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Change in a Secondary Sexual Character As Evidence of Incipient Speciation in Drosophila Silvestris* (Evolution/Behavior/Morphology/Sexual Selection/Hawaii) HAMPTON L

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Change in a Secondary Sexual Character As Evidence of Incipient Speciation in Drosophila Silvestris* (Evolution/Behavior/Morphology/Sexual Selection/Hawaii) HAMPTON L Proc. Natl. Acad. Sci. USA Vol. 76, No. 4, pp. 1929-1932, April 1979 Evolution Change in a secondary sexual character as evidence of incipient speciation in Drosophila silvestris* (evolution/behavior/morphology/sexual selection/Hawaii) HAMPTON L. CARSONt AND PETER J. BRYANTt tDepartment of Genetics, University of Hawaii, Honolulu, Hawaii 96822; and *Center for Pathobiology and Department of Developmental and Cell Biology, University of California, Irvine, California 92717 Contributed by Hampton L. Carson, January 29, 1979 ABSTRACT Search for genetic changes that are pivotal in In the present paper we report progress in a renewed search species formation has led to intraspecific studies of Drosophila for cases wherein certain intraspecific populations give evidence silvestris, a giant species found only on the geologically new of incipient speciation (5). This approach unfortunately suffers island of Hawaii. Males bear large, curved, modified bristles or cilia on the dorsal surface of the foreleg tibia and tarsus. In from the same difficulty that confronts the comparison of full males from the south and west parts of the island there are two species: How can crucial genetic changes be identified within rows of cilia separated by a naked area, but in males from the segments of what appears to be an incompletely subdivided north and east there is a mean of between 20 and 30 additional gene pool? How can the change be judged as novel and func- cilia between the two major rows on the tibia. These extra cilia tionally important, and how can its age be determined? are absent in closely related species of this subgroup, including present and cytological findings in the sympatric species D. heteroneura and three species from We here morphological adjacent islands. Males use the foreleg tibiae in vibratory the study of populations of the species Drosophila silvestris movements against the female's abdomen during courtship, so from the island of Hawaii. Hawaiian Drosophila provide an this character difference is likely to be important in the repro- extraordinary opportunity to identify incipient species. Recent ductive biology of the species. Inversion polymorphisms are exuberant speciation has occurred; in less than six million years similar in both northeast and southwest populations; they show about 500 good species of the genus Drosophila have evolved large and strikingly parallel altitudinal shifts in frequency dis- tributions involving the same inversions. Populations from in situ on these extremely isolated oceanic islands (6). Evolution various parts of the island cannot be distinguished by routine has, in most cases, progressed stepwise down the archipelago electrophoresis of soluble proteins encoded by 25 loci. Thus the in a line from the older islands and volcanoes in the northwest "extra cilia" character is superimposed on a more ancient ge- to the newest island (Hawaii) in the southeast. netic background of similarity involving both chromosomal and D. silvestris is confined to the high-altitude mesic forests of electrophoretic polymorphisms. We interpret the extra cilia as Hawaii island, where all of the lava flows are younger than a specific new embellishment of a secondary sexual character brought about by altered sexual selection occurring very recently 700,000 years. Populations of this species, furthermore, extend in one part of the species range. This suggests incipient spe- onto the slopes of the two newest volcanoes (Mauna Loa and ciation. Kilauea), which are currently active volcanically. The leg-bristle character dealt with in this study is particu- Identification of the crucial genetic changes that occur as a larly relevant to the behavior and evolution of Hawaiian Dro- diploid species diverges into two or more new species has sophila. One of the most striking characteristics of this fauna proved to be very difficult (1, 2). Even with the newer molec- is the extraordinary elaboration of male secondary sexual ular and chromosomal methods for assaying genetic variability characters. Wings, antennae, and mouthparts of males show (3), the study of closely related species still suffers from the old bizarre modifications, but the most elaborately changed organ problem: How can the pivotal changes that occurred when the is the male foreleg (7). This is presumably related to the ex- species were diverging be distinguished from changes that tensive use made of the forelegs by the male in stimulating the follow