Forty million years of mutualism: Evidence for Eocene origin of the yucca-yucca moth association

Abstract

The obligate mutualism between yuccas and yucca moths is a major model system for the study of coevolving species interactions. Exploration of the processes that have generated current diversity and associations within this mutualism requires robust phylogenies and timelines for both moths and yuccas. Here we establish a molecular clock for the moths based on mtDNA and use it to estimate the time of major life history events within the yucca moths. Colonization of yuccas had occurred by 41.5 ؎ 9.8 million years ago (Mya), with rapid life history diversification and the emergence of pollinators within 0-6 My after yucca colonization. A subsequent burst of diversification 3.2 ؎ 1.8 Mya coincided with evolution of arid habitats in western North America. Derived nonpollinating cheater yucca moths evolved 1.26 ؎ 0.96 Mya. The estimated age of the moths far predates the host fossil record, but is consistent with suggested host age based on paleobotanical, climatological, biogeographical, and geological data, and a tentative estimation from an rbcL-based molecular clock for yuccas. The moth data are used to establish three alternative scenarios of how the moths and plants have coevolved. They yield specific predictions that can be tested once a robust plant phylogeny becomes available.Obligate pollination mutualisms such as the yucca-yucca moth and fig-fig wasp associations provide some of the classically cited examples of coevolution (1, 2). In these interactions, the adult insects serve as the exclusive pollinators of their hosts. Their larvae subsequently feed on host seeds, but because many seeds are left intact the interaction carries a net positive effect for the plants. Both plants and insects show obvious coadapted traits, such as specific pollen collection and deposition behaviors in the insects, and structural adaptations that mediate pollinator specificity in the flowers.Given the strong associations between these organisms, they serve as excellent model systems for exploring many aspects of evolutionary biology, such as the origins of mutualism (3-7), the evolution of virulence (8), evolution of mating systems (9), stability and reversal of obligate mutualism (5, 7, 10, 11), and consequences of specialization on population structure in species (12). Because of this utility for many branches of evolutionary biology, it would be highly desirable to develop a strong phylogenetic framework for the organisms and to establish a timeline for their diversification. This framework would allow for macroevolutionary analyses of the insect-host association, assessing for example the importance of codiversification (13), and the role of intrinsic and extrinsic factors in driving diversification (14).Here we use molecular data in conjunction with biogeographic and fossil data to develop a phylogeny for the yucca moth family, Prodoxidae, to estimate minimum ages of divergence and determine patterns of diversification within the family. This work builds on an earlier study (15) based on limited molecular data that ...

Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps

“…Similarly, molecular estimates suggest that the actual age of the yucca^yucca moth mutualism (40 Myr) substantially pre-dates the fossil evidence of the host plant (14 Myr) (Pellmyr & Leebens-Mack 1999). The longevity of these obligate plant^insect associations emphasizes the fact that mutualisms, even those with clear con£icts of interest, can nonetheless be evolutionarily stable over vast expanses of time (Anstett et al 1997;Herre & West 1997;Herre et al 1999).…”

Coevolutionary Dynamics and the Conservation of Mutualisms

“…Slight cheats that arise by mutation could gradually erode the mutualistic interaction, and lead to dissolution or reciprocal extinction (Roberts and Sherratt 1998;Doebeli and Knowlton 1998). Although cheating has been assumed to be under strict control, recent empirical findings (reviewed by Bronstein 2001b) indicate that cheating is rampant in most mutualisms; in some cases, cheaters have been associated with mutualisms over long spans of evolutionary time (Després and Jaeger 1999;Pellmyr and Leebens-Mack 1999;Lopez-Vaamonde et al 2001). Recent theoretical advances have increased our understanding of the ecological and evolutionary persistence of particular forms of mutualism (e.g., Holland and DeAngelis 2001;Law et al 2001;Yu 2001;Holland et al 2002;Morris et al 2003;Wilson et al 2003).…”

Molecular Phylogenies of Fig Wasps: Partial Cocladogenesis of Pollinators and Parasites

“…Interaction and coevolution have probably been important during the radiations of plant lineages and their insect herbivores, with plant chemistry playing a key role (Ehrlich and Raven 1964); however, strict sense cospeciation seems generally unlikely Mitter, 1990, 1998). More specific interactions occur between certain groups of plants and their pollinators and perhaps the two best-known cases are figs and fig wasps (Herre, 1996;Anstett et al, 1997) and yuccas and yucca moths (Pellmyr and Leebens-Mack, 1999). Both of these systems are mutualisms but also involve conflicts of interest, principally over whether female flowers nourish developing seeds or insect larvae.…”