Meiotic drive reduces egg-to-adult viability in stalk-eyed flies

Abstract

23SR meiotic drive is a selfish genetic element located on the X chromosome in a number of 24 species that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of 25 offspring, causing extreme sex ratio bias. SR in several species is found in a stable 26 polymorphism at a moderate frequency, suggesting there must be strong frequency-27 dependent selection resisting its spread. We investigate the effect of SR on female and male 28 egg-to-adult viability in the Malaysian stalk-eyed fly, Teleopsis dalmanni. SR meiotic drive in 29 this species is old, and appears to be broadly stable at a moderate (~20%) frequency. We 30 use large-scale controlled crosses to estimate the strength of selection acting against SR in 31 female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In 32 females, homozygous females experience greater reduction in viability (sf = 0.242) and the 33 deleterious effects of SR are additive (ℎ = 0.511). The male deficit in viability (sm = 0.214) is 34 not different from that in homozygous females. The evidence does not support the 35 expectation that deleterious side-effects of SR are recessive or sex-limited. We discuss how 36 these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, 37 act to maintain SR polymorphism in this species. 38 157

Meiotic drive reduces egg-to-adult viability in stalk-eyed flies

“…Data accessibility. Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.kc49jk1 [79].…”

Resistance to natural and synthetic gene drive systems

“…In the related species D. subobscura , only an extremely weak suppressor of drive has been found, again despite a high frequency of drive in natural populations and substantial costs of drive (Verspoor et al., 2018). The same lack of suppressors occurs in Teleopsis dalmanni stalk‐eyed flies which again have a high frequency SR drive system which imposes significant viability costs in males and females (Finnegan et al., 2019) and is estimated to be a million years old (Reinhardt et al., 2014). The hybridizing species D. testacea and D. neotestacea each bear driving X chromosomes, but the former shows strong autosomal suppression (Keais, Lu, & Perlman, 2020), whereas the latter shows no evidence of suppression at all (Pinzone & Dyer, 2013).…”

“…One possibility is that the locus that confers susceptibility to drive is small, providing a small mutational target. However, many drivers impose broad costs across the genome (Dyer & Hall, 2019; Finnegan et al., 2019; Hamilton, 1967; Larner, Price, Holman, & Wedell, 2019; Zanders & Unckless, 2019), so loci throughout the genome are predicted to evolve to resist costly gene drives. Here, the lack of resistance mechanisms cannot be due to the small size of the mutational target, suggesting the involvement of other evolutionary constraints.…”

“…Drivers may themselves have a range of harmful pleiotropic effects, or be in linkage with deleterious alleles (Burt & Trivers, 2006). Fitness loss is often observed in both males and females, especially when drivers are homozygous (Dyer & Hall, 2019; Finnegan et al., 2019; Hamilton, 1967; Larner et al., 2019; Zanders & Unckless, 2019).…”

Adequacy and sufficiency evaluation of existing EFSA guidelines for the molecular characterisation, environmental risk assessment and post‐market environmental monitoring of genetically modified insects containing engineered gene drives

“…Beeman et al, 1992;Burt and Trivers, 2006;Sinkins and Gould, 2006;Champer et al, 2016;Agren and Clark, 2018;Collins, 2018;R € udelsheim and Smets, 2018;Cash et al, 2019Cash et al, , 2020Frieb et al, 2019). The study of natural gene drive systems has provided considerable theoretical and empirical insights into how natural gene drives work, how they spread and how simple model predictions on engineered gene drives may fail (Courret et al, 2019;Dyer and Hall, 2019;Finnegan et al, 2019;Larner et al, 2019;Lea and Unckless, 2019;Price et al, 2019;Wedell et al, 2019;Dhole et al, 2020). These insights can provide baseline information for the design of engineered gene drives, and in some cases, for the risk assessment of GDMIs.…”