Spermatophore retention may accommodate sexual signal loss in pacific field crickets

Sexual signals are gained and lost over evolutionary time. While signal gain has obvious fitness benefits, signal loss should present significant costs due to decreased mating opportunities. Because sexual signal loss has rarely been observed in real time, it is unclear how this process unfolds in nature. Just as female mating preferences can promote evolutionary gain and elaboration of sexual signals, they may also facilitate signal loss. We investigated how two components of female mate choice are involved in rapid sexual signal loss in the Pacific field cricket (Teleogryllus oceanicus), in which many males have lost the ability to sing. Males that can sing (“normal-wings”) and obligately silent males (“flatwings”) coexist in Hawaiian populations. While we know that females prefer not to mate with flatwings, we tested whether females discriminate against flatwing males before copulation due to the lack of song, or something inherent about their wing morphology. We combined this assessment with a test of post-copulatory preference by presenting females with either a normal-wing or flatwing male in the presence or absence of a courtship song stimulus. Females took significantly longer to mount males in the absence of courtship song regardless of male wing morph. This is the first evidence that females discriminate against the absence of song during mate choice, not male wing morph. However, females retained spermatophores for equally long regardless of male wing morph and whether they heard courtship song. Pre- and post-copulatory sexual selection do not operate synchronously in this system, which may help explain the success of the silent morph in wild populations.

性信号（sexual signals）在进化时间尺度上不断获得与丢失。信号获得具备明确的适合度（fitness）收益，而信号丢失则会因交配机会减少而带来显著代价。由于实时观测到性信号丢失的案例极少，目前学界对该过程在自然环境中的具体演化机制仍不明确。正如雌性择偶偏好可推动性信号的演化获得与精细化修饰，这类偏好同样可能促进性信号的丢失。本研究以太平洋田野蟋蟀（Pacific field cricket, *Teleogryllus oceanicus*）为对象，该物种种群中诸多雄性已丧失鸣唱能力，夏威夷种群中同时存在可鸣唱的“正常翅型（normal-wings）”雄性与专性沉默的“平翅型（flatwings）”雄性。此前已知雌性倾向于不与平翅型雄性交配，本研究进一步检验：雌性在交配前（pre-copulatory）对平翅型雄性的排斥，究竟源于其无法鸣唱，还是平翅型雄性本身的翅型形态固有特征？我们将两项评估相结合：一是为雌性提供正常翅型或平翅型雄性，并设置存在/不存在求偶鸣唱刺激的组别，以此检验雌性的交配前择偶偏好；二是开展交配后（post-copulatory）偏好测试。实验结果显示，无论雄性翅型如何，当无求偶鸣唱刺激时，雌性攀附雄性的时长显著延长。本研究首次证实，雌性在择偶过程中排斥的是鸣唱的缺失，而非雄性的翅型形态本身。不过，无论雄性翅型如何、是否接触到求偶鸣唱刺激，雌性保留精荚（spermatophores）的时长均无显著差异。该系统中交配前与交配后性选择并未同步发挥作用，这或可解释沉默翅型在野生种群中的存续优势。