Sperm cooperation has evolved in a variety of taxa and is often considered
a response to sperm competition, yet the benefit of this form of collective
movement remains unclear. Here, we use fine-scale imaging and a minimal mathematical model to study sperm aggregation in the rodent genus
Peromyscus. We demonstrate that as the number of sperm cells in an aggregate
increase, the group moves with more persistent linearity but without increasing speed. This benefit, however, is offset in larger aggregates as the geometry
of the group forces sperm to swim against one another. The result is a nonmonotonic relationship between aggregate size and average velocity with
both a theoretically predicted and empirically observed optimum of six to
seven sperm per aggregate. To understand the role of sexual selection in driving these sperm group dynamics, we compared two sister-species with
divergent mating systems. We find that sperm of Peromyscus maniculatus
(highly promiscuous), which have evolved under intense competition, form
optimal-sized aggregates more often than sperm of Peromyscus polionotus
(strictly monogamous), which lack competition. Our combined mathematical
and experimental study of coordinated sperm movement reveals the importance of geometry, motion and group size on sperm velocity and suggests
how these physical variables interact with evolutionary selective pressures
to regulate cooperation in competitive environments.