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. Dr. Engel- before the public, some of the best in meteorology and published articles on the mann presented three specimens of a weed arguments in favor of the doctrine. All Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 altitude of Pike’s and Long’s peaks in Colo- that were extraordinarily similar despite their great truths that oppose long rado (Hendrickson 1966). having been collected from St. Louis County, established popular belief must needs Engelmann first took notice of the genus Mo., France, and Italy. This prompted Riley belong to the few when nascent…in Yucca in 1842, when acquaintances sent him to ask Engelmann how he accounted for the my humble opinion, the idea of specimens from Texas, northern Mexico, and fact that many European plants and weeds evolution is founded on fact, and, like New Mexico (Engelmann 1873). In the years had become well established in the United a gem freed from the deposits which that followed, he paid particular attention States, yet very few American plants had be- for ages have hidden its lustre, will to yuccas on his U.S. and European expedi- come established in Europe. Riley added that shine all the brighter as the obstacles tions. In Europe, he was “first struck with insects in Europe vs. the United States exhib- which surround it are removed by the the ‘fact’ that ‘[y]uccas do not bear fruit’,” ited the same pattern. Engelmann replied that light of truth. (Anonymous 1868– whereas he had seen yucca fruits in some no theory was necessary to explain these 1877, p. ccxlvii) U.S. collections and observed yucca seed phenomena; the answer lay in the “fact that By this time, even Engelmann may have pods in St. Louis gardens (Engelmann 1873). some plants are more vigorous than others” moved somewhat closer to Riley’s thinking. He speculated that European yuccas were (Anonymous 1868–1877, p. xlii). Then, the At a March 1876 meeting of the academy, sterile because of incomplete development of Proceedings relate that Engelmann commented on the ability of cer- the flowers or problems arising from self- Mr. Riley undertook to account for it tain hybrid oaks to propagate “when re- fertilization. However, from the outset he on the Darwinian theory, that from moved from the struggle for existence” pre- considered the chances of self-fertilization to the greater competition and struggle sented by more hardy competitors be remote because the anthers of the yucca for existence that had gone on in (Hendrickson 1972). flower point away from the stigmatic tube, Europe under the civilized conditions making it extremely difficult for pollen to of man, their species were, many of Riley Embarks on his Yucca Moth– fall into this tube (Engelmann 1872, 1873). them, better able to thrive under similar Yucca Plant Studies Engelmann also noted that the glutinous conditions here than our own Riley reputedly pursued his research with nature of yucca pollen rendered it highly indigenous species. Dr. Engelmann enormous zeal and dogged determination improbable that the pollen could leave the feared such theories would lead us (Smith 1992, Smith and Smith 1996), traits anthers unassisted. astray. (Anonymous 1868–1877, pp. evidenced by his record of investigations of After observing yucca flowers in the xlii–xliii) yuccas and their associated insects. He set to United States, Engelmann concluded that Also present at the meeting was Dr. work immediately, examining the behavior “insects (in these night-blooming flowers, of Frederick Adolphus Wislizenus, age 61, an- of Engelmann’s little white moth; and within course, nocturnal insects) must be the agents other founding member of the academy and three months, he reported his initial findings which introduced the pollen into the tube” Engelmann’s long-time friend, fellow medi- in a paper read before the 21st meeting of (Engelmann 1873, p. 19) and suspected that cal practitioner, meteorologist, and botani- the American Association for the Advance- the pollinator was “a white moth of the ge- cal explorer. Wislizenus attributed the spread ment of Science (AAAS) in August 1872.4 nus Tortrix” (Engelmann 1872, p. 33). In of European plants to the greater space af- The next month he presented his paper to the summer of 1872, Engelmann passed to forded them in the New World, making no the members of the academy; and a few his young colleague, C. V. Riley, the insects mention of Darwinian theory. he found most frequently in the yucca flow- This sparring match marks the first of ers at night. several recorded between Riley and older 4This particular AAAS meeting is of historical significance in that the Entomological Sub-section was members of the Academy of Science of St. formed, at whose first meeting was discussed Samuel “Such Theories Would Lead Us Astray” Louis, who were grappling with Darwin’s H. Scudder’s “Revision of American Butterflies,” put Given Riley’s entomological expertise and revolutionary theory. The historian forth in advance of his Butterflies of North America. According to a report of the meeting, “There was a proximity to Engelmann, it is not surprising Goldstein (1989) characterized Riley as “an unanimous expression of regret and that the latter chose to give the yucca moths almost combative Darwinian” who intended disapprobation…at the wholesale and radical changes proposed by this distinguished author in the generic to his associate for further investigation. to “inject Darwinian theory into Academic and specific names of the butterflies.…The feeling was History, however, marks the irony of the discussions whenever possible.” Given that manifested by all, that changes so radical and so event because Riley quickly recognized the Riley joined the Academy in 1868, Goldstein sweeping in the received nomenclature were uncalled for, and would prove of great detriment to the study unique and mutually adaptive significance speculates that similar disputes may have and popularity of this department of entomology.” of the yucca plant–yucca moth relationship, taken place but went unrecorded by the (Anonymous 1872, p. 183)

34 AMERICAN ENTOMOLOGIST • Spring 2004 months later it was published in the Tegeticula yuccasella Pupae Described academy’s Transactions (Riley 1873a), pre- Riley was anxious to procure T. yucasella ceded immediately by a report by Engelmann pupae for taxonomic purposes. Because the (1873) on the genus Yucca. insect overwinters in the larval stage, he at- In his paper, Riley acknowledged his debt tempted to accelerate metamorphosis (i.e., to Engelmann for having drawn his atten- break diapause) by maintaining larvae at tion to the fact that filamentose-leaved spe- about 80o F throughout the winter of 1872– cies of yucca “must rely on some insect or 1873. His efforts met with modest success, other for fertilization” (Riley 1873a, p. 59). but in June 1873, he wrote a publication Riley erected the genus Pronuba for the yucca describing the chrysalids of the male and fe- moth, described both sexes and the larval male moth (Riley 1873b). stage of Pronuba (now Tegeticula) yuccasella Meanwhile, the report of his yucca moth (Riley), and related what he had ascertained presentation at the AAAS meeting had of the insect’s natural history. He observed piqued people’s interest, such that in his fifth that male and female moths meet and copu- annual report as Missouri state entomolo- late on the yucca flower. The female then gist, Riley (1873c) provided excerpts from Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 scrapes the pollen from the anthers with a letters sent by several readers, relating per- pair of highly specialized, prehensile, hairy sonal observations of seed production, or tentacles (Fig. 4), modifications of the basal lack thereof, by yucca plants. The letters, joint of the female’s maxillary palps not found which had been published in various peri- in males (Fig. 5). As he explained, “With her odicals, represented divers geographic re- maxillary tentacle [palp]…she collects the gions in the United States and Europe. Thus pollen in large pellets, and holds it under the Riley began the long process of amassing neck and against the front trochanters…she information relevant to his hypothesis about sometimes carries a mass thrice the size of the unique pollinating activity of T. her head” (Riley1873a, p.60). Once the fe- yuccasella. male has collected a ball of pollen, she “clings to the top of the pistil, bends her head, thrusts Oviposition and Pollination: Revision of her tongue into the stigmatic nectary and Hypotheses brings the pollen-mass right over its mouth” Riley worked sedulously and with great (Riley 1873a, p.60). care, as Pellmyr has commented: The female Tegeticula moth was the only [I]n contrast to the records of most of species that Riley found to be actively en- Fig. 4. Female T. yuccasella gathering pollen his contemporaries, there are very few gaged in pollinating yucca flowers,5 but dur- (from Riley 1892b). inaccuracies in [Riley’s] accounts, ing the 1872 season, he was unable to wit- simply because of his reliance on ness any females in the act of oviposition. He his most important yucca-related hypoth- empirical observation. In this, he knew of no Lepidoptera that oviposited by esis: that yucca moths serve as the sole polli- arguably belonged in the exclusive puncturing the flesh of fruit, and found no nators of yucca plants. group of exceptional naturalists with evidence that any punctures led to eggs nor that eggs were deposited externally. Given this, Riley hypothesized that T. yuccasella eggs were inserted into the fruit through the pol- len tubes. In addition, because he had exam- ined “hundreds of [yucca seed] capsules” around St. Louis and southern Illinois, of which “not more than four or five percent were uninfested,” he conjectured that ovi- position immediately followed, not preceded, pollination (Riley 1873a, p. 62). Reportedly Riley’s AAAS paper was “lis- tened to with marked attention, and was fol- lowed by an animated discussion” in which Asa Gray, then out-going AAAS President, and others took part (Anonymous 1872). Gray, a renowned Harvard University taxo- nomic botanist and the most influential American advocate of Darwinian theory (Dupree 1959, Ghiselin 1969), was held in high esteem by Riley. A few years later, Riley sent Gray yucca moth cocoons to help test

Fig. 5. Illustration by Riley (1873a) from his first yucca moth publication, showing key features 5Riley (1873a) listed several other non-pollinating insects (Coleoptera and Heteroptera species) that he of adult T. yuccasella: (a) denuded head of female with (1) pollen mass, (b) female maxillary palp had collected from yucca flowers. with (c) tubercle, (j) ovipositor.

