶劣的环境会放大女性之间的遗传差异，导致偏好的遗传变异。因此，一些雌性基因型在所有环境中都会持续产生强烈的偏好，而另一些基因型则会随着环境条件的恶化而表现出逐渐下降的偏好。我们将在QTL研究中进一步探讨这一预测。我们已经证明，柄眼蝇的雌性偏好强度与雌性的眼长和雌性的生育能力密切相关，这两个特征分别强烈反映了幼虫和成虫发育期间的可利用资源。我们将检验雌性偏好QTL是否与雌性眼长QTL和雌性繁殖力QTL位于相同的基因组区域。这种模式可能表明，相同的条件基因构成了偏好、眼距和繁殖力等几种特征的基础。

There is considerable interest amongst the general public and scientists in understanding how exaggerated male sexual ornaments have evolved through female mate preferences. Much recent interest in sexual selection has been directed toward understanding the causes of variation in male ornaments, both genetic and environmental, and the signalling value of these traits. In contrast, there has been a neglect of in depth studies of variation in female sexual preferences. This in part reflects the difficulty of accurately quantifying preferences - which requires repeated measures of female responses to a variety of male stimuli, which are often difficult to study under laboratory conditions. It also reflects a general under appreciation of the variability and complexity of female preference behaviour. We have already developed an excellent system for quantifying variation in female mate preference in the African stalk-eyed fly Diasemopsis meigenii. In this species, females actively reject unwanted male mating attempts. This has allowed us to develop protocols to accurately measure individual female mate preferences. We have previously demonstrated that the strength of preference varies positively with phenotypic variation in female eyespan and female fecundity. A key question to address is the genetic underpinnings of variation in female mate preferences. Without genetic variation female preference cannot evolve. We will carry out the first QTL (quantitative trait locus) study of the genetics of preference. This will uncover the number of separable genetic factors underlying variation in preference. It may be that there are one or two genetic factors with major effects or alternatively a more even distribution of effect sizes of genes across the genome. It will also reveal the linkage pattern of preference genes and whether there is a bias towards the X-chromosome, as some theory predicts. Another critical issue that we will investigate is the evidence that preferences are condition-dependent. Several recent studies have shown that females reared under good conditions in which high quality resources are freely available have different preferences than females reared on poor quality resources. For example, in our previous work, we have shown that female stalk-eyed flies with access to better larval or adult resources have stronger directional preferences for males with larger sexual ornaments. This has wide ranging implications for the strength of sexual selection, if the females with the highest condition not only show the greatest discrimination of who they mate with but are also the most fecund. We will investigate the genetics of condition-dependent preferences using a quantitative genetic study. Genetically related families will be raised in three environments which vary in food quality. It is possible that the environmental variation will overwhelm the genetic signal. But from our previous studies measuring the responses of male traits to environmental stress, we do not expect this. Rather we believe that the harsh environment will amplify genetic differences between females, bringing out genetic variation in preference. So some female genotypes will consistently produce strong preference in all environments, whereas others genotypes will show declining preference as environmental conditions deteriorate. We will further probe this prediction in our QTL study. We have already shown that the strength of female preference in stalk-eyed flies covaries with female eyespan and female fertility, two traits that strongly reflect resources available during larval and adult development respectively. We will test whether QTL for female preference are located in the same genomic regions as QTL for female eyespan and QTL for female fecundity. This pattern could indicate that the same genes for condition underlie several traits such as preference, eyespan and fecundity.