Ecological drivers of coexistence and lethal variant evolution in the t haplotype

One of the most extensively studied segregation distorters is the t haplotype in house mice (Mus musculus), which can have transmission rates as high as 99 in heterozygous males. Numerous t-haplotype variants exist that induce male sterility or cause embryonic lethality when homozygous. Lethal t variants are thought to have evolved through the accumulation of lethal mutations on a sterile background, but theoretical work indicates that this process is plausible only under substantial inbreeding and reproductive compensation. Here, we use a spatially explicit and stochastic individual-based model to investigate how sperm competition and polyandry, pre-copulatory mate choice, and male-specific fitness costs influence coexistence of sterile and lethal t-haplotype variants. Polyandry, pre-copulatory mate choice, male-specific fitness costs and immigration reduced t-haplotype frequencies, but there was substantial variation in coexistence patterns. Coexistence between two sterile variants was rare unless their transmission rates were nearly identical, whereas coexistence between two noncomplementing lethal variants was more common even when their transmission rates varied widely. The coexistence of sterile and lethal variants was highly asymmetric; the lethal variant was able to persist only when its transmission rate greatly exceeded that of the sterile variant. Notably, pre-copulatory mate choice exhibited by t-carrying females against t-carrying males impacted only the sterile variant negatively and allowed the lethal variant to persist without a transmission ratio advantage. Our results reconcile longstanding discrepancies between theoretical predictions and observations in natural populations and provide new insights into the evolution of lethal variants.