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 35 whom he regularly corresponded, such as Charles Darwin, Alfred Russel Wallace, Henry Walter Bates, Thomas Belt, Fritz and Hermann Müller, and Asa Gray. (Pellmyr 2003, p. 37) By the close of the 1873 summer season, Riley reported his further observations of the oviposition behavior of T. yuccasella. As noted earlier, he had initially hypothesized that oviposition occurred after pollination, and that the ovipositor was not used to punc- ture the fruit of the plant (Riley 1873a). These hypotheses proved incorrect. In collaboration with Engelmann, Riley (1873d, 1874) discovered that the female’s ovipositor does, in fact, puncture the ovary. Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 Over time, the aperture of the puncture forms a depression and, as the fruit enlarges, the oviposition passage becomes obliterated, which explains why Riley was misled by his initial observations. Indeed, only by dipping the pistil in ink a day or two after oviposi- tion and examining the stained tissue under a magnifying lens was he able to trace the passage created by oviposition that led to the egg locus. Riley explained that he could observe the oviposition of hundreds of eggs because once the female selects a suitable site and her ovipositor penetrates the pistil, “the 6 whole perigon may be detached, some of Fig. 6. Engelmann’s unpublished sketches, dated July1873 (Missouri Botanical Garden, William the encumbering petals and stamens re- Trelease Professional Papers, Agavaceae, Box 8). Far left, T. yuccasella egg, 60–66 hours post- moved, the insect brought within focus of a oviposition in Y. filamentosa. The elongate egg (1.5 mm long, 0.08 mm diam) holds the developing good lens and all her movements observed “curled up larva” at one end. Sketches at right compare relative size and form of an ovule 60–66 to the greatest advantage, without disturb- hours post-ferilization (top) vs. an unfertilized ovule from a bud (bottom). In the former, the ing her” (Riley 1873d, p. 620). stigmatic tube is closed, whereas in the latter it is still open. Also contrary to his original hypothesis, Riley determined in the second season that the female first oviposits, and then, “no by the aid of which our yuccas can be Engelmann (1875) reported that the stig- sooner is the ovipositor withdrawn into the fully fertilized; for I have studied this matic opening closes immediately after the abdomen than the moth runs up to the top fertilization diligently night after night, first night of flowering (Fig. 6). Riley (1873d) of the pistil, uncoils her pollen-bedecked ten- without seeing any other species go thus noted that it is during this one night tacles, thrusts them into the stigmatic open- near the stigma. (Riley 1873d, p. 622) that female T. yuccasella must pollinate the ing, and works her head vigorously…up and yucca and lay her eggs; subsequently, Riley down” (Riley 1873d, pp. 620–621). He Engelmann’s Further Studies of T. (1892a) stated that, on occasion, this added that the female may deposit two, three, yuccasella and Yucca spp. timeframe could be 1–2 nights. These find- or more eggs before pollination occurs, and During the summer of 1873, while Riley ings are substantiated in a recent review he suspected that “the converse of this is pursued his yucca moth oviposition studies, (Pellmyr 2003). equally true” (Riley 1873d, p. 621).7 Engelmann made in situ observations of T. At the conclusion of his paper, he strongly yuccasella in various yucca species. His origi- Influence of Darwin and Gray on Riley’s reiterated his view: nal drawings depict egg morphology and Scientific Conceptualization [My observations this summer] have embryonic development of T. yuccasella con- The work of Darwin strongly influenced convinced me more than ever that comitant with early post-fertilization changes Riley’s scientific conceptual framework. He Pronuba [Tegeticula] is the only insect in the yucca ovule (Fig. 6). He observed that unequivocally supported the Darwinian the developing embryo, with segmentation, theory of species origin versus the older view is evident at 60–66 hours after oviposition of special creation and immutable species. 6"Perigon” (Latin form of “perigone”) refers to a (Fig 7). Engelmann also found that very soon Moreover, Riley immediately recognized that flower in which the calyx and corolla (collectively after oviposition, the young seeds “begin to the mutualism between yucca moths and termed the perianth) are not clearly differentiated. (Swartz 1971) swell up to three or four times the thick- yucca plants represented “one of the first ness” of the normal seeds and “are thus pre- and strongest examples of evolution by paring the sustenance of the young larva, means of natural selection” (Pellmyr 2003, 7The latter scenario, which has never been documented which feeds on one or usually both of them p. 36). Riley openly expressed this opinion (Olle Pellmyr, personal communication), would until able to attack the meanwhile more or at scientific meetings and in publications, and account for the pollination of capsules that contain no larval Tegeticula nor evidence of ever having less developed young seeds” (Fig. 7; Engel- often interpreted his entomological findings contained any. mann 1875, p. 211; Riley 1873d). in light of evolutionary theory. For example,

36 AMERICAN ENTOMOLOGIST • Spring 2004 cited Gray’s 1872 work, How Plants Behave, in his first yucca moth publication to sup- port the fact that, typically, the flowers of angiosperms are “curiously and elaborately constructed so as just not to do of them- selves what must necessarily be done for them in order to prevent degeneracy or ex- tinction of the species,” thereby facilitating cross-pollination (Riley 1873a, p. 57). He pointed out that many plants depend on other organisms to transfer their pollen from plant to plant and stated that the yuccas he had been studying “seem to depend for as- sistance, so far as we now know, on the single little Tineid [Prodoxid] which I have de- scribed” (Riley 1873a, p. 58). Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021

Evidence for the Exceptional Pollinating Activity of T. yuccasella Whether Riley anticipated that his yucca moth research would span two decades and Fig. 7. Engelmann’s unpublished sketches, dated July 1873, of T. yuccasella development in raise the hackles of many a colleague is moot; Yucca flaccida (Missouri Botanical Garden, William Trelease Professional Papers, Agavaceae, undoubtedly, he was cognizant from the Box 8). Top left, larva (1 mm in length) at 60–66 hours after oviposition, showing segmentation; outset of the enormity of his claim, which he top and lower right, seeds with spherical holes from feeding larvae, which eclose from the egg had couched in cautious terms in his first 4–5 days after oviposition. Lower left, seed pod. yucca moth publication (Riley 1873a). He admitted that he knew of no other case in which a single insect species was solely re- in his first yucca moth publication, he wrote: neither. These peculiarities are, sponsible for pollinating a given plant, and We have in this little moth a remarkable moreover, mutually and reciprocally he had witnessed the discussion that his pre- adaptation of means to an end. There beneficial, so that the plant and the sentation provoked among his respected is between it and its food-plant a animal are each influenced and colleagues at the 1872 meeting of the AAAS. mutual interdependence which at once modified by the other, and the same Riley based his hypothesis on several lines excites our wonder, and is fraught with laws which produced the beneficial of evidence: His observation that female T. interesting suggestions to those who specialization of parts would maintain yuccasella was the only insect found actively are in the habit of reasoning from them by the elimination of all forms pollinating the flower; the appearance of the effect to cause. Whether we believe, as tending to depart from them. (Riley female’s highly modified maxillary palps and I certainly do, that this perfect 1873a, p. 63) her behavior regarding pollen collection and adaptation and adjustment have been Riley recognized the significance of cross- deposition; the fact that exclusion of the fe- brought about by slow degrees pollination largely because of Darwin’s work male moth (by netting) did not result in yucca through the long course of ages, or in this area.8 In a paper summarizing his many self-pollination; and the glutinous nature of whether we believe that they always years of research on the relationship between yucca pollen. He also had additional infor- were so from the beginning, they are yucca moths and yuccas, Riley made refer- mation from Engelmann, Gray, and others, equally suggestive of that same law and ence to several of Darwin’s botanical publi- who reported that yucca plants introduced harmony so manifest throughout the cations from the 1860s: to northern United States and European gar- realm of Nature. (Riley 1873a, p. 63) The importance of insects as agents in dens where the yucca moth is absent fail to In this same paper, Riley elaborated on cross-fertilization was scarcely yield fruit and seed, but that pods of wild the adaptive advantages to the yucca plant appreciated, however, until the late yucca (Yucca angustifolia, [now Y. glauca] and the yucca moth: The plant was guaran- Charles Darwin published the results from the Black Hills of Colorado, Y. rupicola teed pollination with a high degree of prob- of his researches on Primula, Linum, from Texas, and Y. whipplei from Califor- ability, and it lost only a few seeds in return; Lythrum, etc., and his elaborate work nia) show “unmistakable holes of egress of the insect received a safe larval feeding site. on the fertilization of orchids. The the larvae” (Riley 1873a, p. 64). As a good Darwinist (and with clear refer- publication of these works gave to In his first yucca publication, Riley ex- ence to plant–insect coevolution), Riley ac- flowers a new significance and to their pressed hope that “the next blooming-sea- counted for this arrangement on the basis of study almost as great an impulse as son of our Yuccas will find other eyes than gradualism, postulating that this mechanism did his immortal “Origin of Species” my own watching [Tegeticula’s] ways and could have resulted in the development of to the general study of biology.9 (Riley methods,” because much remained to be dis- the “peculiarities” present in the plant and 1892a, p. 101) covered about the insect (Riley 1873a, p. 63). the insect: Riley’s early thinking about pollination Such professional generosity may sound [I]t is quite easy to conceive, on also drew upon the work of Asa Gray. Riley somewhat specious, given the potential im- Darwinian grounds, how both these characters may gradually have been 8Darwin’s influence in this regard has been noted by 9Riley (1882) articulated the same thoughts in an produced in the course of time from many; see Ghiselin, 1969, Faegri and van der Pijl earlier address to the Biological Society of Washing- archetypal forms which possessed 1971, Bowler 1990, Proctor et al. 1996. ton.

