Nephilid spiders are known for gigantic females and tiny males. Such extreme sexual dimorphism and male‐biased sex ratios result in fierce male–male competition for mates. Intense sperm competition may be responsible for behaviors such as mate guarding, mate binding, opportunistic mating, genital mutilation, mating plugs and male castration (eunuchs). We studied the mating biology of two phylogenetically, behaviorally and morphologically distinct south‐east Asian nephilid spider species (Herennia multipuncta, Nephila pilipes) in nature and in the laboratory. Specifically, we established the frequencies and effectiveness of plugging (a plug is part of the male copulatory organ), and tested for male and female copulatory organ reuse. Both in nature and in the laboratory, plug frequencies were higher in H. multipuncta (75–80% females plugged) compared with N. pilipes (45–47.4%), but the differences were not significant. Plugs were single and effective (no remating) in H. multipuncta but multiple and ineffective (remating possible) in N. pilipes. In Herennia, the males plugged when the female was aggressive and in Nephila plugging was more likely when mating with previously mated and larger females. Further differences in sexual biology are complete palpal removal and higher sexual aggressiveness in Herennia (sexual cannibalism recorded for the first time), and mate binding in Nephila. Thus, we propose the following evolutionary hypothesis: nephilid plugging was ancestrally successful and enabled males to monopolize females, but plugging became ineffective in the phylogenetically derived Nephila. If the evolution of nephilid sexual mechanisms is driven by sexual conflict, then the male mechanism to monopolize females prevailed in a part of the phylogeny, but the female resistance to evade monopolization ultimately won the arms race.
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