Interspecific Mutualisms Research Articles

Non-mutualistic yucca moths and their evolutionary consequences.

Interspecific mutualisms are regarded as having evolved from antagonistic or commensalistic interactions, with most mutualisms remaining facultative but some having coevolved into obligate reciprocal dependency. Underlying mutualism is an intrinsic conflict between the parties, in that each is under selection for increased exploitation of the other. Theoretical models suggest that this conflict is a source of evolutionary instability, and that evolution of 'cheating' by one party may lead to reciprocal extinction. Here we present phylogenic evidence for reversal of an obligate mutualism: within the yucca moth complex, distinct cheater species derived from obligate pollinators inflict a heavy cost on their yucca hosts by laying their eggs but not pollinating the yucca. Phylogenetic data show the cheaters to have existed for a long time. Coexisting pollinators and cheaters are not sister taxa, supporting predictions that evolution of cheating within a single pollinator is evolutionarily unstable. Several lines of evidence support a hypothesis that host shifts preceded the reversal of obligate mutualism. Host or partner shifts is a mechanism that can provide a route of evolutionary escape among obligate mutualists in general.

The Benefits of Mutualism: A Conceptual Framework

SummaryThere are three general mechanisms by which phenotypic benefits are transferred between unrelated organisms. First, one organism maypurloinbenefits from another by preying on or parasitizing the other organism. Second, one organism may enjoy benefits that areincidentalto or aby‐productof the self‐serving traits of another organism. Third, an organism mayinvestin another organism if that investment produces return benefits which outweigh the cost of the investment. Interactions in which both parties gain a net benefit are mutualistic. The three mechanisms by which benefits are transferred between organisms can be combined in pairs to produce six possible kinds of original or ‘basal’ mutualisms that can arise from an amutualistic state. A review of the literature suggests that most or all interspecific mutualism have origins in three of the six possible kinds of basal mutualism. Each of these three basal mutualisms have byproduct benefits flowing in at least one direction. The transfer of by‐product benefits and investment are common to both intra‐ and interspecific mutualisms, so that some interspecific mutualisms have intraspecific analogs. A basal mutualism may evolve to the point where each party invests in the other, sometimes obscuring the nature of the original interaction along the way. Two prominent models for the evolution of mutualism do not include by‐product benefits: Roughgarden's model for the evolution of the damsel‐fish anemone mutualism and the ‘Tit‐for‐Tat’ model of reciprocity. Using the conceptual framework presented here, including in particular by‐product benefits, I have shown how it is possible to construct more parsimonious alternatives to both models.

Evolutionary stability of mutualism between yuccas and yucca moths

INTERSPECIFIC mutualisms inherently possess a conflict of interests between the interacting species in that fitness increases of one species occur at the expense of the other. This holds for mutualisms as diverse as plant associations with mycorrhizal fungi or nitrogen-fixing bacteria, animals and endosymbionts, and obligate plant-pollinator associations1–6. Prevailing models of interspecific cooperation predict that mutualistic interactions are evolutionary stable only when both interacting species possess mechanisms to prevent excessive exploitation3–6. In light of this, it is paradoxical that some of the classical examples of coevolved obligate mutualism seemingly do not meet this criterion. In mutualisms involving seed parasites that actively pollinate their hosts, such as yucca/ yucca moth and fig/fig wasp interactions, there is no apparent means of retaliation on behalf of the plant. Predictions from theory suggest that a cryptic mechanism, such as selective abortion of flowers with heavy egg loads, could stabilize these interactions4,6–9. Here we present the first empirical evidence that such a mechanism in fact exists in the yucca/yucca moth interaction. A strong nega-tive effect exists between moth egg number and probability of flower retention. Furthermore, we show a strong positive effect between the number of pollinations received and the probability of flower retention. Selective maturation of fruit with low egg loads and high pollen loads provides a mechanism to increase the quantity and possibly quality of seeds produced, and simultaneously select against moths that lay many eggs per flower or provide low-quality pollinations4,6,8,10. Not only can these results explain the stability of this type of interaction, but selection for high-quality pollination also provides a mechanism to help explain the evolution of active pollination among yucca moths.