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 37 pact of such an extraordinary discovery, Riley wrote from 1893 to 1894 indicate that other provocation for it than a certain but perhaps he believed that the opportu- the following correspondents were sent co- ill-will on my critic’s part. It comes, too, nity to obtain corroborating evidence out- coons: Professors M. Valery Mayet and M. with all the less grace from one who weighed the possibility of another scientist Viala (Ecole Nationale Agronomique, confessedly made hasty and incorrect stealing his thunder. In any event, the most Montpellier, France), D. Morris (Assistant observations on the position of the meaningful publications on yucca moths Director, Royal Botanic Gardens, Kew, En- species. From one less honored and and mutualism would come from Riley, and gland), T. Hanbury, FRS (Ventimiglia, Italy), esteemed, such captious remarks T. yuccasella and other insects closely asso- and Professor G. L. Goodale (Cambridge, would have received no notice at my ciated with yuccas would continue to be a Mass.). Riley asked that the cocoons be hand. (Riley 1876, p. 326, fn.) part of Riley’s scientific investigations for placed around yuccas in the filamentose In response to his publication, Riley received 20 years. group, or those which typically bloomed in a personal letter from Zeller14 that began, May and June. You do me a great injustice by thinking Riley Sends T. yuccasella Cocoons to that I wrote the notes on Pronuba Colleagues Criticism and Confusion: True Yucca [Tegeticula] with any ill feeling towards Riley hypothesized that if T. yuccasella Moths, Bogus Yucca Moths, and More you. I am quite convinced that if were the sole pollinator of yuccas, then yuc- In the years following his first publica- you had written them in the same Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 cas that never produce fruit should be found tion on the yucca moth, T. yuccasella, Riley manner in opposition to me I would in areas where yuccas had been transported encountered much criticism, from botanists not have felt injured at all, but would but the moth was absent. He further rea- and entomologists, who questioned his sci- only have felt impelled to repeat my soned that if his hypothesis were correct, in- entific description of the moth, his observa- observations, for, least of all, do I hold troducing yucca moths to areas devoid of tions of its behavior, and his conclusions myself to be infallible, but am of the moths would yield fruit-producing yuccas. about its unique relationship with yucca. As opinion that every observation must Riley proposed to test the validity of his hy- we will discuss, many of the disagreements go through the crucial test of repetition pothesis: arose because naturalists unwittingly con- by several observers before it can It is my intention to obtain a large fused T. yuccasella with other insect species. be regarded as correct and number of cocoons this year Regardless of the reasons underlying a given incontrovertible. and…distribute them among those contentious issue, Riley’s record of scientific In his letter, Zeller stated that he had asked who grow the yucca in those parts of publications and presentations attest to the Stainton for his opinion of the polemic. this country or in Europe where seed considerable time and energy he expended Stainton replied that Zeller’s statements re- is not produced. (Riley 1873d, pp. countering those who impugned the accu- garding Riley’s observations were “truly 622–623) racy of his findings. Zellerian, i.e., a little too dogmatic. You say During 1873 and 1874, Riley sent larvae Riley vs. Zeller that it is quite impossible that Yucasella can (the numbers are shown in parentheses) in The first dispute occurred when Professor do what R. says it does.” Zeller explained to their cocoons to Asa Gray, Cambridge, Mass. P. C. Zeller, an entomologist from Prussia, Riley that because “even great investigators, (150); botanist Jules-Emile Planchon,10 questioned Riley’s assertions that larval yucca as for example Réaumur, have made mis- Montpellier, France (100); botanist moths lack anal prolegs and that the adult takes,” the remarkable features that Riley Hermann Müller, Lippstadt, Germany (250); female moth collects pollen with her maxil- had described caused him to question Riley’s Charles Darwin, Down, England (100); lepi- lary tentacles. (Pellmyr [2003] has pointed observations. In closing his letter, Zeller dopterist Henry Tibbats Stainton, out that Zeller’s experience with yucca moths wrote: “As you have up to this time only Mountsfield, England (50); and Meade was “limited to three pinned specimens given shown a kind spirit toward me, I cannot Woodson (whom Riley described as a “great to him.”) Zeller proposed that the female’s imagine at all how I could return it with ill- admirer” of Yucca), Kansas City, Mo. (100) “tongue” (proboscis) could, by itself, accom- will.” Whether Riley responded to the letter (Riley 1881). Riley requested that the co- plish the task of gathering pollen. is unknown. coons be buried in the ground near yucca In his rebuttal, a clearly vexed Riley (1876) Riley vs. Boll plants. Darwin, having no yucca plants at reiterated his published statement, in which Jacob Boll of Dallas, Tex., attempted to his home, sent his insects to Joseph Dalton he had indicated that all of his conclusions refute Riley’s oviposition and pollination Hooker, noted botanist and director of the had been based on careful, repeated observa- findings with assertions based on cursory Royal Botanic Gardens, Kew, England.11 tions conducted over the course of three sum- observations and a poorly designed experi- Müller’s moths hatched, but no ornamental mers. He also took umbrage at Zeller’s last ment. Moreover, Boll had never bothered to yuccas were in flower at the time (Pellmyr sentence13 : “In my opinion, Riley, while mak- read Riley’s yucca moth publications and 2003) and the results of the remaining ex- ing his most interesting discovery, hasn’t seen eventually admitted to Riley that he “knew periments are unknown. everything yet; and other observers will be absolutely nothing of [Riley’s] writings on We do know that Riley was mailing yucca necessary to explain satisfactorily the curious the subject except what he learned through cocoons to naturalists until just before his goings-on during reproduction of the moth.” Prof. Zeller’s notice” (Riley 1877, p. 572). accidental death in 1895. Extant letters12 that Riley wrote: Unlike Riley, Boll (1876) made no effort to …as for the reflection in the last observe the behavior of the moth under field sentence which I have quoted, I am conditions, but instead he had caged female 10Planchon collaborated with Riley on grape vain enough to believe that there is no yucca moths with cut yucca flowers that had phylloxera research (Smith 1992). apparently already been fructified. Boll also put forth the fallacious notion that the fe- 11Darwin to Hooker, 7 April 1874 (Cambridge 13"Meines Erachtens hat Riley bei seiner höchst University Library, classmark DAR 95:321). interessanten Entdeckung noch nicht Alles gesehen, und noch andere Beobachter werden erforderlich sein, 14Missouri Botanical Garden, William Trelease um die sonderbaren Vorgänge bei der Fortpflanzung professional papers, Box 8, folder 1; letter dated 3 12Missouri Botanic Gardens: William Trelease papers. der Motte ganz genügend zu erklären.” April 1876.

