A meiotic driver alters sperm form and function in house mice: a possible example of spite

Abstract

The ability to subvert independent assortment of chromosomes is found in many meiotic drivers, such as the t haplotype in house mice Mus musculus, in which the t-bearing chromosomal homolog is preferentially transmitted to offspring. This is explained by a poison-antidote system, in which developing + and t sperm in testes of + /t males are exposed to 'poison' coded by t loci, from which t sperm are protected, allowing t sperm an overwhelming fertilisation advantage in monogamous matings. This system is thought to result in poorly and normally motile sperm subpopulations within + /t sperm, leaving t sperm unharmed. Conversely, we found that the fastest quartile of sperm from + /t males swam more slowly, both forwards and along their travel path, and had reduced straightness and linearity, compared to the fastest quartile of + / + sperm. Moreover, sperm from + /t males had shorter tails and narrower heads than + / + sperm, and these morphological differences covaried with motility differences. Finally, + /t traits did not show evidence of bimodal distributions. We conclude that the t haplotype drive results in lasting damage to the motility of both + and t developing sperm, although previous studies indicate that + must be more harmed than t sperm. This damage to all sperm may explain the low success of + /t males in sperm competition with + / + males, seen in earlier studies. We propose that the harm the t causes to itself could be termed 'spiteful', which may also be common to other gamete-harming meiotic drive systems.

Keywords: competition; gene drive; selfish genetic element; social evolution; sperm motility; t complex; transmission ratio distortion.

Fig. 1

Greyscale microscope image of CBB stained sperm at 1000 × magnification. Black arrow indicates acrosome-intact and white arrow acrosome-reacted sperm

Fig. 2

Density plots of individual sperm parameters as measured by CASA in red + /t (n = 34 males) and in blue + / + (n = 46 males), including means and standard deviations for mean trait of individuals. Statistical analysis results are in Table S2

Fig. 3

Density plots of individual sperm parameters as measured by CASA in red + /t (n = 34 males) and in blue + / + (n = 46 males) only including the 25% fastest sperm per sample, including means and standard deviations for mean trait of individuals. Statistical analysis results are in Table S3

Fig. 4

Density plots of sperm morphological traits for + /t males (red) and + / + (blue), including means and standard deviations for mean traits of individuals. A Midpiece length, B tail length, C head length, D head width, E head shape ratio (head length/head width) and F head-flagellum ratio (head length/(midpiece + tail length)). Statistical analysis results are in Table S6