Abstract
Mutualisms, or interactions between species that lead to net fitness benefits for each species involved, are stable and ubiquitous in nature mostly due to “byproduct benefits” stemming from the intrinsic traits of one partner that generate an indirect and positive outcome for the other. Here we verify if myrmecotrophy (where plants obtain nutrients from the refuse of their associated ants) can explain the stability of the tripartite association between the myrmecophyte Hirtella physophora, the ant Allomerus decemarticulatus and an Ascomycota fungus. The plant shelters and provides the ants with extrafloral nectar. The ants protect the plant from herbivores and integrate the fungus into the construction of a trap that they use to capture prey; they also provide the fungus and their host plant with nutrients. During a 9-month field study, we over-provisioned experimental ant colonies with insects, enhancing colony fitness (i.e., more winged females were produced). The rate of partial castration of the host plant, previously demonstrated, was not influenced by the experiment. Experimental plants showed higher δ15N values (confirming myrmecotrophy), plus enhanced vegetative growth (e.g., more leaves produced increased the possibility of lodging ants in leaf pouches) and fitness (i.e., more fruits produced and more flowers that matured into fruit). This study highlights the importance of myrmecotrophy on host plant fitness and the stability of ant-myrmecophyte mutualisms.
Highlights
Mutualisms, defined as cooperative interactions between species where each partner derives a fitness benefit, are based on ‘‘invested benefits’’ corresponding to an adaptation by each species to obtain benefits from its partner with the return exceeding the costs of the investment [1,2,3,4]
Defoliating insects destroyed 21 of these buds as well as the five flowers produced. Both plant growth and reproductive investment were enhanced by over-provisioning the ant colonies as the experimental trees produced significantly more leaves (3.5860.40 vs. 2.1760.31, p,0.001), more flower buds (5.8161.45 vs. 3.2760.64, p,0.0001), more flowers (3.6160.83 vs. 1.7860.39, p,0.0001) and more fruits (1.9060.50 vs. 0.4960.19, p,0.0001) than control trees (Likelihood ratio test on the generalized linear model (GLM)-Poisson model; R statistics)
We show that colony fitness was enhanced through overprovisioning with prey as more winged females were produced by experimental colonies
Summary
Mutualisms, defined as cooperative interactions between species where each partner derives a fitness benefit, are based on ‘‘invested benefits’’ corresponding to an adaptation by each species to obtain benefits from its partner with the return exceeding the costs of the investment [1,2,3,4]. When hosts transmit symbionts by ‘‘vertical transmission’’ to their offspring the mutualisms are evolutionarily stable; yet, most mutualistic interactions are transmitted ‘‘horizontally’’ as the partners disperse separately In the latter case, the reproduction of each partner might be subject to a trade-off if the resources invested by one partner in its own reproduction are lost for the other partner. The reproduction of each partner might be subject to a trade-off if the resources invested by one partner in its own reproduction are lost for the other partner Such a trade-off is a major source of instability as the symbionts may evolve traits promoting a reduction in cost, engendering the emergence of ‘‘cheaters’’ obtaining benefits at minimal cost [6]. They end up by completely sterilizing their hosts [7,8]
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