Puniamoorthy Nalini, Su Kathy Feng-Yi, Meier Rudolf
Department of Biological Sciences, National University of Singapore, 14 Science Dr 4, Singapore 117543, Singapore.
BMC Evol Biol. 2008 May 21;8:155. doi: 10.1186/1471-2148-8-155.
Sexually dimorphic structures contribute the largest number of morphological differences between closely related insect species thus implying that these structures evolve fast and are involved in speciation. The current literature focuses on the selective forces that drive these changes, be it 'sexual conflict' or 'female choice'. However, there are only few studies examining the function of sexual dimorphisms and even fewer that investigate how functional changes influence dimorphisms. This is largely due to the paucity of taxa for which the morphology, behavior, and phylogenetic relationships for multiple species are known. Here we present such data for sepsid flies. Sepsids have starkly dimorphic forelegs whose function can be documented under laboratory conditions. We use data from 10 genes to reconstruct the phylogenetic relationships for 33 species and test whether mounting positions are correlated with the presence and absence of sexual dimorphisms in the forelegs.
The phylogenetic tree fully resolves the relationship with 29 of the 31 nodes of the tree having a posterior probability of 1.0. Twenty-eight of the 31 sepsid species have sexually dimorphic forelegs. All 28 species with such forelegs have the same mounting technique whereby the male uses his modified forelegs to grasp the female wingbase. Mapping mounting behavior and foreleg morphology onto the tree reveals that the wing grasp evolved once and was reduced twice. All changes in the mounting behavior are strictly and statistically significantly correlated with the origin and losses of sexually dimorphic legs (concentrated changes test: P < 0.001); i.e., the two species that have independently lost the wing grasp have both also re-evolved monomorphic legs. The wing grasp in these species is replaced with a novel but very similar mounting technique not involving the forelegs: the males bend their abdomens forward and directly establish genital contact to the female. In addition, one of the secondarily monomorphic species, Sepsis secunda, has evolved a new sexual dimorphism, a 'bump' on the dorsal side of the 4th tergite, which is now touching the ventral side of the female abdomen.
Our study reveals that the evolution of sexually dimorphic legs in Sepsidae can only be understood once the function of the legs during mating is considered and the relationships of species with and without sexual dimorphisms are known. We demonstrate that homoplasy in sexually dimorphic structures can be due to homoplasy in mating behavior. We furthermore document that the two species with secondarily monomorphic legs have independently replaced the typical sepsid wing grasp with very similar, new mounting techniques. This suggests that convergent evolution may be common in mating behaviors.
两性异形结构在亲缘关系密切的昆虫物种之间造成了数量最多的形态差异，这意味着这些结构进化迅速且参与了物种形成过程。当前的文献主要关注驱动这些变化的选择力量，无论是“性冲突”还是“雌性选择”。然而，仅有少数研究考察了两性异形的功能，而研究功能变化如何影响两性异形的则更少。这主要是因为对于多个物种的形态、行为和系统发育关系都已知的分类单元数量稀少。在此，我们展示了关于蚤蝇的数据。蚤蝇具有明显两性异形的前腿，其功能在实验室条件下可以得到记录。我们使用来自10个基因的数据重建了33个物种的系统发育关系，并测试交配姿势是否与前腿两性异形的有无相关。
系统发育树完全解析了各物种间的关系，该树31个节点中的29个节点的后验概率为1.0。31种蚤蝇中有28种具有两性异形的前腿。所有这28种具有此类前腿的物种都有相同的交配技术，即雄性使用其经过改造的前腿抓住雌性的翅基部。将交配行为和前腿形态映射到树上表明，翅抓握行为进化了一次，退化了两次。交配行为的所有变化都与两性异形腿部的起源和消失严格且在统计学上显著相关（集中变化检验：P < 0.001）；也就是说，两个独立失去翅抓握行为的物种也都重新进化出了单态的腿部。这些物种中的翅抓握行为被一种新的但非常相似的不涉及前腿的交配技术所取代：雄性将腹部向前弯曲并直接与雌性建立生殖器接触。此外，次生单态物种之一，即二等蚤蝇，进化出了一种新的两性异形特征，在第4背板的背侧有一个“凸起”，现在它会接触到雌性腹部的腹侧。
我们的研究表明，只有在考虑到腿部在交配过程中的功能以及已知有或没有两性异形的物种之间的关系后，才能理解蚤蝇科两性异形腿部的进化。我们证明了两性异形结构中的同形现象可能是由于交配行为中的同形现象导致的。我们还记录到，两个具有次生单态腿部的物种独立地用非常相似的新交配技术取代了典型的蚤蝇翅抓握行为。这表明趋同进化在交配行为中可能很常见。
