Cooperation between kin and cooperation between non-kin often appear functionally similar, but the evolutionary mechanisms that drive the emergence of these two forms of cooperation can be dramatically different. The mechanisms responsible for non-kin cooperation, in particular, are not well established in an empirical context. To truly understand the emergence of non-kin cooperation, the fitness outcomes of cooperation should be compared with the alternate strategy of solitary living in the same environment. Ant populations that contain a mix of queens who found nests alone (monogyny), and cooperative unrelated ant queens who found nests together and remain together through colony development (primary polygyny), provide a useful natural context to make such a comparison. To estimate the reproductive costs for primary polygyny relative to solitary nest founding, we measured alate (reproductive) production for colonies in a mixed population of polygynous and monogynous California harvester ant colonies over a 2-year period. Colony-level reproductive output was not substantially higher in polygynous colonies compared to those with single queens, and consequent per-queen reproductive gain was significantly lower. Given that polygynous queens in this population are unrelated, nest sharing thus generates a significant annual and potentially lifetime cost for cooperative queens. Comparative measures of colony dynamics, however, suggest that polygynous colonies have a larger or more active workforce than monogynous colonies. Additionally, polygynous colonies may be more conservative than monogynous colonies in resource allocation towards reproduction. These results collectively suggest that primary polygyny generates annual reproductive fitness costs. However, polygynous colonies likely also shift life history strategies in ways that emphasize long-term survival and colony growth over immediate reproduction. Over time, this shift may mitigate the annual fitness costs of cooperation. Significance statement When things get difficult, it pays to work together. In some ant species, unrelated queens form long-term cooperative associations that share resources and a workforce within a single nest. The fitness consequences and evolutionary drivers of non-kin cooperation in this and other systems are unclear. We compared the reproductive investment and colony dynamics of single-queen and multi-queen California harvester ant colonies in a shared environment to directly compare the fitness of cooperative and non-cooperative queens. Our data suggest that cooperation not only lowers annual per-queen reproduction, but also produces a more robust colony that may recoup annual fitness losses by extending colony longevity.
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