Telomere-to-Telomere Genome Assembly UncoversWolbachia-Driven Sex-Specific Demography and Challenges Fisher’s Principle in a Sawfly

Abstract

Wolbachia, a widespread endosymbiotic bacterium, can reshape the evolutionary fates of its insect hosts by distorting reproduction and altering population dynamics. Despite extensive laboratory research, its long-term effects on host evolution in nature remain poorly understood, particularly regarding genetic mechanisms underlying changes in sex determination and reproduction. Here, we report the first telomere-to-telomere (T2T) genome assembly of the sawflyAnalcellicampa danfengensisand the complete genome of it symbioticWolbachia. Comparative population genomics of six closely relatedAnalcellicampaspecies revealed thatWolbachia-infected populations experience marked changes in sex-specific demography. While uninfected species maintain balanced genetic features between males and females, infected species show a persistent reduction in male effective population size alongside a stable or even growing female population, ultimately driving males toward extinction. Genomic scans identified positively selected genes associated with reproductive functions, sensory perception, neural development, and longevity, suggesting thatWolbachiamanipulates critical host biological pathways to promote its transmission. These findings provide direct genomic evidence thatWolbachiaacts as a powerful evolutionary force, reshaping host genomes in a way that disrupts Fisher’s principle, ultimately driving female-biased demography and the extinction of males at evolutionary timescales. This work provides deeper insights into host– endosymbiont coevolution and has important implications for evolutionary theory and pest management strategies.