38 AMERICAN ENTOMOLOGIST • Spring 2004 male yucca moth used pollen or stamen hairs Boll’s moths were not, in fact, T. yuccasella, to seal her oviposition puncture. He further but a closely related species. One month later, opined that the exclusive fertilization of yuc- Riley attended the annual meeting of the cas by yucca moths had not been proven AAAS held in Saratoga, N.Y. There he an- and that “internal fertilization, if one should nounced to the Entomology Club that he take this for such, would belong to the realm had likely discovered the cause of the dis- of fable” (cited in Riley 1877, p. 573). Riley crepancy between his findings and those of called Boll’s publication “palpably superfi- Boll and Chambers—namely, that the moths cial and erroneous” (Riley 1877, p. 570) and the latter two had been observing were concluded with a biting rejoinder: Prodoxus decipiens Riley15 (Lepidoptera: Mr. Boll should increase his knowledge Prodoxidae) (Riley 1880b) (Fig. 8). Al- by perusing what has been written on though very similar in appearance to the the fertilization of flowers by insects. yucca moth, P. decipiens oviposits on the He should also learn something more flower stem and is not a yucca pollinator than he has done in this instance of a (Fig. 9). subject he intends to treat, and Ever the careful observer, Riley had re- Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 especially of observations which he has ported the presence of the then-unnamed P. undertaken to criticize. Investigations, decipiens in his first yucca moth publication. however instigated, should be carried He wrote of finding “a smaller white, on, not under the warping influence apodous larva” in the pulp of Y. aloifolia, of individual motive, but solely for the “sometimes in considerable numbers,” love of truth and knowledge. (Riley which “occasionally gnaws into the seed from 1877, p. 573) the outside,” adding that this larva has hy- Riley vs. Chambers menopterous affinities and that its legless Another clash occurred in 1877, when V. character “will at once distinguish it” from T. Chambers published his account of the larval Tegeticula (Riley 1873a, p. 59, fn.). Tineina of Colorado in Hayden’s Geological In the publication that derived from his and Geographical Survey of the Territories. presentation at the 1879 AAAS meeting, Chambers (1877) claimed that he had dis- Riley (1880a) pointed out the various ways covered a “spotted version” of adult Pronuba [Tegeticula], thereby bringing into Fig. 9. Riley’s rendering of a yucca flower question Riley’s taxonomic description of the stem with (a) oviposition scars and (b) pupal moth’s front wings as “uniformly silvery- exuvia of P. decipiens (from Riley 1892a). white.” Chambers sent all of his specimens to Hagen at Harvard, a few of which were forwarded to Riley, whose incredulity upon in which Prodoxus differed from Tegeticula: examining the specimens is evident in this The adults show an inclination to macula- passage: tion, and the female lacks the characteristic …what is more remarkable, they are maxillary tentacles; the larvae are legless; and one of Mr. C.s’ own described there are differences in the chrysalis, male species—[H]yponomeuta 5-punctella. genitalia, and habits of the two species. Of the six specimens submitted to me, In addition, having been unable to exam- there was but one Pronuba ine Chambers’s “supposed spotted [Tegeticula], and that was immaculate, Pronubas [Tegeticula], the types of which are as the species always is. …I have reared in the Cambridge [Harvard University] mu- upward of 500 specimens of Pronuba seum,” Riley conjectured that the specimens [Tegeticula], and have it from South would turn out to be Prodoxus, based on Carolina, Texas, California, Colorado Chambers’s description of its habits and his and Missouri, and there is never the depiction of the pattern of maculation. He faintest tendency to maculation. (Riley openly expressed his displeasure with the 1877, p. 569) carelessness of Chambers’s scientific work: To make matters worse, Riley was asked We assumed that Mr. Chambers had by Hagen not to denude the specimens and, made a proper reference in describing as a result, was incorrect in his identification his Hyponomeuta 5-punctella, but we of the “spotted” Tegeticula as H. 5-punctella are now perfectly satisfied that he had Chambers. Riley would eventually be in a not, since many specimens of position to correct his error and, in so do- Prodoxus agree exactly in maculation ing, erect a new genus. Fig. 8. Female Prodoxus decipiens Riley with his description and figure. More As fate would have it, in July 1879, Riley ovipositing in a yucca flower stalk (from Riley careful study plainly shows that had occasion to pass through Dallas, where- 1892a). Prodoxus does not even belong to the upon he visited Boll, who had bred what he same family, but must be placed with thought to be T. yuccasella from the flower Pronuba [Tegeticula] in the Tineidae. 15The genus name derives from the Greek, “judging of stem of Y. rupicola (Riley 1880a). Upon ex- a thing prior to experience” (Riley 1880b, p. 155, …Mr. Chambers…has published some amining the insects, Riley determined that footnote). 14 pp. of matter containing many

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 39 interesting but irrelevant facts, and had been unwilling to send Riley any of in which he claimed to have bred T. yuccasella more that is funny than convincing Meehan’s specimens for identification be- from yucca flower stems, was in error. when it comes to the point at issue. He cause, Hagen explained, he had been study- Riley’s abstract for the 1882 AAAS meet- brings forward no fresh evidence ing them and was “about to publish it” ing resounded with confidence that his latest except such as he calls circumstantial, (Hagen 1880). As we shall see, Riley would findings would finally silence his critics: and admits that he does not ‘pretend once again find himself defending his find- This paper records some recent that they [the arguments] are ings (this time to Darwin) because of Meehan’s experiments and observations which conclusive of the question, especially flawed scientific work and unfounded asser- establish fully and conclusively the fact when opposed to the positive tions. that Pronuba [Tegeticula] is necessary statements of so competent an to the fertilization of the capsular observer’. (Riley 1880a, p. 143) Riley Erects Prodoxidae; Hagen Yuccas. It describes for the first time Recent research has revealed another Misidentifies P. decipiens how the pollen is gathered and twist in the P. decipiens story. For many years, In 1878, Riley resigned his post as the collected by the female Pronuba this species was considered synonymous with first state entomologist of Missouri to be- [Tegeticula]. The act is as deliberate and P. quinquepunctellus (Chambers) (Chambers come the head federal entomologist in Wash- wonderful as that of pollination. 1875). However, Althoff et al. (2001) have ington, D.C., the position he held (except for Going to the top of a stamen she Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 shown P. decipiens to be a distinct species, a 2-year hiatus) until 1894, the year before stretches her tentacles to the utmost ranging from the eastern United States west- his death. During that time, Riley briefly re- on the opposite side of the anther, ward to central Texas; Riley’s P. decipiens vived the American Entomologist as a new presses the head down upon the pollen series derived from South Carolina. series and, with L. O. Howard, co-edited a and scrapes it together by a horizontal P. quinquepunctellus occurs in the southwest- new journal, Insect Life, published by the motion of her maxillae. The head is ern United States into the northern Bureau of Entomology, USDA. He also was then raised and the front legs are used Great Plains states; Chambers’s P. founder and first president of the Entomo- to shape the grains into a pellet, the quinquepunctellus specimens were from logical Society of Washington [D.C.] and a tentacles coiling and uncoiling Colorado. These two sister taxa are sympa- founding member of the Biological Society meanwhile. She thus goes from one to tric in central Texas (Althoff et al. 2001). It is of Washington [D.C.], both of which pub- another until she has a sufficiency. also worth noting that although Riley (1880a) lished their own Proceedings. Thus, much of (Riley 1883, p. 467) stated that a few P. decipiens larvae are found the ensuing yucca-related controversy was Riley (1883) reported several other im- in the fruit, this observation has not been recounted by Riley in the pages of these peri- portant findings: He confirmed Engelmann’s corroborated and whereas certain prodoxids odicals and at his presentations at AAAS conclusion that the stigmatic apices of cer- are gall-makers in fruit, no species is known meetings. tain Yucca species are impotent and that the to do both (Olle Pellmyr, personal commu- In 1881, a seminal paper by Riley ap- flower morphology of Y. aloifolia, the only nication). peared in the Proceedings of the AAAS,17 species known to self-fertilize, is such that Riley vs. Meehan which he sent to Darwin (discussed later). In the flowers can achieve this task; he demon- Mr. Thomas Meehan, botanist and edi- this publication, Riley summarized his yucca- strated that the irregularities in yucca pods, tor for Gardeners’ Monthly, also attended associated findings to date; quoted exten- then considered a character state by bota- the 1879 AAAS Saratoga meeting. He gave a sively from the criticisms by Meehan and Boll nists, are attributable to Tegeticula oviposi- paper in which he reported that although he of his work and his rebuttals thereof; de- tion punctures (Fig. 10); and he determined had observed T. yuccasella to be abundant scribed several new yucca-associated insect exactly where and how the egg of Tegeticula at the time of flowering of Y. glauca, the plant species (Pronuba [Tegeticula] maculata, is oviposited by examining the internal never produced fruit unless he artificially Prodoxus intermedius [now Tegeticula anatomy of the yucca ovule and the oviposi- pollinated it. Based on this, he concluded that intermedia (Riley); see Pellmyr 1999], tor of T. yuccasella. His new findings not- T. yuccasella must not pollinate Y. Prodoxus marginatus, Prodoxus cinereus, withstanding, if Riley believed that he had at filamentosa as Riley had claimed. and Prodoxus aenescens); noted that G. H. last quelled the yucca moth controversy, he Riley (1877) had known since 1876 that Horn had informed him that the name was indeed mistaken. T. yuccasella adults typically appear 2–3 Pronuba was preoccupied in Coleoptera and Riley vs. Hulst weeks after Y. glauca blooms and that this if so, then Zeller’s Tegeticula would take pre- In 1886, the Reverend George D. Hulst yucca species rarely produces seed. He in- cedence; and erected a new family, instigated what would become a contentious formed Meehan at the AAAS meeting that Prodoxidae, which stands today. debate with Riley. Hulst, editor of the jour- the moths in question most likely were P. Riley (1881) also set the record straight nal Entomologica Americana, argued in its decipiens. Riley added that the one time he on two points of taxonomic interest. First, pages that honey bees must be extensive did observe a few seeds in Y. glauca in St. he corrected his earlier misidentification of fertilizers of yuccas because he had observed Louis was when it had bloomed a bit later the specimens that Chambers had sent to honey bees “plentiful about the flowers,” than usual; upon inspection, he found that Hagen—having finally been given permission the majority of yucca seed capsules he ex- the capsules contained T. yuccasella larvae. to denude some of Chambers’s specimens, amined gave no indication of the presence As if to further frustrate Riley, Meehan, like Riley identified them as a 5-spotted form of of Tegeticula larvae, and yuccas are some- Chambers, had sent his specimens (living lar- P. decipiens, thereby supporting the validity times fertile in foreign countries (Hulst vae) to Hagen,16 who initially thought them of his earlier conjecture (Riley 1880c). Sec- 1886). In response, Riley began by under- to be Coleoptera; once they had pupated, ond, Riley reported Hagen’s admission to scoring the depth and breadth of his yucca Hagen realized his error. At the time that having mistaken P. decipiens for T. yuccasella; moth studies: Riley’s paper (1880a) went to press, Hagen thus, Hagen’s then-recent publication (1880), For over 16 years now I have very carefully studied the habits of Pronuba 16According to Hagen (1880), Meehan sent the 17This paper was read by Riley at the 1880 AAAS [Tegeticula] in connection with Yucca, specimens at Engelmann’s request. meeting (Anonymous, 1880). not in one locality alone but in nearly

