A rapidly evolving actin mediates fertility and developmental tradeoffs inDrosophila

Abstract

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.

Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development

“…The question of how often evolutionary new genes develop essential functions is a critical problem in understanding the genetic basis of development and general phenotypic evolution. New genes in evolution have widely attracted discussion [1][2][3][4][5][6], supported by increasing studies with fulsome evidence in various organisms [7][8][9][10][11][12][13]. The detected large number of new genes with unexpected rate of new gene evolution [14][15][16] and the revealed important functions of new genes [2,[17][18][19][20] challenged a widely held dogma that the genetic basis in control of development is conserved in a long time scale of evolution [21][22][23][24].…”

New gene evolution with subcellular expression patterns detected in PacBio-sequenced genomes ofDrosophilagenus

“…These various mechanisms which lead to new gene origination perpetually occur throughout long periods of evolutionary time, thus the origination of new genes is important to explain biological diversity and genomic variation. New genes can rapidly become indispensable and acquire essential functions in diverse processes such as de novo genes related with human health (Toll-Riera et al 2009; Van Oss and Carvunis 2019), new genes formed by duplication resolving intralocus sexual conflict in D. melanogaster (VanKuren and Long 2018; Schroeder et al 2020), and new genes impacting reproductive behavior (Dai et al 2008) and brain evolution (Chen et al 2012). These phenomena are surprising as genes with critical biological functions are thought to be ancient and highly conserved.…”

Genomic Analyses of New Genes and Their Phenotypic Effects Reveal Rapid Evolution of Essential Functions in Drosophila Development

“…Ruiz-Orera et al 2018; Xie et al 2019; Vakirlis et al 2020; Witt et al 2019; Jiang and Assis. 2017; Rogers et al 2014; Schroeder et al 2020). The detected large number of new genes with unexpected rate of new gene evolution (e.g.…”