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

Abstract

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. mutualism | symbiosis | morphology | comparative phylogenetic methods | ants U nderstanding how mutualisms arise, persist, or break down is a major focus in ecology and evolutionary biology (1-3). Symbiotic mutualisms can revert to the free-living state if the costto-benefit ratio shifts so that costs outweigh benefits. There are three main pathways through which mutualism can break down, namely, extinction of the partner, reversion to the free-living state, or shift to parasitism (2). Extinction of one partner in an obligate mutualism should entail the extinction of the other, whereas in a facultative mutualism, extinction might lead to a reversion to autonomy (4-8), but these predictions have limited support from empirical studies. Similarly, mutualism could also break down if one partner becomes scarce, which may be especially important in laterally transferred symbioses where partners disperse independently and the interaction needs to be reestablished at each generation, involving vulnerable stages for both. Mutualisms can also break down by shifting to parasitism. Such shifts are predicted by theory (9, 10) because reducing or stopping reciprocation increases the fitness of the cheating partner (11)(12)(13)(14). Phylogenetically unrelated freeloaders may also disrupt a mutualism by exploiting it (15-18). Finally, mutualism can break down if benefits can be obtained cheaply or freely from the environment, for example, when plants involved in mycorrhizal or rhizobia symbioses grow in nutrient-rich soils (19,20) or when antiherbivore defense by ant mutualists is no longer required (21). Most of these theoretical expectations ab...

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