Multiple origins of the yucca-yucca moth association.

Abstract

The association of species of yucca and their pollinating moths is considered one of the two classic cases of obligate mutualism between floral hosts and their pollinators. The system involves the active collection of pollen by females of two prodoxid moth genera and the subsequent purposeful placement of the pollen on conspecific stigmas of species of Yucca. Yuccas essentially depend on the moths for pollination and the moths require Yucca ovaries for oviposition. Because of the specificity involved, it has been assumed that the association arose once, although it has been suggested that within the prodoxid moths as a whole, pollinators have arisen from seed predators more than once. We show, by using phylogenies generated from three molecular data sets, that the supposed restriction of the yucca moths and their allies to the Agavaceae is an artifact caused by an incorrect circumscription of this family. In addition we provide evidence that Yucca is not monophyletic, leading to the conclusion that the modern Yucca-yucca moth relationship developed independently more than once by colonization of a new host.The Yucca-yucca moth [Parategeticula and Tegeticula spp. (Prodoxidae)] interrelationship is one of the classic examples of a tight mutualism in pollination biology. The relationship has been called "a complete, unbreakable and unshakable tie-up between plant and pollinating insect" (1) and the "quintessential example" of an obligate mutualism (2). In the simplest form of the story, the 40-odd species of Yucca (Agavaceae) are believed to be virtually dependent on the activities of four species of yucca moths (three Tegeticula and one Parategeticula) for sexual reproduction. The yucca moths are in turn obligately dependent on either Yucca seeds (Tegeticula) or degenerating ovules enclosed in cysts (Parategeticula) for their larval development.The behavior of the moths involved in the mutualism is unique in the Lepidoptera. Typically, a fertilized female moth enters a large creamy-white to pinkish Yucca flower and actively gathers a mass of the sticky pollen with her maxillary tentacles, specialized appendages formed by modifications of the maxillary palps. The moth leaves the flower carrying the pollen pressed with her tentacles and forelegs against her thorax and flies to another flower of (generally) the same Yucca species in which she then oviposits in one of its three carpels. She subsequently crawls up the style and smears some of the pollen from her load onto the stigma (Yucca whipplei) or forces it into the stigmatic cavity (all other species of Yucca). The moth can repeat the process of oviposition followed by pollination several times within a flower (3, 4). The eggs hatch and the larvae feed on the developing seeds or ovarian tissue, crawl out of the fruit, and then drop to pupate in the soil. This pollination system, referred to as brood place pollination, is rare (5, 6) presumably because the balance it imposes between parasitism and mutualism is a delicate one (7).The publication costs of th...

Repeated independent evolution of obligate pollination mutualism in the Phyllantheae– Epicephala association

“…Kawakita & M. Kato 423 yucca systems have indicated that these associations arose only once in each partner lineage 40-60 Myr ago (Pellmyr & Leebens-Mack 1999;Rønsted et al 2005). An exception is Hesperoyucca whipplei, which is phylogenetically distant from the rest of the yuccas and independently established the mutualism with a yucca moth (Bogler et al 1995;Pellmyr et al 2007;Smith et al 2008). In the Phyllantheae-Epicephala system, major lineages of Phyllantheae had already emerged when Epicephala colonized these plants ca 30 Myr ago.…”

The evolution of obligate pollination mutualisms: senita cactus and senita moth

“…Fruit production is resource limited in basal members of this family as well as in the highly derived Yucca, which is paraphyletic (Bogler et al 1995). Nocturnally opening¯owers and ample nectar production are common in basal members; nocturnal¯owering is retained but nectar production has been lost in Yucca.…”

“…The time lines for both curves are the same and re¯ect days since¯ower closing Table 2 Comparison of yucca and senita pollination mutualisms. Based on Shreve and Wiggins (1964), Addicott (1986), Powell (1992), Dodd and Linhart (1994), Bogler et al (1995), Pellmyr et al (1996) been important during the evolution of these obligate mutualisms. Nocturnal¯ower opening is important for the evolution of these mutualisms because it limits the number of potential¯ower visitors to moths.…”

Macroevolutionary assembly of ant/plant symbioses:Pseudomyrmexants and their ant-housing plants in the Neotropics

“…Co-speciation in mutualistic partnerships that do not involve vertical transmission may exist in some obligate systems-for instance figs and their wasp pollinators as suggested by matching divergence times, although occasional wasp switches to other figs have been documented [8]. Other obligate mutualisms, such as the Yucca/yucca moth pollination mutualism, were found to have evolved multiple times [9,10]. Non-specialized mutualisms can exist between partners of highly discordant ages, for example, between introduced plants and native insect or bird pollinators [11].…”