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Rapid Evolution of a Geographic Cline in Size in an Introduced R EPORTS nificant increase in the probability of spawning ob- 30. Two other cases exist in which the traits that form the 32. Supported by a Natural Sciences and Engineering served for populations of females with males of the proximate basis of reproductive isolation have known Research Council of Canada (NSERC) fellowship to other ecomorph from different lakes versus males of adaptive significance. These are beak and body size in H.D.R., NSERC research grants to D.S., and a National the other ecomorph from the same lake was significant Darwin’s finches in the Gala«pagos Islands [P. T. Boag and Science FoundationÐNATO (USA) fellowship to in the absence of the phylogenetic correction (paired t P. R. Grant, Science 214, 82 (1981); L. M. Ratcliffe and J.W.B. E. Taylor provided unpublished microsatellite ϭ ϭ test, t5 3.37, P 0.020) (Fig. 2, comparison C). P. R. Grant, Anim. Behav. 31, 1139 (1983); T. D. Price, DNA data. A. Agrawal, S. Morgan, and K. Rozalska 28. No significant difference in microsatellite or mtDNA P. R. Grant, H. L. Gibbs, P. T. Boag, Nature 309, 787 helped conduct mating trials. T. Day and M. Linde«n divergence is detected between pairs of populations (1984)] and copper tolerance in Mimulus [M. R. MacNair provided technical support. S. Otto, M. Whitlock, (conspecific pairs excluded) from the same versus a and P. Christie, Heredity 50, 295 (1983); P. Christie and three reviewers, and the rest of the Schluter Otto different environment [microsatellite, analysis of M. R. MacNair, J. Hered. 75, 510 (1984)]. Whitlock group at the University of British Columbia variance (ANOVA), F ϭ 0.22, P ϭ 0.65; mtDNA, 31. W. J. Rowland, Behav. Ecol. Sociobiol. 24, 433 (1989); ϭ 1,10 ϭ provided comments on the manuscript. ANOVA, F1,10 0.76, P 0.40]. W. J. Rowland, Anim. Behav. 38, 112 (1989); M. 29. D. J. Funk, Evolution 52, 1744 (1998); J. S. McKinnon, Borland, thesis (University of British Columbia, Van- S. Mori, D. Schluter, unpublished data. couver, 1986). 18 October 1999; accepted 23 November 1999 per sex per population) and measured wing Rapid Evolution of a Geographic length as the combined length of the basal and distal segments of vein IV (15). Cline in Size in an Introduced Wing length of native European females increased significantly with latitude (Fig. 1A), as in previous studies (14–16). Wing length of Fly introduced North American females also in- Raymond B. Huey,1*† George W. Gilchrist,1*‡ creased significantly with latitude (Fig. 1A) Margen L. Carlson,1 David Berrigan,1§ Luõ«s Serra2 (19), and the slope of the regression was not significantly different from that of European The introduction and rapid spread of Drosophila subobscura in the New World females (comparison of slopes, P ϭ 0.834). two decades ago provide an opportunity to determine the predictability and Wing length of males also increased signifi- rate of evolution of a geographic cline. In ancestral Old World populations, wing cantly with latitude in both native and intro- length increases clinally with latitude. In North American populations, no wing duced populations (Fig. 1A), but the slope for length cline was detected one decade after the introduction. After two decades, North American males was less steep than that however, a cline has evolved and largely converged on the ancestral cline. The for European males (P Ͻ 0.001) or that for rate of morphological evolution on a continental scale is very fast, relative even North American females (P Ͻ 0.001) (20). to rates measured within local populations. Nevertheless, different wing sec- The striking convergence of clinal varia- tions dominate the New versus Old World clines. Thus, the evolution of geo- tion in wing size (Fig. 1A) has been achieved graphic variation in wing length has been predictable, but the means by which through analogous, not homologous, changes the cline is achieved is contingent. in the relative lengths of different parts of the wing (Fig. 1B). The increase in wing length How fast can evolution occur in nature (1, 2)? introduced populations quickly evolved clines with latitude in Europe is caused by a relative Are evolutionary trajectories predictable or that converge on clines among ancestral popu- lengthening of the basal portion of vein IV, idiosyncratic (3, 4)? Answers to these two lations (12, 13). A candidate species is Drosoph- whereas the increase in NA is caused by a questions are fundamental to attempts to fore- ila subobscura. This fly is native to the Old relative lengthening of the distal portion of cast evolutionary responses to natural or an- World (12, 13), where it exhibits a clinal in- vein IV (21). These differences in slopes thropogenic perturbations (5). Rates of evo- crease