A rapidly evolving actin mediates fertility and developmental tradeoffs in Drosophila

Courtney M. Schroeder, Sarah A. Tomlin, John R. Valenzuela, Harmit S. Malik

Preprint posted on September 28, 2020

Fast actin’ : non-canonical, rapidly evolving Arp detrimental to the male germline retained in flies for boost to female fertility

Selected by Hiral Shah, Dey Lab

Introduction/ Background

Actin-related proteins (Arps) constitute an ancient (1,2) superfamily of cytoskeletal proteins with specialized functions in polymerisation of actin structures, dynein motility and chromatin remodeling (3). Arps retain the characteristic actin fold domain (4) but have diverged to incorporate other structural elements. While many Arps are widely conserved, others appear to evolve rapidly, restricted to certain lineages or ‘orphaned’. Interestingly, many of these Arps show sex- and tissue-specific expression, contrary to the ubiquitous presence of actin and canonical Arps (5). It is likely that non-canonical Arps play specialized but important roles in cytoskeletal organization, however, their functions remain largely unknown. Arp53D, for instance, the first non-canonical Arp to be described (6), is conserved across the Drosophila lineage, is absent outside insects and is enriched in the male testis. Arp53D proteins are defined by an unstructured 40 amino acid N-terminal stretch and a fast evolving actin fold domain. Owing to the male germline expression of Arp53D, this preprint set out to understand its function in male fertility using genetic and cytological studies.


Key Findings 

Arp53D localized to testis-specific actin structures – such as the fusome and the actin cones. The N-terminal stretch was important for this unique localisation pattern of Arp53D. To identify Arp53D function, Arp53D knock-out (KO) flies were generated, marked with DsRed fluorescent eyes, to facilitate analysis of future crosses. Based on the tissue-specific localization and conservation across Drosophila, the authors expected the KO to show a decline in male fertility. Intriguingly, the loss of Arp53 led to an increase in male fertility, producing a higher number of progeny. Independent of the method, KO or RNAi, the Arp53D deficient flies consistently produced more progeny. What could be the possible advantage of retaining a gene that has detrimental effects on male fertility? Could the gene provide a benefit in competition between males? To address this, the authors attempted crosses with Arp53 KO males in isolation and in presence of Wild type (WT) competitors. Once again, irrespective of the competition, the Arp53 KO males outdid the WT counterparts. One possible explanation for selection of a gene with negative effects, the authors reasoned, would be an advantageous effect on some other traits. Which other traits could this gene affect?


Figure 1: Taken directly from Fig. 6 A & B of Schroeder et al. 2020 under a CC-BY-NC-ND 4.0 international license.


All the authors’ observations thus far related to KO males. What would happen in reciprocal crosses? Interestingly, when Arp53D KO females were crossed with WT or KO males the fitness advantage conferred by Arp53 KO males was lost (Fig. 1). This opened up two possibilities: either Arp53D affected zygotic development or female fertility.  The lower number of progeny in crosses with KO females and WT males pointed in the direction of reduced maternal effects. A further reduction in progeny number when both parents lacked Arp53D suggested additional defects in zygotic development or viability, with KO females making the larger contribution. What was causing this decline in progeny numbers? While there was no difference in egg numbers, it turns out the number of eggs developing into larvae was much smaller.

Thus, despite its negative impact on male fertility, Arp53D was likely retained for advantages conferred on maternal fertility and zygotic fitness. This was only possible if the net outcome of retaining Arp53D was beneficial. Would it be possible to demonstrate this in the lab? Indeed, the authors carried out population cage experiments over multiple generations to study long term changes in frequencies of the WT and KO alleles in a population isogenic for all other loci. At each generation randomly selected individuals were used to set up the subsequent cross and the Arp53D status of the remaining progeny was determined based on DsRed fluorescence. The Arp53D WT allele increased significantly within 20 generations, rising from less than one-third to almost two thirds of the fly population. 



Does lack of the N-terminal stretch affect progeny size, male or female fertility? 

What is the evolutionary history of this fitness tradeoff? In other words, would it be possible to reconstruct ancestral Arp53D variants and evaluate their impact on fitness? Alternatively, since this might be difficult for such a fast-evolving protein, would swapping Arp53D between species alter progeny numbers or female fertility? How would these different versions compete in population cage experiments?

