The last piece of the puzzle? Phylogenetic position and natural history of the monotypic fungus-farming ant genus Paramycetophylax (Formicidae: Attini).

The evolutionary history of fungus-farming ants has been the subject of multiple morphological, molecular phylogenetic, and phylogenomic studies. Due to its rarity, however, the phylogenetic position, natural history, and fungal associations of the monotypic genus Paramycetophylax have remained enigmatic. Here we report the first excavations of colonies of Paramycetophylax bruchi and describe its nest architecture and natural history. Utilizing specimens from these collections, we generated ultraconserved-element (UCE) data to determine the evolutionary position of Paramycetophylax within the fungus-farming ants and ribosomal fungal barcoding ITS sequence data to identify the fungal cultivar. A maximum-likelihood phylogenomic analysis indicates that the genus Paramycetophylax is the sister group of the yeast-cultivating Cyphomyrmex rimosus group, an unexpected result that renders the genus Cyphomyrmex paraphyletic. A Bayesian divergence-dating analysis indicates that Paramycetophylax diverged from its sister group around 36 mya (30-42 mya, HPD) in the late Eocene-early Oligocene, a period of global cooling, expansion of grasslands, and large-scale extinction of tropical organisms. Bayesian analysis of the fungal cultivar ITS gene fragment indicates that P. bruchi practices lower agriculture and that the cultivar grown by P. bruchi belongs to the Clade 1 group of lower-attine fungi, a clade that, interestingly, also includes the C. rimosus-group yeast cultivars. Based on these results, we conclude that a better understanding of P. bruchi and its fungal cultivar, including whole-genome data, is critical for reconstructing the origin of yeast agriculture, a major transition in the evolution of fungus-farming ants.

培菌蚂蚁的演化历史一直是多项形态学、分子系统发育学及系统基因组学研究的核心议题。然而由于该类群极为稀有，单型属Paramycetophylax的系统发育位置、自然历史及与真菌的共生关系始终难以捉摸。本研究首次对Paramycetophylax bruchi的蚁巢进行发掘，并对其巢室结构与自然历史展开描述。本研究利用此次发掘获得的标本，获取了超保守元件（UCE）数据以明确Paramycetophylax属在培菌蚂蚁中的演化位置，同时通过真菌核糖体条形码ITS序列数据鉴定其共生的栽培真菌。最大似然系统基因组学分析结果显示，Paramycetophylax属与培育酵母的Cyphomyrmex rimosus种群互为姊妹群，这一意外结果导致Cyphomyrmex属成为并系群。贝叶斯分化定年分析表明，Paramycetophylax属与其姊妹群的分化时间约为36百万年前（30-42百万年前，最高后验密度区间），正值始新世晚期至渐新世早期——这一时期全球气候变冷、草原扩张，同时发生了大规模热带生物灭绝事件。对栽培真菌ITS基因片段的贝叶斯分析显示，P. bruchi采用低级培菌农业模式，其栽培的真菌属于低等培菌蚁真菌的Clade 1进化枝；有趣的是，该进化枝同时包含C. rimosus种群的酵母栽培菌种。基于上述结果，本研究认为，若要重建酵母培菌农业的起源——这是培菌蚂蚁演化历程中的一次重大转变，我们需要对P. bruchi及其共生栽培真菌（包括全基因组数据）展开更深入的研究。