40 AMERICAN ENTOMOLOGIST • Spring 2004 from the same flower or from other flowers either on the same or other racemes, by touching the mere apices with anther or brush, and by forcing the pollen by either conveyance into the stigmatic tube. In these experiments…I have endeavored to guard against all influences, such as the condition of the plant and the weather, which might affect or vitiate the results. (Riley 1888, pp. 151) Riley also contrasted Hulst and “his good friend” Meehan, stating that the latter had written much on the fertilization of Yucca—much, too, that has not shown the keenest penetration nor the Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 strictest accuracy. But, in candidly admitting his errors when shown to be wrong (as he has done to the writer, and, I have reason to believe, to Mr. Hulst, who sought his support in the Fig. 10. Illustration by Riley (1892a) of mature pods of Y. angustifolia (now Y. glauca): (a) belief here combated), he has proved artificially pollinated (thus lacking punctures and constrictions due to oviposition), (b) pollinated himself to be the true naturalist. (Riley by Tegeticula (showing oviposition punctures, constrictions, and larval exit holes), (c) larva 1888, p. 150–151) within the pod. Riley pointed out that Meehan had been working with Y. glauca, whose flower mor- phology and abundant stigmatic liquor likely every State east of the Rocky remain open until 10 a.m., and “business made it more susceptible to artificial pollina- Mountains where that genus occurs hours for honey bees begin long before that tion; a quote from a letter of Engelmann to either indigenously or by introduction. time” (Hulst 1887, p. 237). He added that Riley supported this assertion. Riley also cited I have also had occasion to study it in Meehan’s work with artificial fertilization the research of his trusted colleague, botanist many places in Europe in which it is suggested that self-fertilization in yuccas was William Trelease, who had shown that female cultivated, and the results have been possible. Tegeticula, in the act of pollinating, repeats published in several papers. (Riley The beleaguered and clearly annoyed the process several times, “first from one of 1887, p. 233) Riley penned his response in August 1887, the angles between the apices, then from an- Riley continued, stating that he had seen while en route to Europe, and mailed it to other, and…the tongue18 is used, in addition neither honey bees nor other nectar-feeding Hulst from England (Riley 1888, p. 150, fn.). to the tentacles, to push the pollen down to Hymenoptera frequenting yuccas and that But according to Riley, Hulst “exercised his the bottom of the tube” (Riley 1888, p. 152). this was not surprising, given certain char- editorial prerogative in declining to publish In addition, Riley (1888) provided more acteristics of the flowers—they are half- [Riley’s] communication…” (Riley 1888, p. recent evidence to discount Hulst’s belief that closed in the daytime, opening when bees 150, fn.), which prompted Riley to send his honey bees could serve as pollinators of yuc- are done foraging, and their glutinous pol- response to the Proceedings of the Entomo- cas. He had those in his employ (L. O. len would not stick to hirsute Hymenoptera. logical Society of Washington. Riley ex- Howard, T. Pergande, O. Lugger) observe He reiterated that years earlier, he had listed plained that he had deferred in his response more than 200 yucca stalks at the USDA in the insect species found in yucca flowers to Hulst mostly because he had hoped that Washington between 9 and 10 a.m., and no and that his associates and others had cor- Hulst “would himself gracefully amend his honey bees were seen around the flowers. roborated his findings. In response to opinions to accord with the facts” because Riley noted that he himself had seen a single Hultz’s criticism that T. yuccasella larvae are the yucca fruiting season had ended, and he bee on two occasions, but each time it merely not always found in the fruit, Riley empha- would have been “able to make more careful probed the flower on its outer base and flew sized that pollination can (albeit rarely) oc- observations” (Riley 1888, p. 150). Riley off without entering it. Furthermore, Riley cur without oviposition, and that sometimes then countered each of Hulst’s arguments in noted, these findings had been corroborated the eggs may fail to hatch successfully or full, stating that he had “followed up on by Professors Cook and Beal at Michigan the larvae may perish (in which cases the [Meehan’s] experiments, and made many State Agricultural College (now Michigan fruit bear evidence of oviposition activity). others during the past seven years, on [Yucca] State University). Riley cited his earlier publications, which filamentosa and aloifolia.” At a time when Lastly, Riley related the findings of Trelease provided substantiating evidence in re- relatively few entomologists were perform- (1886), who reported that the stigmatic cav- sponse to others who also had questioned ing experiments of any sort, Riley’s brief de- ity of Y. filamentosa is not nectariferous and his findings, to rebut Hulst’s other criti- scription of the pollination experiments he that the small amount of nectar it secretes is cisms. conducted speak to his scientific acumen and Unconvinced by Riley’s reply, Hulst the thoroughness of his approach: (1887) wrote a rejoinder that was printed My experiments have been made in 18Trelease (and Riley 1873a) was incorrect, as the immediately beneath Riley’s response. Hulst the afternoon, evening, and morning, “tongue” is not used to pollinate, but is held straight out above the tentacles. However, he subsequently persisted in his belief that honey bees could with flowers one day, two days, and described its proper position during pollination for T. act as yucca pollinators because the flowers three days after opening; with pollen synthetica (Trelease 1893).

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 41 located at the base of the pistil or the petals, point in time, Darwin was well acquainted plant does very little good; & if I am not near the stigma. Riley stated that he had with Riley’s work because the latter had sent not mistaken you believe that Pronuba corroborated Trelease’s findings “by dissec- him copies of his Annual Report of the Mis- [Tegeticula] gathers pollen from the tion [of the pistil] and study of the insects souri State Entomologist. Indeed, according same flower which she fertilizes—. seeking this scant nectar” (Riley 1888, p. to Darwin’s son, Francis, and A. C. Seward, In his reply,22 Riley clarified his findings 154). “These reports were greatly admired by Mr. regarding Tegeticula and cross fertilization23: Without doubt (and understandably so), Darwin, and his copies of them, especially of My language is perhaps ambiguous what most infuriated Riley was Hulst’s alle- Nos. 3 and 4, show signs of careful read- on this point, but in fact she not only gation that “[to] Dr Engelmann…we are in- ing.” (Darwin and Seward 1903, p. 385, fn. pollinizes with the same load of pollen debted for the discovery of the fact that 2). different flowers on the same panicle, Pronuba [Tegeticula] is an agent in the fer- Darwin (1876) cited Riley’s yucca work but often flies from plant to plant. I tilization of Yucca (though he did not work in his book, “The Effects of Cross and Self have never seen her gather the pollen, out the history which Prof. Riley has done Fertilisation in the Vegetable Kingdom;” and but have watched her thus go from so well)…” (Hulst 1887, p. 236). Regarding soon after its publication, Meehan sent Dar- flower to flower and from plant to this, Riley remarked: “Whatever may have win a letter calling into question the signifi- plant during a single evening and with led Mr. Hulst to make this assertion, it is cance of Riley’s findings. Meehan wrote that one and the same load.24 Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 simply untrue….” Riley acknowledged that Gray had admitted in a letter to him that In the same letter, Riley voiced a harsh it was quite likely he might never have stud- “there is far more self fertilization among assessment of Meehan’s scientific prowess: ied the yucca moth had Engelmann not called flowers than he [Gray] had supposed.” His trouble is that he has not been so it to his attention, but he correctly asserted Meehan added that although only T. trained that he can appreciate a truth that Engelmann had “made no observation yuccasella can fertilize the yucca, “as you are whether it conflict with his own whatever upon insect pollination.” Riley con- no doubt aware, the Pronuba [Tegeticula] opinions or not. There is a bias in most tinued: fertilizes the flower with its own pollen,— everything he writes or says, and he is The discovery that Pronuba and it seems to me a great mystery why the especially fond of controverting [Tegeticula] was the agent was my own, plant should not be arranged to use any it- generally-accepted doctrine, upon as were all the subsequent discoveries self, and not be necessitated to have insect his own observations—oft-times in reference to the insect made that aid in the use of its own pollen.”20 insufficient and even inaccurate. He is, year; but they were always Subsequently, when Riley sent Darwin a withal, unfair, not to say, untruthful. communicated to him, and often copy of his 1881 AAAS publication, he re- In exasperated tones, Riley recounted at shared with and witnessed by ceived the following response from Darwin:21 length what had transpired between him and him.…Dr. Engelmann was, during my I must write half a dozen lines to say Meehan. Riley had visited Meehan at his in- residence in St. Louis, at once my how much interested I have been by vitation during the summer of 1881, when friend, companion, and master in your “Further Notes” on Pronuba Y. glauca was finishing flowering and Y. natural-history matters, and I have too [Tegeticula], which you were so kind filamentosa was about to commence doing much reverence for his memory to as to send me.—I had read the various so. Riley observed numerous P. decipiens allow to pass unchallenged what he criticisms, & though I did not know ovipositing into the stems of Y. filamentosa. himself would repudiate were he still what answer could be made yet I felt Riley also had collected several hundred among us. (Riley 1888, pp. 153) full confidence in your result, & now I moths, every one of which he determined to With the remark that he had “already see I was right.—What an inaccurate be P. decipiens, as he subsequently informed devoted more time to Mr. Hulst’s opinions man Mr. Meehan is! His Epitaph Meehan. To Riley’s surprise, that August, than they justify,” Riley recapitulated his ought to be “He retarded natural Meehan read a paper in Cincinnati in which denouncement of Hulst’s assertions. He con- science in the U. States as much as any he reported that he had collected from a cluded, one man advanced it.” …If you make single Y. glauca flower 17 moths, 4 of which I await with interest and curiosity any any further observation on Pronuba were Prodoxus, the remainder being new discoveries in this connection, [Tegeticula]—it would I think be well Tegeticula. Because Y. glauca were not fertil- but, so far as present knowledge worth while for you to observe ized, Meehan inferred that Tegeticula was in- justifies anticipation, I should expect, whether the moth can or does capable of pollination. When Riley asked where neither Pronuba [Tegeticula] occasionally bring pollen from one who had identified the moths, he was in- nor Pronuba [Tegeticula]-like insect plant to the stigma of a distinct one formed that Meehan had sent them to Hagen exists, to find the plant modified to for I have shown that the Cross- the day after Riley’s visit. A patently annoyed more readily permit self-fertilization fertilisation of the flowers on the same Riley continued, sooner than to find Apis mellifica the [Meehan] made no mention whatever pollinating agent, the opinion…of of my visit or my determinations Mr. Hulst, to the contrary 19Darwin to Hooker, 7 April 1874 (Cambridge notwithstanding. (Riley 1888, p. 154) University Library, classmark DAR 95: 321). In a letter to C. V. Riley, Hermann Müller echoed Darwin, 22Riley to Darwin, 18 Dec. 1881. (Cambridge calling it “the most wonderful instance of mutual University Library, classmark DAR 176: 158) Darwin: “It is the most wonderful case adaptation” yet detected. (Private letter to C. V. Riley, of fertilisation” cited in [Riley 1881, p. 623, fn. 4]) On 7 April 1874, Darwin wrote to J. D. 23Pellmyr et al. (1997) state that Riley erred in his assertion that yucca moths do not perform Hooker, the celebrated botanist and one of 20Meehan to Darwin, 1 July 1877. (Cambridge geitonogamous pollinations and provide evidence to his closest friends, about the yucca moth– University Library, classmark DAR 171: 112) the contrary. yucca plant relationship as elucidated by Riley, stating: “It is the most wonderful case 21Darwin to Riley, 28 Sept. 1881. (Cambridge 24Trelease corroborated this finding (letter from of fertilisation ever published.”19 By this University Library, classmark DAR 147: 303) Trelease to Riley, quoted in Riley 1892a, p. 125).

