Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Mutualisms that involve symbioses among specialized partners may be more stable than mutualisms among generalists, and theoretical models predict that in many mutualisms, partners exert reciprocal stabilizing selection on traits directly involved in the interaction. A corollary is that mutualism breakdown should increase morphological rates of evolution. We here use the largest ant-plant clade (Hydnophytinae), with different levels of specialization for mutualistic ant symbionts, to study the ecological context of mutualism breakdown and the response of a key symbiosis-related trait, domatium entrance hole size, which filters symbionts by size. Our analyses support three predictions from mutualism theory. First, all 12 losses apparently only occur from a generalist symbiotic state. Second, mutualism losses occurred where symbionts are scarce, in our system at high altitudes. Third, domatium entrance hole size barely changes in specialized symbiotic species, but evolves rapidly once symbiosis with ants has broken down, with a “morphorate map” revealing that hotspots of entrance hole evolution are clustered in high-altitude areas. Our study reveals that mutualistic strategy profoundly affects the pace of morphological change in traits involved in the interaction and suggests that shifts in partners’ relative abundances may frequently drive reversions of generalist mutualisms to autonomy.