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Protein Comparisons (Drosophila/Scptomyza/Larval Hemolymph Protein/Microcomplement Fixation/Hawaiian Geology) STEPHEN M

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Protein Comparisons (Drosophila/Scptomyza/Larval Hemolymph Protein/Microcomplement Fixation/Hawaiian Geology) STEPHEN M Proc. Nadl. Acad. Sci. USA Vol. 82, pp. 4753-4757, July 1985 Evolution Ancient origin for Hawaiian Drosophilinae inferred from protein comparisons (Drosophila/Scptomyza/larval hemolymph protein/microcomplement fixation/Hawaiian geology) STEPHEN M. BEVERLEY*t AND ALLAN C. WILSON* *Department of Biochemistry, University of California, Berkeley, CA 94720; and tDepartment of Pharmacology, Harvard Medical School, Boston, MA 02115 Communicated by Hampton L. Carson, March 25, 1985 ABSTRACT Immunological comparisons of a larval we recently showed that this may apply to LHPs in more than hemolymph protein enabled us to build a tree relating major 30 species of Drosophila and related flies, including two groups of drosophiline flies in Hawail to one another and to lineages of Hawaiian Drosophila (11). The conclusion was continental flies. The tree agrees in topology with that based on that the variance in rate of LHP evolution is low enough to internal anatomy. Relative rate tests suggest that evolution of permit the use of LHP as a tool for estimating times of hemolymph proteins has been about as fast in Hawaii as on divergence (11). continents. Since the absolute rate of evolution of bemolymph This report extends our studies to 18 species of Hawaiian proteins in continental flies is known, one can erect an drosophilines, including members of the genus Scaptomyza. approximate time scale for Hawaiian fly evolution. According Our analysis suggests that rates of LHP evolution are not to this scale, the Hawaiian fly fauna stems from a colonist that accelerated within the Hawaiian drosophilines, supporting landed on the archipelago about 42 million years ago-i.e., the use of LHP as an estimator of divergence times. The before any of the present islands harboring drosophilines divergence times estimated from the LHP distances indicate formed. This date fits with the geological history of the that an ancient origin model is the correct one for the archipelago, which has witnessed the sequential rise and Hawaiian drosophilines. erosion of many islands during the past 70 million years. We discuss the bearing of the molecular time scale on views about METHODS AND MATERIALS rates of organismal evolution in the Hawaiian flies. Fly Strains and LHP Extracts. Of the 21 species examined The Hawaiian archipelago has received extensive study as (Table 1), 3 are continental and 18 are Hawaiian; included are the setting of seemingly rapid biological evolution within representatives of two genera, Drosophila and Scaptomyza. many taxonomic groups (1, 2). Hawaiian members of the Third instar larvae of these species were provided by the subfamily Drosophilinae, for example, comprise more than National Drosophila Species Stock Center (Univ. of Texas, 400 described species representing more than 15% of the Austin) or by Herman Spieth (Univ. of California at Davis). world's drosophilines, yet Hawaii accounts for less than Protein extracts containing monomeric LHP were made from 0.01% of the world land area (3-5). This observation could third instar larvae as described (10). imply that evolution in Hawaii has been extremely fast, ifthis Protein Comparisons. Immunological distances between large group offly species were no older than the oldest island pairs of LHPs were measured by the quantitative Kauai, or about 5-6 million years (Myr) (6). Another pos- microcomplement fixation method with antisera to highly sibility is that the fly fauna is far older (3, 4, 7, 8). Even though purified LHPs. The five antisera used and the way of doing the fossil record of Hawaiian flies is poor, much is known microcomplement fixation tests with LHPs have been de- about the geological history of the archipelago and the scribed (10). All immunological distances were checked phylogenetic relationships of some of these flies. For one qualitatively by the Ouchterlony double-diffusion test (10). subgroup, in particular, it has been possible through intensive Immunological distance (y) between 290 pairs of monomeric cytogenetic, biogeographic, and radiometric dating studies to proteins is correlated (r = 0.9) to the percentage difference in develop an evolutionary time scale; we refer to the picture- amino acid sequence (x) by an equation ofthe formy = Sx (10, winged flies of the planitibia subgroup, which appears to be 24). The average error in measuring an immunological dis- less than 5 Myr old (3, 9). tance between two LHPs (e.g., A and B) with one antiserum Our approach has been to build a temporal framework for (e.g., anti-A) is ±2.6 units (10), and the average deviation the evolution of these flies by using biochemical methods of from perfect reciprocity (i.e., anti-A vs. B compared with estimating approximate times ofdivergence between lineages anti-B vs. A) is 14.2% of the mean distance (10). leading to living species. We use immunological comparisons of a larval hemolymph protein (LHP) found throughout the RESULTS AND DISCUSSION higher diptera to estimate degree of amino acid sequence Immunological Distances. The immunological distances divergence (10, 11), an approach used with success in the observed between the LHPs of the 5 reference species and study of vertebrate proteins and evolution (12). Attesting to those of 16 additional Hawaiian species are presented in the validity of this approach is the fact that the phylogenetic Table 1. The antiserum to Drosophila crucigera LHP sepa- tree constructed from the immunological distances observed rates the 9 species tested within the picture-winged group into among drosophiline LHPs agrees approximately in branching two divisions. Division I has LHPs that are nearly identical order with that based on 60 anatomical traits ofdrosophilines with D. crucigera LHP, the immunological distances from (13, 14). Point mutations are now known to accumulate at this reference species being 4 or less. Included in this division fairly steady rates in the proteins of vertebrates (12, 15) and are LHPs from 7 species representing most of the recognized subgroups within the picture-winged group (5, 8). Division II The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviations: LHP, larval hemolymph protein; Myr, millions of in accordance with 18 U.S.C. §1734 solely to indicate this fact. years. 4753 Downloaded by guest on October 2, 2021 4754 Evolution: Beverley and Wilson Proc. Nad Acad Sd USA 82 (1985) Table 1. Immunological distances within Hawaiian Drosophilinae Table 1 and refs. 10 and 11. This tree (Fig. 1), which is in Immunological distance general agreement with that based on anatomy and behavior (4, 25, 26), depicts two clusters of lineages, one leading from Source of LHP Cru Mim Sca Mul Mel node E to the LHPs of 14 Hawaiian Drosophila species and Genus Drosophila the other leading to the LHPs offour Scaptomyza species and Subgenus Sophophora the subgenus Engiscaptomyza. The remaining two lineages, D. melanogaster (C)* 76 90 80 74 0 leading from node D to continental species of the subgenus Subgenus Drosophila Drosophila and from node C to the subgenus Sophophora D. mulleri (C) 50 59 56 0 78 signify the phylogenetic position occupied by the LHPs of Picture-winged group Drosophila mulleri and Drosophila melanogaster, respec- LHP division I tively, as well as other continental species studied (11). D. crucigera 0 32 53 58 84 The thickest bar in the protein tree is intended to point out D. conspicua -3 NP NP NP NP that nodes D (54.3 + i.9; results represent mean + SEM) and D. odontophallus NPt 34 NP NP NP E (52.9 ± 3.4) are not clearly resolved, possibly because the D. orthofascia -2 NP N? NP NP immunological distance method provides only an approxi- D. picticornis 4 NP NP NP NP mate estimate of the extent of protein divergence. For this D. punalua 1 NP NP NP NP reason, one cannot rule out the possibility that certain D. silvarentis 2 NP NP NP NP continental species-specifically, those belonging to the LHP division II pinicola, immigrans, robusta, and virilis groups and the D. adiastola 34 49 37 49 NP subgenus Hirtodrosophila* (see figure 5 of ref. 11)-are as D. setosimentum 40 53 NP 49 NP closely related to Scaptomyza and Hawaiian Drosophila as Modified-mouthparts group those two groups are to each other. Hence, the possibility D. mimica 17 0 54 52 79 that the Hawaiian archipelago was colonized twice at about D. biseriata NP 25 NP NP NP the same time, once by the ancestor ofScaptomyza and once D. dissita 39 13 75 NP NP by the ancestor ofthe Drosophila, cannot be ruled out. On the D. eurypeza 36 26 80 NP NP grounds of parsimony, as well as Throckmorton's (4) obser- D. hirtitarsus 23 19 58 NP NP vations on the morphological traits of Hawaiian Drosophila Subgenus Engiscaptomyzat and Scaptomyza, the hypothesis of a single colonization D. amplilobus 39 44 25 61 61 event followed by immediate divergence is favored. Genus Scaptomyza Adiastola Subgroup (Division H). The tree analysis shows Subgenus Parascaptomyza that the LHPs of picture-winged flies consist of two S. adusta (C) 42 57 0 57 70 phylogenetically distinct groups: division I (most species) S. elmoi 33 59 24 61 NP and division II (the adiastola subgroup; Fig. 1). Consistent Subgenus Bunostoma with this finding, the mean LHP distance between the S. varifrons 42 71 40 NP 69 division I and the modified-mouthparts groups (node G; 30.2 Subgenus Trogloscaptomyza + 3.5) is significantly smaller than that between division II S. affiniscuspidata 47 55 29 61 NP and the former two groups (node F; 44 ± 4.3). To check on the possibility that the large LHP distance Immunological distances were determined by reaction with anti- sera to LHPs from various species. Cru, anti-D.
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