A selfish genetic element and its suppressor causes abnormalities to testes in a fly

Abstract

Selfish genetic elements (SGEs), specifically X-chromosome meiotic drive (XCMD), create huge conflicts within a hosts genome and can have profound effects on fertility. Suppressors are a common evolutionary response to XCMD to negate its costs. However, whether suppressors themselves can cause negative non-target effects remains understudied. Here, we examine whether the intragenomic conflicts created by XCMD and its suppressor affects gonad morphology in Drosophila subobscura. We found significant differences in testes, seminal vesicle, and accessory gland size depending on whether a male carried a non-driving X chromosome, an XCMD, and if the XCMD was suppressed. We also found the first evidence of extreme whole-organ damage to testes that is specifically associated with a suppressor of XCMD. Unlike other studies, our evidence suggests that XCMD in D. subobscura inflicts extreme damage on male gonads. This damage is most severe if both XCMD and its suppressor are both present. While costs of suppression have importance in theoretical models, they have largely been ignored in empirical XCMD systems. Overall, this study highlights that genetic conflict, created by SGEs and their suppressors, is a potent evolutionary force that can have major impacts on gonad development and gametogenesis.

The suppression of a selfish genetic element increases a male's mating success in a fly

“…We used isofemale lines (Parsons & Hosgood, 1967 ) of Drosophila subobscura established from flies collected in Tabarka, Tunisia (abbreviated to Tab) (36.95° N 8.74° E) in 2013 (Verspoor, Cuss, & Price, 2015 ), Ras el Oued, Morocco (abbreviated to Ras) (34.15° N 4.00° W), Demnat, Morocco (abbreviated to Dem) (31.73° N 7.01° W), and Ouzoud, Morocco (abbreviated to Ouz) (32.02° N 6.72° W) (Lyth et al., 2023 in review), using traps baited with banana, beer, and yeast. Flies were collected from these locations as it is representative of the range of D. subobscura populations across North Africa and locations were separated by a distance of 1400 km.…”

“…Yet, the influence of SGE suppressors on mating behavior has not been widely examined. This is surprising as SGEs and their suppressors can affect gonad development (Bradshaw et al., 2022 ; Lyth et al., 2023 in review; Meade et al., 2020 ), which could impact male quality and fertility.…”

“…Unexpectedly, it appears that the suppressor has not spread through populations as it remains rare at a frequency of 1–5% in populations across North Africa (Verspoor, R.L., Lyth, S., & Price, T.A.R., unpublished data), suggesting that the suppressor may also be costly in itself. Interestingly, suppression of XCMD in the SR system is also associated with abnormal testes size and even visible abnormalities to testes (Lyth et al., 2023 in review), which could in itself influence the fitness of those males that carry both XCMD and suppressors.…”