An actin-related protein that is most highly expressed in testes is critical for embryonic development.

Most actin-related proteins (Arps) are highly conserved and carry out well-defined cellular functions in eukaryotes. However, many lineages like and mammals encode divergent non-canonical Arps whose roles remain unknown. To elucidate the function of non-canonical Arps, we focus on , which is highly expressed in testes and retained throughout evolution. We show that Arp53D localizes to fusomes and actin cones, two germline-specific actin structures critical for sperm maturation, via a unique N-terminal tail. Surprisingly, we find that male fertility is not impaired upon loss, yet population cage experiments reveal that is required for optimal fitness in . To reconcile these findings, we focus on function in ovaries and embryos where it is only weakly expressed. We find that under heat stress -knockout (KO) females lay embryos with reduced nuclear integrity and lower viability; these defects are further exacerbated in -KO embryos. Thus, despite its relatively recent evolution and primarily testis-specific expression, non-canonical is required for optimal embryonic development in .