Sperm Sociality: Cooperation, Altruism, and Spite

A swimming sperm cell appears to perfectly capture the individualist Darwinian struggle, as it frantically races onwards towards a waiting egg. Consistent with this imagery, sperm morphology and behaviour in many organisms appears exquisitely designed to maximise the chances of fertilisation of each individual sperm cell [1]. However, there are numerous less obliging cases where sperm seem poorly suited to the task, even to the extent that the majority of sperm in an ejaculate may be infertile [2,3]. Why would such sperm evolve? The secret to unravelling the mystery of subfertile and infertile sperm may lie in understanding their social lives. Sperm evolution requires one to consider Darwinian selection on multiple interacting parties and at multiple levels, and this lends itself to the tools of sociobiology: kin selection and multi-level selection theory [4]. A male and female have just mated; what would one predict? Her evolutionary interests can be complex but, generally speaking, her priorities are to make sure that all of her eggs are fertilised, and that they are fertilised by sperm delivering the best genes for her offspring. It is in the interests of each individual sperm to rise to the challenge and do anything to fertilise an egg. This might mean a temporary alliance with some fellow sperm, but should others fl ounder and fail, all the better [5]. The male interests, however, are different. He has little to gain from sperm infi ghting, and instead only seeks to ensure that all of the eggs available are fertilised by his sperm. In other words, taking the perspective of the haploid genome in a sperm cell, different sperm haplotypes from the same male are in evolutionary confl ict [5,6], while from the perspective of the diploid genome of the male parent, all sperm are equally valuable. This means that, in addition to confl ict among individual sperm, there is also potential confl ict between each sperm and the male, which could lead to an evolutionary arms race over which controls sperm morphology and behaviour [5,7]. But now our female mates with a second male, and the battlegrounds shift somewhat. The two males are in strong confl ict with one another as their ejaculates compete to fertilise the eggs, an inter-male process called sperm competition. This competition from a foreign male has important knock-on effects for the other confl icts. In particular, the presence of foreign sperm better aligns …