The tiniest genomes shrink much further: extreme reductive evolution in planthopper symbionts

Endosymbiotic bacteria that provide limiting nutrients to sap-sucking hemipteran insects are known for their highly reduced genomes conserved in organization and function, a product of long-term co-diversification with hosts. Here, through genomics exploration of ancient Sulcia and Vidania endosymbionts from across 19 families of planthoppers (Hemiptera: Fulgoromorpha), we present multiple departures from that genomic stability. We show that gene have been lost gradually during ~263 my of host-symbiont co-diversification, with more dramatic changes promoted by co-infecting additional microbes and host ecological switches. This has resulted in the convergent evolution, in two planthopper superfamilies, of bacterial genomes at barely 50-52 kb, strikingly similar in gene contents and the ability to produce a single essential amino acid, phenylalanine. Our work identifies key drivers and limits of symbiont reductive genome evolution.