A putative novel role for Eip74EF in male reproduction in promoting sperm elongation at the cost of male fecundity

Abstract

Spermatozoa are the most morphologically variable cell type, yet little is known about genes controlling natural variation in sperm shape. Drosophila fruit flies have the longest sperm known, which are evolving under postcopulatory sexual selection, driven by sperm competition and cryptic female choice. Long sperm outcompete short sperm but primarily when females have a long seminal receptacle (SR), the primary sperm storage organ. Thus, selection on sperm length is mediated by SR length, and the two traits are coevolving across the Drosophila lineage, driven by a genetic correlation and fitness advantage of long sperm and long SR genotypes in both males and females. Ecdysone induced protein 74EF (Eip74EF) is expressed during postmeiotic stages of spermatogenesis, when spermatid elongation occurs, and we found that it is rapidly evolving under positive selection in Drosophila. Hypomorphic knockout of the E74A isoform leads to shorter sperm but does not affect SR length, suggesting that E74A may be involved in promoting spermatid elongation but is not a genetic driver of male-female coevolution. We also found that E74A knockout has opposing effects on fecundity in males and females, with an increase in fecundity for males but a decrease in females, consistent with its documented role in oocyte maturation. Our results suggest a novel function of Eip74EF in spermatogenesis and demonstrates that this gene influences both male and female reproductive success. We speculate on possible roles for E74A in spermatogenesis and male reproductive success.

Susceptibility of the Non-Targeted Crustacean Eurytemora affinis to the Endocrine Disruptor Tebufenozide: A Transcriptomic Approach

“…In addition, Br-c is reported to be involved in reproductive processes such as vitellogenesis [85], oogenesis [86], and embryogenesis [87] in both insects and crustaceans. Recently, Eip74EF was proposed to be involved in Drosophila spermatogenesis and male fecundity [88]. In the present study, genes coding for proteins involved in the reproductive process were mis-regulated in males exposed to 50 µg/L of TEB.…”

Genetic coordination of sperm morphology and seminal fluid proteins promotes male reproductive success inDrosophila melanogaster

“…We measured 1-7 sperm per male, with an average of 4. These sample sizes are standard (e.g., 24,32) and sufficient to capture variation among males (Fig S5). To measure testis size, we dissected a testis with attached seminal vesicle using fine forceps in 1X PBS and transferred the tissue to 40 μl of PBS, mounted under a cover slip, imaged immediately at 100X under phase contrast, and measured using the segmented line tool in ImageJ.…”

“…22097, 22125) that were originally phenotyped as part of another study in 2019. The standard competitor male derived from a Canton-S stock with a protamine-GFP construct that is expressed in sperm heads as well as an external GFP eye marker for scoring paternity (32). All stocks new to the lab were reared for at least two prior generations on yeast-sugar-agar medium at 23 °C sprinkled with live yeast at moderate densities.…”

“…Despite a detailed understanding of spermatogenesis and mechanisms of spermatid elongation, developmental processes that regulate production of sperm length diversity remain a mystery. A number of genes have been identified whose disruption interrupts elongation and is required for successful spermatogenesis (e.g., 30,31), but fewer genetic manipulations produce sperm that differ in length but are still functional (32). During spermatogenesis, transcriptional activity is highest in late spermatogonia and early spermatocytes and lowest in late spermatids (33), confirming that post-meiotic transcription is low relative to pre-meiotic, and many gene products necessary for late stages are transcribed during earlier stages (34).…”

Identification of the transcription factor E74A gene from Chilo suppressalis which is essential for vitellogenesis

“…E74A , a subtype of the E74 gene, is a key early response gene induced by 20E in the transcription factor cascade and belongs to a member of the E26 transformation‐specific (ETS) family (Fletcher & Thummel, 1995; Sharrocks, 2001; Sharrocks et al, 1997; Sun et al, 2005). Numerous studies have shown that E74 is involved in insect molting, chitin synthesis, growth and development, ecdysone titer, virus infection mechanism, male sperm length, and fertility (Chebbo et al, 2021; Fletcher et al, 1995; Stilwell et al, 2003; Zhang, Yao, et al, 2022;). MsE74A expression was found to be induced by 20E in Manduca sexta , and the expression level remains high during larvae, pupae, and adult molting (Stilwell et al, 2003).…”