Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.

Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general.

Female multiple mating (polyandry) is widespread across many animal taxa and indirect genetic benefits are a major evolutionary force favouring polyandry. An incentive for polyandry arises when multiple mating leads to sperm competition that disadvantages sperm from genetically inferior mates. A reduction in genetic quality is associated with costly selfish genetic elements (SGEs), and studies in invertebrates have shown that males bearing sex ratio distorting SGEs are worse sperm competitors than wild-type males. We used a vertebrate model species to test whether females can avoid an autosomal SGE, thethaplotype, through polyandry. Thethaplotype in house mice exhibits strong drive intheterozygous males by affecting spermatogenesis and is associated with homozygousin uterolethality. We used controlled matings to test the effect of thethaplotype on sperm competitiveness. Regardless of mating order,theterozygous males sired only 11% of zygotes when competing against wild-type males, suggesting a very strong effect of thethaplotype on sperm quality. We provide, to our knowledge, the first substantial evidence that polyandry ameliorates the harmful effects of an autosomal SGE arising through genetic incompatibility. We discuss potential mechanisms in our study species and the broader implications for the benefits of polyandry.

Sperm competition was defined by Geoff Parker 50 years ago as the competition between sperm from two or more males over the fertilization of a set of eggs. Since the publication of his seminal paper, sperm competition has developed into a large field of research, and many aspects are still being discovered. One of the relatively poorly understood aspects is the importance of selection and competition among sperm within the ejaculate of a male. The sheer number of sperm present in a male's ejaculate suggests that the competition among sibling sperm produced by the same male may be intense. In this review, we summarize Parker's theoretical models generating predictions about the evolution of sperm traits under the control of the haploid gamete as opposed to the diploid male. We review the existing evidence of within-ejaculate competition from a wide range of fields and taxa. We also discuss the conceptual and practical hurdles we have been facing to study within-ejaculate sperm competition, and how novel technologies may help in addressing some of the currently open questions. This article is part of the theme issue ‘Fifty years of sperm competition’.

Rising and more variable global temperatures pose a challenge for biodiversity, with reproduction and fertility being especially sensitive to heat. Here, we assessed the potential for thermal adaptation in sperm and egg function using Tribolium flour beetles, a warm-temperate-tropical insect model. Following temperature increases through adult development, we found opposing gamete responses, with males producing shorter sperm and females laying larger eggs. Importantly, this gamete phenotypic plasticity was adaptive: thermal translocation experiments showed that both sperm and eggs produced in warmer conditions had superior reproductive performance in warmer environments, and vice versa for cooler production conditions and reproductive environments. In warmer environments, gamete plasticity enabled males to double their reproductive success, and females could increase offspring production by one-third. Our results reveal exciting potential for sensitive but vital traits within reproduction to handle increasing and more variable thermal regimes in the natural environment.