How much should a female be willing to risk in any one reproductive event? Highly iteroparous females will be risk averse and very conservative in their behaviour. Such females will be expected to avoid mortality risks and seek assurance that any current reproductive activity is safe. By way of minimizing risk, these same females will not engage in mate assessment or mate searching to the same degree as less iteroparous species, if these activities involve increased risk of mortality. Using a field experiment in a highly iteroparous species (the bluehead wrasse, Thalassoma bifasciatum), it is shown that females in this species are indeed relatively risk averse. More importantly, the experiment also shows that individuals vary in their risk aversion depending on local population size, in a manner predicted from life-history theory. Then it is reviewed how several important aspects of the mating system in this species are best interpreted as results of conservative, risk-averse female behaviour. Finally, these ideas are generalized to suggest how basic aspects of the mating system might differ between species with many reproductive events over the lifetime (e.g. many tropical reef fishes) v. species with few reproductive opportunities (e.g. many temperate freshwater and marine fishes).