or are irrelevant to the speciation process? female during courtship (8). Much recent research has been devoted to making detailed We will show that a novel foreleg character has evolved in comparisons between full species that are obviously closely certain populations of D. silvestris and that this change has been related and thus presumed to have speciated recently. From superimposed on an underlying similarity of chromosomal and these data, extrapolations to the formative phase of the species' allozymic polymorphisms. We regard it as a character that has history are frequently made (2). A more difficult approach is been newly acquired by sexual selection and that is intimately to attempt to identify incipient speciation within what appears concerned with the reproductive biology of the species. As such, to be, by most criteria, a single species. Such attempts, for ex- it is relevant to the problem of species incipience. ample, led to the original discovery of morphologically cryptic (sibling) species. Recent research has shown, however, that most such species are widely different in reproductive biology, ad- MATERIALS AND METHODS aptations, and physiology. They are frequently disparate ge- Specimens of D. silvestris were captured by using yeasted ba- netically, as indicated by molecular genetic comparisons (4). nana and mushroom baits at 11 sites on the island of Hawaii Indeed, morphological similarity can be a misleading facade; (Fig. 1). Further information on most of these sites is given in sibling species are usually full species and are far from being ref. 9. New sites with altitudes are: 1, Hualalai, 1400 m, North incipient (3). * This paper is no. 6 in the series "Genetic variation in Hawaiian The publication costs of this article were defrayed in part by page Drosophila." Paper no. 5 is ref. 9. The substance of this paper was charge payment. This article must therefore be hereby marked "ad- presented at a symposium, "The Dynamics of Speciation," sponsored vertisement" in accordance with 18 U. S. C. §1734 solely to indicate by the United States-Japan Cooperative Science Program held at this fact. Tokyo, Japan, October 14-18, 1978. 1929 Downloaded by guest on September 28, 2021 1930 Evolution: Carson and Bryant Proc. Natl. Acad. Sci. USA 76 (1979) Table 1. Number of cilia on the tibia of the male foreleg in various populations of D. silvestris from the island of Hawaii (mean and SEM) Site and sample N* Row 5 Middle rows Row6 1. Hualalai U5B 20 22.5 0.55 0.35 ± 0.15 27.8 ± 0.54 2. Pauahi S89; T90 21 21.0 I 0.44 0.38 + 0.15 26.2 ± 0.44 3. Kahuku T96V 20 23.0 + 0.48 0.20 i 0.12 28.3 ± 0.52 4. Pahip'a U27 45t 19.9 + 0.29 0.31 d 0.09 23.0 ± 0.44 5. Waihaka U52; U69 5 21.6 b 0.93 0.60 k 0.25 28.0 + 1.11 6. Kohala T89B 10 30.1 1.11 23.3 1.66 26.5 + 0.64 7. Mawae U18 20 35.2 + 1.02 32.8 + 1.70 30.7 + 0.76 8. Piihonua U57G 23 28.8 0.42 20.2 + 0.84 28.7 + 0.49 9. Olaa U13B 20 34.4 1.01 26.1 ± 1.71 31.3 ± 0.73 10. Volcano T81 18 33.7 0.80 30.4 ± 1.41 31.1 ± 0.64 11. Kilauea T92 17 33.1 1.01 32.5 + 1.45 30.5 ±0.62 * N, number of wild males examined. t F1 males from several wild-caught females. RESULTS The basic pattern of bristle rows on Drosophila legs is evolu- tionarily conservative so that we have been able to use for D. silvestris the same nomenclature used for D. melanogaster (11). Accordingly, the bristles in rows 5 and 6 on the dorsal surface FIG. 1. The island of Hawaii, showing the places from which of the tibia, which are posterodorsal and anterodorsal, respec- samples of D. silvestris came. At sites 1-5 (Kona-Ka'd), males have are very few cilia in the middle rows of the foreleg tibia. At sites 6-11 tively, modified into cilia in males of all the populations of (north and east populations) males have 20-30 extra cilia in this region D. silvestris studied here, as well as in males of many other of the tibia. Hawaiian drosophilids. These cilia are distinguished from bristles in being long, recurved, and unbracted. Table 1 gives cilia counts for various populations of D. sil- Kona District, directly up the mountain from the older site at vestris. In males from the west and south sides of the island 1000 m; 3, Kahuku Ranch, 1220 m, Ka'u District; 5, Waihaka (Kona and Ka'u Districts; sites 1-5, Fig. 1; Table 1) there are Gulch, 1310 m, Ka'u District; 8, Piihonua, 1341 m, South Hilo virtually no cilia on the bare dorsal surface between rows 5 and to as District (formerly referred "Kipuka, 4400 ft"); and 9, 6. This is illustrated in Fig. 2A, in which only a single cilium is Volcano Experiment Station, 1250 m, Puna District. Generally, shown; the largest known number is two. On the other hand, the flies occur in small local populations near their principal host tibiae of males from populations elsewhere on the island (sites plants (lobeliads of the genus Clermontia) in rain forests be- 6-11, Fig.
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