pre-copulatory choices drive post-copulatory decisions: mechanisms of female control shift across different life stages

The ‘wallflower’ hypothesis proposes females mate indiscriminately to avoid reproductive delays. Post-copulatory mechanisms may then allow ‘trading up’, favouring paternity of future mates. We tested links between pre- and post-copulatory choice in Latrodectus geometricus female spiders paired sequentially with two males. These females copulate as adults or as subadults and store sperm in paired spermathecae. Choosy adults have a higher risk of delays to reproduction than subadults. We predicted low pre-copulatory, but high post-copulatory choice at first matings for adults and the opposite for subadults. At second matings, we expected all females would prefer males superior to their first. We found all females mated indiscriminately at their first pairing, but in contrast to subadults, adults usually copulated only once (leaving one spermatheca empty); a mechanism of post-copulatory choosiness. Adult-mated females were more likely to remate than subadult-mated (adult) females, showing a preference for larger males, while subadult-mated females tended to prefer males in better condition. Our results show that the ‘wallflower’ effect and ‘trading up’ tactics can be linked, allowing females to employ choice even if rejecting males is costly.

Methods

Data were collected in a laboratory experiment in which brown widow females each mated with two males:

First, subadult and adult females mated with naive males.
Next, adult females who had previously mated either as a subadult or adult related with new naive males.

Mating trials were video recorded and the occurrence and timing of courtship and mating behaviours were scored by an observer. See the paper for full details of data collection and analysis.

“‘壁花假说’（wallflower hypothesis）提出，雌性会采取无差别交配策略以规避繁殖延迟风险。后续的交配后机制则可支持‘升级择偶’行为，即偏向于赋予后续配偶更高的父权概率。我们以几何寇蛛（Latrodectus geometricus，俗称褐寡妇蜘蛛）为研究对象，让雌性个体依次与两只雄性配对，以此检验交配前与交配后选择之间的关联。该物种的雌性可在成虫期或亚成虫期完成交配，精子储存于成对的受精囊（spermathecae）中。相较于亚成虫个体，挑剔的成虫个体面临的繁殖延迟风险更高。我们曾提出如下预测：成虫在首次交配时的交配前选择程度较低，但交配后选择程度较高；亚成虫个体则呈现相反模式。在第二次交配环节，我们预期所有雌性个体都会优先选择优于首任配偶的雄性。实验结果显示，所有雌性个体在首次配对时均无差别地完成交配，但与亚成虫雌性不同的是，成虫个体通常仅完成一次交配（导致一个受精囊空置），这属于一种交配后选择机制。与首次交配发生在亚成虫期的雌性相比，首次交配发生在成虫期的雌性更倾向于再次交配，且表现出对体型更大雄性的偏好；而首次交配发生在亚成虫期的雌性则更偏好身体状态更佳的雄性。本研究结果表明，‘壁花效应’与‘升级择偶’策略可以共存，即便拒绝雄性会付出相应代价，雌性依然能够实施择偶行为。

方法

实验数据采集自实验室交配实验，每只褐寡妇雌性个体均与两只雄性完成交配流程：
首先，亚成虫与成虫雌性均与未交配过的雄性个体进行交配。
随后，此前曾以亚成虫或成虫身份完成交配的成虫雌性，与新的未交配雄性个体开展交配实验。
所有交配试验均进行录像记录，由观察者对求偶与交配行为的发生时机及过程进行评分。完整的数据采集与分析细节请参阅研究原文。