PT - JOURNAL ARTICLE AU - Courtney M. Schroeder AU - Sarah A. Tomlin AU - John R. Valenzuela AU - Harmit S. Malik TI - A rapidly evolving actin mediates fertility and developmental tradeoffs in <em>Drosophila</em> AID - 10.1101/2020.09.28.317503 DP - 2020 Jan 01 TA - bioRxiv PG - 2020.09.28.317503 4099 - http://biorxiv.org/content/early/2020/09/28/2020.09.28.317503.short 4100 - http://biorxiv.org/content/early/2020/09/28/2020.09.28.317503.full AB - Most actin-related proteins (Arps) are highly conserved in eukaryotes, where they carry out well-defined cellular functions. Drosophila and mammals also encode divergent non-canonical Arps in their male-germline whose roles remain unknown. Here, we show that Arp53D, a rapidly-evolving Drosophila Arp, localizes to fusomes and actin cones, two male germline-specific actin structures critical for sperm maturation, via its non-canonical N-terminal tail. Although we expected that Arp53D loss would reduce male fertility, we instead find that Arp53D-KO males are more fertile, both in isolation and in competition with wildtype males. Upon investigating why evolution would retain a gene that negatively impacts male fertility, we unexpectedly found that Arp53D-KO females are less fertile. Moreover, KO embryos exhibit reduced viability, which worsens under heat stress. We conclude that ‘testis-specific’ Arp53D is detrimental to male fertility, but is required for female fertility and early development, leading to its long-term retention and recurrent adaptation in Drosophila.Competing Interest StatementThe authors have declared no competing interest.