HERITAGE Yucca Moths and Yucca Plants: Discovery of “the Most Wonderful Case of Fertilisation” Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 Carol A. Sheppard and Richard A. Oliver he relationship between yucca plants (Yucca and Hesperoyucca spp.: TAgavaceae) and yucca moths (Tegeticula and Parategeticula spp. [Lepi- doptera: Prodoxidae]) is often cited as a clas- sic example of insect–plant coevolution and, in particular, obligate mutualism (Powell 1992, Thompson 1994, Price 1996, Proc- tor et al. 1996, Pellmyr 2003). Female yucca moths exhibit morphological and behavioral adaptations that ensure pollination of yucca plants, which have highly modified flowers that reduce the possibility of self-pollination or passive pollen transfer by other insects (Fig. 1). The ovaries of the plants serve as a protected food source for the females’ off- spring, which feed on seeds that develop as a result of the pollinating activity of the female moths. This relationship was first explored by the distinguished entomologist Charles V. Fig. 1. Illustration by C. V. Riley (1892b) of Tegeticula yuccasella (Riley) ovipositing on Yucca Riley1 (Fig. 2) during the early 1870s, about filamentosa. In this rendering, Riley shows a portion of the petals (top) removed to demonstrate a dozen years after the 1859 publication of that the anthers point away from the stigmatic tube, making self-pollination highly unlikely. the Origin of Species. At the time, Charles Darwin and Alfred Russel Wallace’s revolu- tionary theory of descent with modification denced the Creator’s handiwork. In contrast, Darwin’s interesting work on the was undergoing vigorous debate, in part Darwinian theory, and natural selection in fertilization of Orchids,2 we have come because scientists questioned the significance particular, removed all supernatural expla- to understand more and more the of the role played by natural selection. In nations in accounting for the diversity of life important part which insects play in addition, most older naturalists (i.e., those on earth and thus was problematic for many the fertilization of plants; and the old of Darwin’s generation) clung to natural the- naturalists with strong religious beliefs idea, that color and perfume in flowers ology, which held that organisms were placed (Mayr 1982, 1991; Ruse 1982; Bowler 1989; were intended for man’s especial on earth for man’s benefit and that their Moore 1993). pleasure, is giving way to the more countless and wondrous adaptations evi- This transitional phase in the scientific natural and philosophic view that they community’s conception of the natural world are useful to the plants by attracting was articulated by Riley in his earliest publi- the needed insects. (Riley 1873a, p. 57) 1For biographical treatments of Riley, reputedly the cation on the yucca moth: most important entomologist of the 19th century (Sorensen 1995), see Smith and Smith (1996) and Of late years, and more especially since Sheppard and Weinzierl (2002). the publication of Mr. Charles 2Riley made reference here to Darwin (1862). 32 AMERICAN ENTOMOLOGIST • Spring 2004 1929, White 1902, Long 1995), and at- tended the University of Heidelberg and Ber- lin University, receiving his M.D. from the University of Wurzberg in 1831. Engelmann’s friends and classmates included Alexander Carl Braun (1805–1877) and Karl Friedric Schimper (1803–1867), both of whom be- came well-known botanists, and the re- nowned naturalist Louis Agassiz (1807– 1873), who achieved great stature as a popu- lar lecturer and founder of the Museum of Comparative Zoology at Harvard Univer- sity. In 1835, Engelmann relocated to the United States at the request of his uncles, who wished to invest in land in the Missis- Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 sippi Valley. Engelmann’s emigration facili- tated his desire to explore the New World, following in the tradition of famed natural- ist and explorer Alexander von Humboldt, Fig. 3. G. Engelmann (from Gray and Trelease who sought to construct a holistic view of 1887). nature by teasing out relationships among the natural and physical sciences (Long 1995). of the United States, conducting field excur- Fig. 2. C. V. Riley, ca. 1873. Engelmann eventually settled in St. Louis, sions and visiting herbaria; and he produced Mo., where he became a leading physician. numerous botanical publications, many of Riley was 27 years old when he read this His medical career notwithstanding, Engel- them taxonomic/natural history mono- paper before his fellow members of the Acad- mann is a towering figure in the early days of graphs. emy of Science of St. Louis.3 A strong advo- American botany. Regarded as the indisput- In an era marked by U.S. exploration and cate of Darwinian theory, Riley rebutted the able authority of the Cactaceae and