blue whereas the other one is red or yellow Fish Diversity Threatened by (14). Strikingly, the same dichotomy is Eutrophication That Curbs Sexual Selection found among conspecific male color morphs (14) and matches the two absorbance peaks Ole Seehausen,* Jacques J. M. van Alphen, Frans Witte of the retinal pigments (13). If females pre- fer conspicuous over nonconspicuous males Cichlid fish species of Lake Victoria can interbreed without loss of fertility but are sexually (15), individual variation in color vision isolated by mate choice. Mate choice is determined on the basis of coloration, and strong could be responsible for the origin of the assortative mating can quickly lead to sexual isolation of color morphs. Dull fish col- observed dichotomy in male coloration, and oration, few color morphs, and low species diversity are found in areas that have become interspecific variation in color vision could turbid as a result of recent eutrophication. By constraining color vision, turbidity interferes be responsible for its maintenance (16, 17). with mate choice, relaxes sexual selection, and blocks the mechanism of reproductive We examined the role of color in mate isolation. In this way, human activities that increase turbidity destroy both the mechanism choice of Lake Victoria in labora- of diversification and that which maintains diversity. tory experiments. Females of a sympatric red/blue sibling species pair ( nyererei/“zebra nyererei”) preferred conspe- cific over heterospecific males under broad- In the Great Lakes of Africa, large and di- to3minthe1990s and decreased in the spectrum illumination (n ϭ 8, t ϭ 3.43, P ϭ verse species flocks of cichlid fish have littoral zone from 3 to 1.5 m within the past 0.01; paired two-tailed t test), but mated evolved rapidly (1, 2). Lake Victoria, the decade (11). We have investigated the ef- indiscriminately under monochromatic largest of these lakes, had until recently at fect of these changes on the cichlids. Post- light where color differences were masked least 500 species of cichlids mating reproductive barriers have not been (n ϭ 8, t ϭϪ0.35, P ϭ 0.74) (18). Mate (3). They were ecologically so diverse that found among Lake Victoria cichlids (12), preferences of two sympatric color morphs they utilized almost all resources available to presumably because of their phylogenetic of Neochromis “blue scraper” were positively freshwater fishes in general (2), despite hav- youth. Reproductive isolation among sym- assortative (19). Hence, haplochromine ing evolved in perhaps as little as 12,400 patric species is maintained only by mate cichlids choose mates within and across years (1) and from a single ancestral species choice. have vibrantly col- species on the basis of coloration and in (4). This species flock is the most notable ored males and usually cryptically colored doing so distinguish between mates of their example of vertebrate explosive evolution females (2, 7). Their eyes are equipped with own and other species and color morphs. known today. