An empirical test of the bet-hedging polyandry hypothesis: female red flour beetles avoid extinction via multiple mating

Bet-hedging via polyandry (spreading the extinction risk of the female’s lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when “unsuitable” males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet-hedging strategy, empirical tests are scarce. In the present study, we tested the bet-hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet-hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet-hedging polyandry hypothesis.

基于一妻多夫制（polyandry）的风险分摊策略（bet-hedging，即将雌性谱系的灭绝风险分摊至多个雄性身上），或可解释雌性多次交配行为的演化——此类行为广泛分布于各类动物和植物分类群中。该假说提出，当种群中频繁出现“不适配”雄性（即因各类原因导致繁殖失败的雄性）且雌性无法识别此类不适配配偶时，雌性可通过一妻多夫交配提升自身进化适合度。尽管近期的理论研究已证实一妻多夫可作为风险分摊策略，但相关实证检验仍较为匮乏。本研究以赤拟谷盗（Tribolium castaneum）为实验材料，对风险分摊型一妻多夫假说进行了检验：我们设置了单夫制（monandry）与一妻多夫制（polyandry）两种处理组，让雌性与从包含20%辐照（不育）雄性的实验种群中随机采集的雄性交配，比较两组雌性的繁殖成功率。此外，我们以多代几何平均适合度作为风险分摊性状适应性的评价指标。结果显示，与单夫制雌性相比，一妻多夫制雌性的卵孵化率显著更高，几何平均适合度也更优。上述研究结果为风险分摊型一妻多夫假说提供了强有力的支持。