in body size with latitude (14–16). It was between continents are significant for both lution are usually estimated by monitoring accidentally introduced into western North and females (Fig. 1B, P Ͻ 0.001) and males (22) phenotypic shifts within local populations South America about two decades ago (17) and (P Ͻ 0.001). over time (2, 4, 6–8) and are rarely evaluated spread rapidly in temperate regions (12, 13). No How fast can evolution occur on a conti- on a continental scale (9). The predictability latitudinal cline in wing size was evident on nental scale? Although no cline in wing of evolution is evaluated by determining either continent about one decade after the in- length was evident in samples collected about whether replicate populations show conver- troduction (15, 16). Here we reexamine the one decade after the introduction in NA (15), gent responses (4, 10). North American populations to determine a cline is conspicuous after two decades (Fig. Recently introduced species that quickly col- whether a cline has evolved after two decades 1A). Thus, this cline evolved in only one to onize large areas offer special opportunities to and whether it has converged on the Old World two decades (23). The rate of size divergence address both the speed and predictability of cline. on a continental scale for D. subobscura fe- evolution on a geographic scale (11): Rapid and We collected introduced flies from 11 lo- males is rapid [ϳ1700 darwins, ϳ0.22 hal- predictable evolution would be demonstrated if calities in western North America (NA) danes (2, 24)] and is faster than almost all (April and May 1997) and native flies from previously measured rates in nature, even 1Department of Zoology, University of Washington, 10 localities in continental Europe (May within local populations (2, 24). For morpho- Box 351800, Seattle, WA 98195Ð1800, USA. 2Depar- 1998) (18). We established stocks for each logical traits in natural populations, only rates tament de Gene`tica, Universitat de Barcelona, 08071 (10 per sex from each of 15 to 25 isofemale of Gala´pagos finches during the 1978 drought Barcelona, Spain. lines) and maintained them (20°C, low den- are faster [0.37 to 0.71 haldanes (2, 6)]. *These authors contributed equally to this work. sity) for five to six generations in a common Is evolution predictable or historically †To whom correspondence should be addressed. E- mail: [email protected] garden to ensure that any observed differenc- contingent (3, 4)? Convergent latitudinal ‡Present address: Department of Biology, Clarkson es between populations would be genetic. We clines in wing length of North American D. University, Box 5805, Potsdam, NY 13699Ð5805, then set up four vials per population (50 eggs subobscura (especially of females) and an- USA. per vial) and reared flies to adulthood. Short- cestral European D. subobscura (Fig. 1A), as §Present address: National Cancer Institute, Division of Cancer Prevention and Control, Bethesda, MD ly after the flies eclosed, we mounted the left well as those of many other drosophilids (15, 20852, USA. wing from flies selected haphazardly (ϳ20 25), demonstrate that the evolution of wing 308 14 JANUARY 2000 VOL 287 SCIENCE www.sciencemag.org R EPORTS Fig. 1. The latitudinal cline in and evolutionary responses can be compared directly wing size of introduced North against the Old World evolutionary baseline. American D. subobscura is con- 18. European localities—Spain: Malaga (36.5¡N), Valen- verging on that for native [Euro- cia (39.3¡N), and Barcelona (41.3¡N); France: Mont- pellier (43.4¡N), Lyon (45.3¡N), Dijon (47.2¡N), Gif- pean (EU)] flies. (A) Female wing sur-Yvette (48.4¡N), and Lille (50.4¡N); Leiden, Neth- length (logarithmically trans- erlands (52.1¡N); and Århus, Denmark (56.1¡N). formed, mean slope Ϯ SE) of North American localities—California: Atascadero introduced North American flies (35.5¡N), Gilroy (37.0¡N), Davis (38.6¡N), Redding increases with latitude (b ϭ (40.6¡N), and Eureka (40.8¡N); Oregon: Medford 0.0020 Ϯ 0.0004, P Ͻ 0.001, (42.3¡N) and Salem (44.9¡N); Washington: Centralia R2 ϭ 0.1393) in a pattern virtu- (46.7¡N) and Bellingham (48.7¡N); and British Co- ally identical to that of European lumbia: Peachland (49.8¡N) and Port Hardy (50.7¡N). ϭ Ϯ Ͻ 19. Because a directional hypothesis (size increases with flies (b 0.0018 0.0004, P latitude) is at risk, we used one-tailed tests for eval- 2 ϭ 0.001, R 0.0749). Male wing uating the significance of clines. size also increases positively 20. In Europe, the slope of the size increase does not differ with latitude in NA (b ϭ statistically for males and females (P ϭ 0.130), whereas 0.0007 Ϯ 0.0004, P ϭ 0.0265, the North American sexes are significantly different R2 ϭ 0.0191) and Europe (b ϭ (P ϭ 0.001).
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