42 AMERICAN ENTOMOLOGIST • Spring 2004 [emphasis Riley’s]…[Hagen] knows Final Years: Riley’s Work with Trelease In his final years, Riley worked closely little outside of Neuroptera and only and Others with botanist William Trelease, first appoin- the year before had made a most Riley maintained a steadfast interest in the tee to the George Engelmann Professorship unpardonable blunder in pronouncing complex of moths associated with the genus of the Henry Shaw School of Botany, Wash- certain moths which he had bred from Yucca through the last years of his life. Extant ington University, St. Louis, and first direc- Yucca stems to be Pronuba [Tegeticula] letters25 indicate that in February 1893, Riley tor of the Missouri Botanical Garden, yuccasella where afterward he wrote to J. T. Mason (Houston, Texas, Land founded by Shaw (White 1902, Rodgers confessed they were Prodoxus, and one & Trust Co.) expressing his keen interest in 1944). Trelease (1886) corroborated Riley’s would suppose that a fair man seeking obtaining a Tegeticula species that he felt cer- earlier findings on yucca moth oviposition only truth would have at least put my tain must be associated with Y. filifera, a large and pollination, calling it “a case without own determinations, in relation to tree yucca of northeastern Mexico; Riley had parallel”, and at his urging, Riley (1892a) genera of my own creation, along side evidence of the moth’s existence from seed compiled a comprehensive review of his 20 of Hagen’s. pod samples. A few months later, Riley wrote years of yucca moth studies. Riley noted that Hagen had determined Mason to inform him that the plant specimen Trelease (1892) also performed morpho- the moths to be males, adding that “males he had sent Riley was most likely Y. logical studies of several yucca species, and are not so easily distinguished as the females guatemalensis [now Y. elephantipes] and that detailed his pollination and oviposition stud- Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 and Hagen may again have blundered; but the associated moth was a new species, which ies of T. maculata on Y. whipplei and even if he was correct the explanation is Riley named Prodoxus intricatus (Riley Tegeticula synthetica (Riley) on Yucca simple.” Riley continued, stating that 1893). Riley added, brevifolia (commonly called the Joshua tree) Tegeticula males often emerge before the fe- I am quite confident that further (Trelease 1893). Riley (1892a, 1893) males and that, as Y. filamentosa had not yet intelligent research will give us an quoted extensively from these studies, in- bloomed, the males likely took refuge in the interesting form of Pronuba cluding Trelease’s unpublished findings. In few remaining Y. glauca flowers. He added, [Tegeticula] in this Yucca guatemalensis his research, Trelease was assisted by his But nothing is more certain, from a [elephantipes] and if you have a chance wife, Julia Johnson Trelease, who made be- series of experiments and observations of studying Y. filifera you will havioral observations of the moths and ren- which I made this past summer, than undoubtedly secure a number of dered illustrations of pollination and ovi- that Prodoxus female oviposits in the interesting species of the family, of both position.26 Trelease also collected several stem and that her race is run essentially genera, Pronuba [Tegeticula] and Prodoxus species (P. coloradensis Riley, P. by the time the plant begins to bloom, Prodoxus. The Pronuba [Tegeticula] reticulatus [now Greya reticulata (Riley); see for she can only successfully oviposit associated with filifera must be a large Davis et al. 1992], P. cinereus, P. aenescens, in the tender stem and perishes in the and interesting species and I am quite T. intermedia) from various yuccas and sent act when attempted after the flowers sure will prove different from any of them to Riley, who detailed their morphol- begin to open and the stem gets hard; the three so far characterised [sic]. ogy (Riley 1893). further that she is absolutely incapable Recently, Parategeticula elephantipella of pollinizing and never attempts it. Pellmyr & Balcázar-Lara was described and 26William Trelease Papers, #2560, Division of Rare Approximately six months after Riley appears to be the exclusive pollinator of Y. and Manuscript Collections, Cornell University penned this letter, Darwin died on 19 April elephantipes (Pellmyr and Balcázar-Lara Library. 1882, and one month later, the Biological 2001); information on Y. filifera pollination Society of Washington, D.C., held a memo- remains incomplete (Olle. Pellmyr, personal rial meeting in his honor that was attended communication). by an estimated 700 people. Riley and sev- Riley collaborated with other profes- eral other prominent members of the Soci- sional scientists in his investigations. He gave ety, including its president, Major John J. B. Smith (1893) Tegeticula specimens to Wesley Powell, delivered addresses. investigate morphological homologies be- In his presentation, Riley (1882) pro- tween their maxillae and those of other in- claimed Darwin’s greatness, enumerating sects. As chief entomologist, USDA Divi- his many original contributions to and in- sion of Entomology, Riley directed one of sights into the entomological world. Riley his field agents, D. W. Coquillett, to observe closed with a heartfelt remembrance of the the behavior of female T. maculata on Y. two occasions (in 1871 and 1875) on whipplei in southern California (Coquillett which he had visited Darwin at his resi- 1893). The flower stalk of this yucca spe- dence in Down: cies can reach spectacular heights (Fig. 11). Going to him as a young entomologist Riley had a particular interest in Y. whipplei with no claim on his favor, he seemed because he thought that certain of its traits to take delight in manifesting might facilitate ordinary pollination, yet he appreciation…an interest in natural knew that T. maculata serves as a pollinator science was an open sesame to his (Riley 1893). Riley also described several generous soul. His consideration, Prodoxus spp. from Y. whipplei and, in re- without aggression, was the secret cent times, Powell (1992) cited Y. whipplei and of the gratitude and respect which its associated prodoxids as one of the two all felt who had the honor to know most complex yucca/yucca moth systems. him, either personally or through correspondence. (Riley 1882, pp. 79– 25Missouri Botanical Garden, William Trelease Fig. 11. Yucca whipplei in bloom. (from Insect 80) professional papers, Box 8, Folders 1 & 2. Life 1893).

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 43 In February 1894, Riley wrote Trelease of a possible joint trip to Mexico; three months later, he wrote that he was clearing out his USDA office in preparation for his replacement, L. O. Howard.27 Soon thereaf- ter, Riley was named Honorary Curator of Insects, U.S. National Museum, and on 14 September 1895, he died suddenly follow- ing a bicycling accident. Interested readers seeking the single best review by Riley on prodoxids and yuccas can do no better than to peruse his paper written for the Third Annual Report of the Missouri Botanical Garden (Riley 1892a).28 This comprehensive work provides exten- sive excerpts from his earlier publications, Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 taxonomic descriptions for Pronuba [Tegeticula] and Prodoxus spp., and some of Riley’s unpublished observations. It also contains 10 plates, each featuring several il- lustrations, including renderings of the ovi- positor of T. yuccasella (Fig. 12), and micro- scopic sections of Y. filamentosa pistils with Tegeticula eggs and larvae in situ (Fig. 13).

