Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Israel.
Department of Entomology, Huck Institutes of the Life Sciences, Pennsylvania State University.
Genome Biol Evol. 2018 Nov 1;10(11):2947-2960. doi: 10.1093/gbe/evy204.
Understanding the molecular evolutionary basis of social behavior is a major challenge in evolutionary biology. Social insects evolved a complex language of chemical signals to coordinate thousands of individuals. In the fire ant Solenopsis invicta, chemical signals are involved in the determination of a polymorphic social organization. Single-queen (monogyne) or multiqueen (polygyne) social structure is determined by the "social chromosome," a nonrecombining region containing ∼504 genes with two distinct haplotypes, SB and Sb. Monogyne queens are always SBB, while polygyne queens are always SBb. Workers discriminate monogyne from polygyne queens based on olfactory cues. Here, we took an evolutionary genomics approach to search for candidate genes in the social chromosome that could be responsible for this discrimination. We compared the SB and Sb haplotypes and analyzed the evolutionary rates since their divergence. Notably, we identified a cluster of 23 odorant receptors in the nonrecombining region of the social chromosome that stands out in terms of nonsynonymous changes in both haplotypes. The cluster includes twelve genes formed by recent Solenopsis-specific duplications. We found evidence for positive selection on several tree branches and significant differences between the SB and Sb haplotypes of these genes. The most dramatic difference is the complete deletion of two of these genes in Sb. These results suggest that the evolution of polygyne social organization involved adaptations in olfactory genes and opens the way for functional studies of the molecular mechanisms underlying social behavior.
理解社会行为的分子进化基础是进化生物学的主要挑战之一。社会性昆虫进化出了一种复杂的化学信号语言，以协调成千上万的个体。在红火蚁 Solenopsis invicta 中，化学信号参与了多态社会结构的决定。单后（单巢）或多后（多巢）社会结构由“社会染色体”决定，这是一个不重组的区域，包含约 504 个具有两种不同单倍型 SB 和 Sb 的基因。单后蚁总是 SBB，而多后蚁总是 SBb。工蚁根据嗅觉线索区分单后蚁和多后蚁女王。在这里，我们采用进化基因组学方法，在社会染色体中搜索可能负责这种区分的候选基因。我们比较了 SB 和 Sb 单倍型，并分析了自它们分化以来的进化率。值得注意的是，我们在社会染色体的非重组区域中发现了一组 23 个嗅觉受体，它们在两个单倍型中的非同义变化方面尤为突出。该簇包括由最近的 Solenopsis 特异性复制形成的 12 个基因。我们发现了几个树分支上存在正选择的证据，以及这些基因的 SB 和 Sb 单倍型之间的显著差异。最显著的差异是 Sb 中两个基因的完全缺失。这些结果表明，多巢社会结构的进化涉及嗅觉基因的适应性，并为研究社会行为的分子机制的功能研究开辟了道路。
