Cooperation is widespread across life, but its existence can be threatened by exploitation. Social cheaters can be obligate, incapable of contributing to a necessary function, so that spread of the cheater leads to loss of the function. In the social amoeba Dictyostelium discoideum, obligate social cheaters cannot become dead stalk cells that lift spores up for dispersal, but instead depend on forming chimeras with fully functional altruistic individuals for forming a stalk. Obligate cheaters in D. discoideum are known to pay the cost of being unable to form fruiting bodies on their own. In this study we discovered that there are two additional costs that can apply to obligate cheaters. Even when there are wild-type cells to parasitize, the chimeric fruiting bodies that result have shorter stalks that are disadvantaged in spore dispersal. Furthermore, we found that obligate cheaters were overrepresented among spore cells in chimeras only when they were at low frequencies. Failure to develop into viable fruiting bodies on their own, negative frequency-dependent cheating, and shorter fruiting bodies represent three limits on obligate social cheating so it is not surprising that obligate cheaters have not been found in nature.