Current Research and Closing Remarks Fig. 12. Masterly renderings from Riley (1892a) of T. yuccasella ovipositor: (A, c) file-like After Riley had worked for several years surface of (b), the ovipositor base; (h) extended oviduct; (B) partial enlargement of (A); (C) on various yuccas and their associated moths, ventral tip of abdomen with (k) muscular attachments. Also shown are eggs from the yucca pistil he stated that there was “little doubt” that (m) and the mature ovary of the moth (o), the developing embryo (n), and the male genital other species of Pronuba [Tegeticula] and claspers (r, s). Prodoxus would be discovered (Riley 1880a, p. 145). A dozen years later, he recognized that there was still “much yet to learn of the (1999) reported that T. yuccasella comprises maxillary tentacles needed for pollination pollination of other species of Yucca”, and at least 13 species, of which 2, T. intermedia (Pellmyr 1999, Pellmyr and Krenn 2002). he predicted that “all the [yucca] species (Riley) and T. corruptrix Pellmyr, are (Because he viewed the female’s tentacles as which are sufficiently distinctive in charac- “cheater yucca moths,” that is, moths that an absolute requirement for placement in ters and in range, may be expected to have coexist with yucca pollinators and oviposit Tegeticula, Riley misidentified T. intermedia special Pronubas [Tegeticula] associated with into the fruit, but do not engage in yucca as a bogus yucca moth, naming it Prodoxus them” (Riley 1892b, pp. 95–96). pollination. Females of these species lack the intermedius.) Since then, knowledge of the complex of prodoxids associated with yuccas has in- creased significantly and Riley’s predictions have been validated. In his revision, Davis (1967) described two new Prodoxus species and Parategeticula pollenifera, a yucca polli- nator. Currently there are 78 described spe- cies of Prodoxidae; of these, 11 are Prodoxus and 4 are Parategeticula and, until recently, 3 were Tegeticula species: T. synthetica (Riley), T. maculata (Riley), and T. yuccasella (Riley) (Pellmyr 2003). However, T. synthetica is believed to contain two species and T. maculata may comprise several (Pellmyr 2003). In his recent systematic revision of the yuccasella complex north of Mexico, Pellmyr

27William Trelease Papers, #2560, Division of Rare and Manuscript Collections, Cornell University Library. Fig. 13. Microscopic views of Y. filamentosa and T. yuccasella (from Riley 1892a): (a) longitudinal section through pistil, (b) oviposition punctures, (c) elongate eggs in situ, (d, e) larvae in situ. 28For a condensed version of this publication, see Also shown is a seed (f) at 13 days after oviposition, with a young larva visible at the funicular Riley (1892b). base.

44 AMERICAN ENTOMOLOGIST • Spring 2004 Riley demonstrated remarkable pre- work within which to pursue research of both 23: 427–446 (Part 2); 23: 517–535 (Part 3). science as he considered the phylogeny and sorts. Great naturalists like Riley recognized Boll, J. 1876. Ueber die Befruchtung der evolutionary biology of yucca-associated this and strove to use valid scientific ap- nordamerikanischen Yucca-Arten. Entomol. moths: proaches to test their hypotheses, but at times Z. 37:401–405. Who, studying these two species [T. they labored in the midst of colleagues less Bowler, P. J. 1989. Evolution: the history of an yuccasella and P. decipiens] in all their gifted and far less rigorous in their empiri- idea. University of California Press, Berke- ley. characters and bearing, can fail to cism. Riley’s powers of observation, clarity Bowler, P. J. 1990. Charles Darwin: the man and conclude that, notwithstanding the of reasoning, and abundant self-confidence his influence. Basil Blackwell, Cambridge, essential differences that distinguish served him well in rebutting his relentless crit- MA. them not only specifically but ics. With the writings of Darwin and Gray Chambers, V. T. 1875. Tineina from Texas. Can. generically, they are derivations from laying the theoretical groundwork, and the Entomol. 7: 7–12. one and the same ancestral collaborative efforts of Engelmann, Trelease, Chambers, V. T. 1877. The Tineina of Colorado. form?…Which of the two insects is and others providing the needed botanical Bull. U.S. Geol. Geogr. Survey Terr. 3:121, oldest in time, or whether the expertise, Riley synthesized a corpus of 147–149. divergence from some archetypal form knowledge on a fascinating case of coevolu- Coquillett, D. W. 1893. On the pollination of has been simultaneous, are matters of tion. The majority of his findings have with- Yucca whipplei in California. Insect Life 5: Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 opinion which those interested in stood the test of time for more than a cen- 311–314. evolution will decide for themselves tury, and yuccas and yucca moths continue Darwin, C. 1862. On the various contrivances by which British and foreign orchids are one way or the other, or according as to be a vibrant area of research, perhaps the fertilised by insects, and on the good effects knowledge increases. (Riley 1880a, pp. greatest testament to Riley’s labors. of intercrossing. J. Murray, London. 144–145) Darwin, C. 1876. The effects of cross and self According to Pellmyr’s recent review Acknowledgements fertilisation in the vegetable kingdom. (Re- (2003), prodoxids colonized yuccas about We are indebted to Olle Pellmyr, Depart- printed, 1902). D. Appleton and Co., New 41.7 million years ago. Soon thereafter, the ment of Biological Sciences, University of York. three genera (Tegeticula, Parategeticula, and Idaho, for expertise provided on yucca moth Darwin, F., and A. C. Seward [Eds.]. 1903. More Prodoxus) underwent rapid diversification. taxonomy, systematics, and evolutionary letters of Charles Darwin, vol. 2. J. Murray, Together, these genera exhibit a species di- biology. We thank Shelley Innes, Darwin London. versity greater than 20 times that of their Correspondence Project, Cambridge Univer- Davis, D. R. 1967. A revision of the moths of sister group, Mesepiola, which are sity Library, for frequent and generous as- the subfamily Prodoxinae (Lepidoptera: nonpollinating seed parasites (Pellmyr and sistance; and Rick Weinzierl, University of Incurvariidae). Bull. U.S. Natl. Mus. 255: 1– Krenn 2002). Illinois, for procuring copies of some rare 170. Davis, D. R., O. Pellmyr, and J. N. Thompson. In his review of yuccas and yucca moths, journal articles. We also thank Marina 1992. Biology and systematics of Greya Busck Powell (1992) argued that “insect biologists Meixner, Institut für Bienenkunde, and Tetragma, new genus (Lepidoptera: and ecologists failed to recognize the highly Oberursel, Germany, for German translation, Prodoxidae). Smithson. Contrib. Zool. 524. complex nature of this coevolutionary rela- and Edward H. Smith, Professor Emeritus, Dupree, A. H. 1959. Asa Gray: American bota- tionship until recently,” stating that little re- Cornell University, for information pertain- nist, friend of Darwin. Johns Hopkins Uni- search was done in the 70 years following ing to the Riley–Trelease correspondence and versity Press, Baltimore. Riley’s work. He listed several areas ripe for continuing collegiality. We gratefully acknowl- Engelmann, G. 1872. The flower of Yucca and further investigation, and the recent treat- edge the Syndics of Cambridge University its fertilization. Bull. Torrey Bot. Club. 3: 33. ment of this topic by Pellmyr (2003) pro- Library, for quotation of letters in the Dar- Engelmann, G. 1873. Notes on the genus Yucca. vides an informed measure of the advances win correspondence; the Missouri Botanical Trans. Acad. Sci. St. Louis 3: 17–54. that have been made in the decade since Garden, for citation of Riley letters and re- Engelmann, G. 1875. Notes on the genus Yucca, Powell’s review, including ideas relevant to production of unpublished sketches by En- no. 2. Trans. Acad. Sci. St. Louis 3: 210–214. the evolution of obligate mutualism. gelmann; and Cornell University Library, Di- Faegri, K., and L. van der Pijl. 1971. The prin- ciples of pollination ecology, 2nd rev. ed. Speculation about the possibility of non- vision of Rare and Manuscript Collections, Pergamon Press, Oxford, U.K. yucca moth pollinators of yuccas continued for reference to letters in the William Trelease Ghiselin, M. T. 1969. The triumph of the Dar- to be raised a century after Riley’s death, yet, Collection. Finally, we thank anonymous winian method. University of Chicago Press, according to Pellmyr (2003), the only yucca reviewers for helpful comments on our manu- Chicago. species for which there is even “moderate script. Goldstein, D. 1989. Midwestern naturalists: support” for such came from Trelease Academies of Science in the Mississippi Val- (1893), who performed pollinator exclusion References Cited ley, 1850–1900. Ph.D. dissertation, Yale Uni- experiments on Y. aloifolia. Pellmyr (2003) Althoff, D. M., J. D. Groman, K. A. Segraves, versity, New Haven, CT. argues that carefully executed experiments and O. Pellmyr. 2001. Phylogeographic struc- Gray, A. 1884. George Engelmann. Proc. Am. would settle the recurring question of yucca ture in the bogus yucca moth Prodoxus Acad. Sci. 19: 516–522. copollinators. quinquepunctellus (Prodoxidae): Compari- Gray, A., and W. Trelease [Eds.]. 1887. The bo- Our review of the first two decades of sons with coexisting pollinator yucca moths. tanical works of the late George Engelmann, yucca moth research provides a window on Mol. Phylogenet. Evol. 21: 117–127. collected for Henry Shaw, Esq. John Wilson Anonymous. 1868–1877. J. Proc. St. Louis Acad. and Son, University Press, Cambridge, MA. mid- to late 19th-century entomology, when Sci. 3: i–cclxxv. Hagen H. 1880. A mystery in reference to the discipline broadened from a purely de- Anonymous. 1872. The American Association. Pronuba yuccasella. Can. Entomol. 12: 128– scriptive enterprise (taxonomic and life his- Can. Entomol. 4: 181–183. 129. tory studies) to include research aimed at the Anonymous. 1880. Entomological papers read Hendrickson, W. B. 1966. St. Louis Academy of practical application of scientific knowledge. before the A.A.A.S. Am. Entomol. n.s. 1: 223. Science: the early years. Mo. Hist. Rev. 61: At the same time, Darwin’s theory of evolu- Bek, E. G. 1929. George Engelmann, man of 83–95. tion emerged, providing a conceptual frame- science. Mo. Hist. Rev. 23: 167–206 (Part 1); Hendrickson, W. B. 1972. An Illinois scientist

