Across metazoans, lifespan is limited by the germline. One cost of the germline may lie in germline transcription, although mechanisms remain elusive. During transcription, the COMPASS complex methylates histone H3 at lysine 4 (H3K4me). The Brunet lab has shown that deficiencies in COMPASS subunits, including WDR-5, extend C. elegans lifespan in a germline-dependent manner. In this study, we demonstrate that longevity in
wdr-5 mutants is a transgenerational trait that only manifests after populations lack WDR-5 for eighteen generations. Surprisingly, the full lifespan increase requires both an increase in
wdr-5 mutants and a decrease in wild type recovering from freezing or starvation. We have previously found that levels of repressive H3K9me2 increase at some genes in
wdr-5 mutants, implicating H3K9me2 in COMPASS mutant longevity. In support of H3K9me2's role, we find that genomic H3K9me2 enrichment correlates with transgenerational changes in longevity in both wild-type and
wdr-5 mutants. Furthermore,
wdr-5 mutant longevity requires the H3K9 methyltransferase MET-2 and is phenocopied by a mutation in the putative H3K9 demethylase JHDM-1. These data indicate that a generational increase in H3K9me2 confers longevity in
wdr-5 mutants. Strikingly, the Brunet lab showed that COMPASS mutant longevity can be inherited by their wild-type descendants. Our finding that H3K9me2 is heritable between generations suggests that it may also function in the inheritance of longevity. Bolstering a role for H3K9me2 in inheritance, we find that longevity of
jhdm-1 mutants is similarly inherited by their wild-type descendants. Finally, we show that MET-2 is required for the inheritance of longevity in wild-type descendants of
wdr-5 mutant. Taken together, our findings strongly implicate H3K9me2 in the epigenetic inheritance of longevity. We present a model in which germline transcription-coupled H3K4me encroaches upon regions of H3K9me2. With each successive generation, the gradual reduction of repressive chromatin limits lifespan. The loss of COMPASS alleviates this burden, extending lifespan as well as enabling the inheritance of this complex trait. Thus, we propose that germlines limit lifespan in part because germline transcription reduces heterochromatin.