What do you suspect is the exact nature of the molecular or cellular defects in female fertility and zygote development?



  1. Akıl C., Kitaoku Y., Tran L.T., Liebl D., Choe H., Muengsaen D., Suginta W., Schulte A. & Robinson R.C. 2021. Mythical origins of the actin cytoskeleton. Curr. Opin. Cell Biol. 68:55-63. doi: 10.1016/
  2. Izoré, T., Kureisaite-Ciziene, D., McLaughlin, S.H. & Löwe, J. 2016. Crenactin forms actin-like double helical filaments regulated by arcadin-2. eLife 5:e21600 doi: 10.7554/eLife.21600
  3. Schafer, D.A. & Schroer, T.A. 1999. Actin-related proteins. Annu. Rev. Cell Dev. 15:341-363.
  4. Dominguez, R. & Holmes, K.C. 2011. Actin structure and function. Annu. Rev. Biophys. 40, 169-86. doi: 10.1146/annurev-biophys-042910-155359
  5. Schroeder, C.M., Valenzuela, J.R., Natividad, I.M., Hocky, G.M. & Malik, H.S. 2019. A burst of genetic innovation in Drosophila actin-related proteins for testis-specific function. Mol. Biol. Evol. 37(3):757-772. doi: 10.1093/molbev/msz262
  6. Fyrberg C, Ryan L, Kenton M, Fyrberg E. 1994. Genes encoding actin-related proteins of Drosophila melanogaster. J. Mol. Biol. 241(3):498-503.

Tags: actin, conflict, fitness, tradeoff

Posted on: 16th October 2020


Read preprint (No Ratings Yet)

Have your say

Your email address will not be published. Required fields are marked *

This site uses Akismet to reduce spam. Learn how your comment data is processed.

Sign up to customise the site to your preferences and to receive alerts

Register here

preLists in the cell biology category:

FENS 2020

A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020


List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.


List by Ana Dorrego-Rivas

BioMalPar XVI: Biology and Pathology of the Malaria Parasite

[under construction] Preprints presented at the (fully virtual) EMBL BioMalPar XVI, 17-18 May 2020 #emblmalaria


List by Dey Lab, Samantha Seah


Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.


List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20


List by Maiko Kitaoka, Madhuja Samaddar, Miguel V. Almeida, Sejal Davla, Jennifer Ann Black, Dey Lab

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Preprint missing? Don't hesitate to let us know.


List by Paul Gerald L. Sanchez and Stefano Vianello

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome


List by Hiral Shah

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)


List by Madhuja Samaddar, Ramona Jühlen, Amanda Haage, Laura McCormick, Maiko Kitaoka

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019


List by Dey Lab


Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.


List by Sandra Malmgren Hill

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.


List by Rob Hynds

Cellular metabolism

A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.


List by Pablo Ranea Robles

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019


List by Dey Lab


This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.


List by Sandra Franco Iborra

Biophysical Society Annual Meeting 2019

Few of the preprints that were discussed in the recent BPS annual meeting at Baltimore, USA


List by Joseph Jose Thottacherry

ASCB/EMBO Annual Meeting 2018

This list relates to preprints that were discussed at the recent ASCB conference.


List by Dey Lab, Amanda Haage

Also in the evolutionary biology category:

Festival of Ecology! 14th to 18th December 2020 #BES2020

A list of preprints dealing with the talks/posters presented in the Festival of Ecology virtual conference held in December 2020


List by Baheerathan Murugavel

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.


List by Ana Dorrego-Rivas

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20


List by Maiko Kitaoka, Madhuja Samaddar, Miguel V. Almeida, Sejal Davla, Jennifer Ann Black, Dey Lab

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome


List by Hiral Shah

COVID-19 / SARS-CoV-2 preprints

List of important preprints dealing with the ongoing coronavirus outbreak. See for additional resources and timeline, and for full list of bioRxiv and medRxiv preprints on this topic


List by Dey Lab, Zhang-He Goh


SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.


List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.


List by Alexa Sadier