Horny but barren: Mitochondrial genotype associated with reduced fertility increases mating success rate in male seed beetles

Abstract

Due to non-Mendelian, maternal inheritance, mitochondrial genomes are shaped by natural selection acting only on females. This evolutionary phenomenon results in accumulation of mutations that are detrimental for males, but benign for females, and is known as the Mother’s curse. The sex-specific effects of these mitochondrial mutations are expected to occur in traits that are more energy demanding in males, such as gamete production or mating behavior. Previously, we identified three different mitochondrial genotypes in laboratory populations of the seed beetle (Acanthoscelides obtectus) by sequencing all 13 mitochondrial protein-coding genes. One of them, MG3b, which is characterized by six amino-acid substitutions, specifically reduces male reproductive output and decreases the activity of all OXPHOS complexes compared to other, control genotypes (MG1a and MG1d). In this study, we wanted to evaluate whether the reduced fertility of MG3b males is due to their passive reproductive behaviour. To test this, we expressed MG3b and two control genotypes alongside the same outbred nuclear background and measured the mating success rate, start and duration of copulation of males with specific genotypes when crossed with wild-type females. Our results show that MG3b males have a significantly higher mating success rate compared to MG1a and MG1d males, while start and duration of copulation are the same for all genotypes. This indicates that the lower reproductive output of MG3b males is likely due to impairments in reproductive tissue caused by decreased OXPHOS function, while the higher mating rate could be a compensatory mechanism.