Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

研究从合作的、社会性的生活史到剥削性的社会寄生的行为和生活史的转变，可以破译行为和社会组织的变化导致多样化的条件。全北极蚁属Formica非常适合研究社会寄生进化，因为其 172 个物种中有一半是已确认或怀疑的社会寄生生物，其中包括蚂蚁中已知的所有三个主要社会寄生类别。然而，与该属社会寄生进化相关的生活史转变在很大程度上尚未被探索。为了测试有关社会寄生的起源和进化的相互竞争的假设，我们重建了福米卡蚁的全球系统发育。该属起源于约 30 Ma 前的旧大陆，并多次传播到新大陆并返回。在福米卡内部，专性依附殖民地建立行为曾经源于兼任一夫多妻制的共同祖先，实行独立和兼性依附殖民地基础。暂时的社会寄生可能先于专性依赖群体的建立或同时出现，并且杜洛社会寄生一旦在专性依赖群体建立的进化枝内进化出来。永久性社会寄生从很少进行群体出芽的临时社会寄生祖先进化了两次，这表明专性社会寄生可能起源于社会多态生物中的兼性寄生背景。与其他属的永久社会寄生蚂蚁相比，福米卡的高寄生虫多样性可能起源于异域物种形成，突出了趋同进化轨迹的多样性，导致几乎相同的寄生生活史综合症。