Non-mutualistic yucca moths and their evolutionary consequences

Abstract

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.

Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation

“…Third, some theories suggest that the presence of multiple symbionts produces an unstable situation for a mutualism, and that colonization events provide a likely scenario for the transition from mutualism to parasitism (4,(42)(43)(44)(45)(46)(47). For example, in several cases reported in the moths that either pollinate or parasitize Yucca flowers, a colonization of a novel host has been followed by a transition from mutualism to parasitism (46,48).…”

The evolution of mutualisms: exploring the paths between conflict and cooperation

“…Moreover, the female wasp offspring will carry pollen from the inflorescence in which they developed. In contrast, moths can pollinate and lay eggs in several different flowers, and their offspring are unlikely to provide the additional pollination service because they drop to the ground and emerge as adults much later 10, 38,39 . The difference between the figs and yuccas in the degree to which their interests coincide with their partners is probably reflected in the much higher proportion of the fig seeds that support development of wasp offspring compared with the proportion of yucca seeds that support the development of the moth offspring.…”

“…Specifically, phylogenetic analyses reveal that parasitic lineages can be embedded in largely mutualistic groups and/or vice versa 19,38,39. However, theory suggests that the species that parasitize mutualisms should not be the closest relatives to either partner 38,39 . Available evidence collected from figs (Ficus) and fig wasps (Agaonidae), and the yuccas (Yucca) and yucca moths (Tegeticula), supports this prediction 19,38,39 .…”

Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant

“…The Hirtella-Allomerus system resembles other species-specific mutualisms where mechanisms have evolved to enhance benefits of association and reduce costs due to cheating, and where such mechanisms promote the stability of the relationship (Tyre and Addicott 1993;Pellmyr and Huth 1994;West and Herre 1994;Pellmyr et al 1996). In mutualistic systems involving Ficus and Yucca and their respective pollinators, the plants "pay" their specific pollinators with potentially vi-able seeds for the growing larvae, in exchange for the pollination services provided by adult female insects.…”

“…In mutualistic systems involving Ficus and Yucca and their respective pollinators, the plants "pay" their specific pollinators with potentially vi-able seeds for the growing larvae, in exchange for the pollination services provided by adult female insects. Therefore, the decrease in plant reproductive success is counter-balanced immediately by the pollination service (Tyre and Addicott 1993;Pellmyr and Huth 1994;West and Herre 1994;Pellmyr et al 1996). In constrast, H. myrmecophila suffers a direct loss in reproductive success in exchange for an indirect increase in fitness obtained through protection against herbivores.…”