AMERICAN ENTOMOLOGIST • Volume 50, Number 1 45 defends Darwinism: a case study in the dif- Acad. Sci. 3: 323–344. (reprinted in Eighth cess. University of Chicago Press, Chicago. fusion of scientific theory. Trans. Ill. Acad. Annual Report of the Missouri State Ento- Trelease, W. 1886. The nectary of yucca. Bull. Sci. 65: 25–29. mologist, pp. 169–182) Torrey Bot. Club 13: 135–141. Hulst, G. D. 1886. Society news. Entomol. Am. Riley, C. V. 1877. Further remarks on Pronuba Trelease, W. 1892. Notes and observations. 1. 2: 184. yuccasella, and on the pollination of yucca. Detail illustrations of yucca. Third Annual Hulst, G. D. 1887. Remarks upon Prof. Riley’s Trans. Acad. Sci. St. Louis. 3: 568–573. Report, Missouri Botanical Garden, pp. 159– strictures. Entomol. Am. 2: 236–238. Riley, C. V. 1880a. The true and the bogus yucca 166. Long, M. 1995. George Engelmann and the lure moth; with remarks on the pollination of Trelease, W. 1893. Further studies of yuccas and of frontier science. Mo. Hist. Rev. 89: 251– yucca. Am. Entomol. (n.s.) 1: 141–145. their pollination. Fourth Annual Report, 268. Riley, C. V. 1880b. On a new Tineid genus allied Missouri Botanical Garden, pp. 181–226. Mayr, E. 1982. The growth of biological thought. to Pronuba, Riley. Am. Entomol. (n.s.) 1: White, C. A. 1902. Memoir of George Engel- Belknap Press of Harvard University, Cam- 155–156. mann, 1809–1884. Natl. Acad. Sci. (U.S.) bridge, MA. Riley, C. V. 1880c. “A mystery in reference to Biog. Mem. 4: 3–21. Mayr, E. 1991. One long argument. Harvard Pronuba yuccasella.” Am. Entomol. (n.s.) 1: University Press, Cambridge, MA. 293. Carol A. Sheppard received her M.S. and Moore, J. A. 1993. Science as a way of know- Riley, C. V. 1881. Further notes on the pollina- Ph.D. degrees in Entomology from the Uni- ing. Harvard University Press, Cambridge, tion of yucca and on Pronuba and Prodoxus. versity of Illinois at Urbana–Champaign, Downloaded from https://academic.oup.com/ae/article/50/1/32/2474745 by guest on 27 September 2021 MA. Proc. Am. Assoc. Adv. Sci. 29: 617–639. where a course on the history of biology Pellmyr, O., L. K. Massey, J. L. Hamrick, and M. Riley, C. V. 1882. Darwin’s work in entomol- sparked her long-standing interest in histori- A. Feist. 1997. Genetic consequences of spe- ogy. Proc. Biol. Soc. Wash. 1: 70–80. (re- cal entomology. She is a faculty member at cialization: yucca moth behavior and self- printed 1883; Smithson. Misc. Collect. 499) Washington State University (WSU), Depart- pollination in yuccas. Oecologia 109: Riley, C. V. 1883. Observations on the fertiliza- 273–278. tion of yucca and on structural and ana- ment of Entomology, FSHN Rm. 160, P.O. Pellmyr, O. 1999. A systematic revision of the tomical peculiarities in Pronuba and Box 646382, Pullman, WA, 99164-6382 yucca moths in the Tegeticula yuccasella com- Prodoxus. Proc. Am. Assoc. Adv. Sci. 31: 467– (e-mail: [email protected]) and a mem- plex north of Mexico. Syst. Entomol. 24: 243– 468. ber of the WSU Honors College Faculty. 271. Riley, C. V. 1887. Mr. Hulst’s observations on Richard A. Oliver received his B.S. degree in Pellmyr, O., and M. Balcázar-Lara. 2001. Sys- Pronuba yuccasella. Entomol. Am. 2: 233– Zoology from WSU, where he also was an tematics of the yucca moth genus 236. Honors College student. He conducted some Parategeticula (Lepidoptera: Prodoxidae), Riley, C.V. 1888. Notes on Pronuba and Yucca of this research on yuccas and yucca moths with description of three Mexican species. pollination.. Proc. Entomol. Soc. Wash. as part of a special topics course in entomol- Ann. Entomol. Soc. Am. 93: 432–439. 1:150-154. (reprinted (1889) in Insect Life ogy at WSU. Currently, he is enjoying work- Pellmyr, O., and H. W. Krenn. 2002. Origin of a 1:367-72) ing with animals at the Hogle Zoo in Salt complex key innovation in an obligate in- Riley, C. V. 1892a. The yucca moth and yucca Lake City. sect–plant mutualism Proc. Natl. Acad. Sci. pollination. Third Annual Report, Missouri U.S.A. 99: 5498–5502. Botanical Garden, pp. 99–158. (reprinted Pellmyr, O. 2003. Yuccas, yucca moths, and co- 1892, Insect Life 4: 358–378) evolution: a review. Ann. Mo. Bot. Gard. 90: Riley, C. V. 1892b. Some interrelations of plants 35–55. and insects. Proc. Biol. Soc. Wash 7: 81–104. Powell, J. A. 1992. Interrelationships of yuccas Riley, C. V. 1893. Further notes on yucca insects and yucca moths. TREE 7: 10–15. and yucca pollination. Proc. Biol. Soc. Wash. Price, P. W. 1996. Biological evolution. Sanders 8: 41–53. (reprinted 1893, Insect Life 5: 300– College Publishing, Fort Worth, TX. 310) Proctor, M., P. Yeo, and A. Lack. 1996. The Rodgers, A. D., III. 1944. American Botany, natural history of pollination. HarperCollins, 1873–1892. Princeton University Press, London. Princeton, NJ. (reprinted 1968, Hafner Pub- Riley, C. V. 1873a. On a new genus in the lepi- lishing, New York) dopterous family Tineidae, with remarks on Ruse, M. 1982. Darwinism defended. Addison- the fertilization of yucca. Trans. Acad. Sci. Wesley, London. St. Louis. 3: 55–64 (reprinted in Fifth An- Sheppard, C. A., and R. A. Weinzierl. 2002. En- nual Report of the Missouri State Entomolo- tomological lucubrations: The 19th century gist, pp. 150–160). spirited conflict surrounding the natural his- Riley, C. V. 1873b. Supplementary notes on tory of the armyworm, Pseudaletia unipuncta Pronuba yuccasella. Trans. Acad. Sci. St. (Haworth). Am. Entomol. 48: 108–117. Louis. 3: 178–180. Smith, E. H. 1992. The grape phylloxera: a cel- Riley, C. V. 1873c. On a new genus in the lepi- ebration of its own. Am. Entomol. 38: 212– dopterous family Tineidae: with remarks on 221. the fertilization of yucca. Fifth Annual Re- Smith, E. H., and J. R. Smith. 1996. Charles port of the Missouri State Entomologist, pp. Valentine Riley: the making of the man and 150–160. his achievements. Am. Entomol. 42: 228– Riley, C. V. 1873d. On the oviposition of the 238. yucca moth. Am. Nat. 7: 619–623. (extracts Smith, J. B. 1893. The maxillary tentacles of reprinted in Trans. Acad. Sci. St. Louis 3: Pronuba. Insect Life 5: 161–163. 208–210) Sorensen, W. C. 1995. Brethren of the net: Riley, C. V. 1874. The yucca moth. Sixth An- American Entomology, 1840–1880. Univer- nual Report of the Missouri State Entomolo- sity of Alabama Press, Tuscaloosa. gist, pp. 131–135. Swartz, D. 1971. Collegiate dictionary of botany. Riley, C. V. 1876. Notes on the yucca borer, Ronald Press Co., New York. Megathymus yuccae (Walk.). Trans. St. Louis Thompson, J. N. 1994. The coevolutionary pro-

46 AMERICAN ENTOMOLOGIST • Spring 2004