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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 https://www.biorxiv.org/content/10.1101/2020.09.28.317503v1

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

Selected by Hiral Shah, Gautam Dey

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. 

 

Questions

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?

 

References

  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/j.ceb.2020.08.011
  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

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