expansion, Engelmann received botanical criticism of many of his colleagues who ques- Coniferae, he also earned recognition as the specimens for study and classification from tioned the validity of the theory. He touted principal American authority on yuccas, aga- numerous federally funded expeditions. For the yucca plant–yucca moth relationship as ves, and American Vitis spp. (Rodgers 1944). more than 40 years, he contributed to the a remarkable example of Darwinian evolu- He traveled to Europe and various regions associated official reports including: C. C. tion; and, as the decades passed, Riley’s name and this storied case of plant–insect mutual- ism became conjoined. Yet Riley might never have become interested in the yucca moth, The genus Yucca (Family: Agavaceae) comprises plants had it not been dropped in his lap by George native to North and Central America, with approximately half Engelmann (Fig. 3), a senior botanist and of all yucca diversity occurring in Mexico. Several yucca colleague of Riley who was far from a Dar- win enthusiast (Goldstein 1989). species have been cultivated in Europe since the late 1500s. In this article, we revisit the interactions Y. filamentosa, the pollination of which first captured the of Engelmann and Riley when both were ac- attention of Engelmann and Riley, has been naturalized in tive members of the Academy of Science of the United States for more than 150 years. Yuccas are St. Louis. We then focus on Riley’s elucida- generally associated with arid biomes (chaparral, grassland, tion of the relationship between yucca plants shrub desert), but the two southernmost Yucca spp. occur in and yucca moths, an endeavor that engaged rainforests. According to Pellmyr (2003), Yucca taxonomy and him for over two decades and captured the systematics are in a state of flux and badly in need of interest of foremost scientists of the 19th revision, a formidable task because of a historically confused century, including Asa Gray, Charles Dar- nomenclature, use of horticultural material and cultivars of win, and William Trelease. We close with a unknown origin, a lack of herbarium material, and a dearth brief consideration of the more recent find- ings on this topic. of phylogenetic analyses. To view Yucca spp. images and distribution maps for the Engelmann: Biographical sketch and United States, Puerto Rico, and the Virgin Islands, consult the initial yucca observations USDA, NRCS PLANTS Database (http://plants.usda.gov). George Engelmann (1809–1884) was To view a color image of one of the first yucca moth born in Frankfort-on-the-Main, Germany specimens collected by Engelmann in 1872, see the web (Gray 1884, Gray and Trelease 1887, Bek page by Pellmyr (http://www.webpages.uidaho.edu/ ~pellmyr/Firstmoth.htm); a black and white image appears 3Organized in 1856, the academy resided in the in Pellmyr (2003). bustling portal city to the West and was the center of Missouri’s scientific activity (Hendrickson 1966). AMERICAN ENTOMOLOGIST • Volume 50, Number 1 33 Parry’s of the Colorado region and the Rocky which he accounted for unequivocally ac- academy’s earlier recording secretaries be- Mountains (Parry named a peak in the cording to Darwinian principles. cause of implicit or explicit censorship. Rocky Mountains for Engelmann), F. V. A year before Engelmann gave Riley the In his role as president of the academy Hayden’s of the upper Missouri Valley, C. yucca moth specimens, the two men sparred for 1876, Riley was the first to speak on the Wheeler’s of the territory west of the 100th over Darwinian evolutionary theory at the 6 topic of evolution (Hendrickson 1972). He meridian, A. W. Whipple’s of the region west- March 1871 meeting of the academy. We presaged the widespread acceptance of Dar- ward along the 35th parallel, J. H. Simpson’s might imagine the scene: the august Dr. En- winian theory in his presidential address, of the territory of Utah, J. C. Ives’s of the gelmann, then age 62, a founding member following the custom of reviewing the previ- Colorado river basin; and the reports of the of the academy and its first president (to ous year’s scientific developments: U.S. and Mexican Boundary Survey and the which post he was re-elected 15 times) ver- The visit of Prof. [T. H.] Huxley to Pacific Railway Expeditions (Gray 1884; sus the young challenger, Riley, age 26, serv- America must be looked upon as an Gray and Trelease 1887; Bek 1929, part 1). ing at his third meeting as the academy’s re- event in the progress of evolution in In addition to his work as a physician and cording secretary (Goldstein 1989). Accord- this country—…because he brought botanist, and in true Humboldtian fashion, ing to the academy’s Journal of Proceedings, in succinct form, and so conspicuously Engelmann also cultivated a serious interest the exchange unfolded as follows.