The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies. Ischnura

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the Common Bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male-mimicry originated in an ancestrally sexually-dimorphic lineage in association with multiple structural changes, probably driven by TE transposition. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male-mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes, can give rise to novel and complex phenotypic polymorphisms.

性限形态（sex-limited morphs）可为复杂表型的演化及基因组结构研究提供深刻洞见。性间拟态（inter-sexual mimicry）是性限多态（sex-limited polymorphism）的一类特殊形式，即某一新颖形态与异性相似。尽管雌雄两性及多样动物类群中均已报道性间拟态个体，但其演化起源仍未得到充分阐释。本研究针对普通蓝尾豆娘（Common Bluetail damselfly）的雌性限性形态与雄性拟态现象，解析其基因组基础。此前已有研究报道豆娘类群中不同形态间存在基因表达差异，但尚未明确其因果位点。本研究发现，雄性拟态起源于一个曾具有两性异形的祖先支系，伴随多重结构变异发生，该变异可能由转座因子（transposable element, TE）转座驱动。上述变异产生了约900 kb的全新基因组序列，该序列在近缘类群的雄性拟态个体中存在部分共享，这表明雄性拟态属于跨物种多态现象。更近的演化事件中，一段雄性拟态序列易位至约3.5 兆碱基（megabase, Mb）外的基因组位点，由此产生了第三种形态。本研究提供了平衡选择维持雄性拟态的证据，这与此前野外种群研究的结论相符。本研究结果凸显：仅需影响少量潜在调控基因及形态特异性基因的结构变异，即可催生新颖且复杂的表型多态现象。