  Cells are known to exert forces to sense their physical surroundings for
guidance of motion and fate decisions. Here, we propose that cells might do
mechanical work to drive their own evolution, taking inspiration from the
adaptive immune system. Growing evidence indicates that immune B cells -
capable of rapid Darwinian evolution - use cytoskeletal forces to actively
extract antigen from other cells' surface. To elucidate the evolutionary
significance of force usage, we develop a theory of tug-of-war antigen
extraction that maps receptor binding characteristics to clonal reproductive
fitness, revealing physical determinants of selection strength. This framework
unifies mechanosensing and affinity-discrimination capabilities of evolving
cells: pulling against stiff antigen tethers enhances discrimination stringency
at the expense of absolute extraction. As a consequence, active force usage can
accelerate adaptation but may also cause extinction of cell populations,
resulting in an optimal range of pulling strength that matches molecular
rupture forces observed in cells. Our work suggests that nonequilibrium,
physical extraction of environmental signals can make biological systems more
evolvable at a moderate energy cost.
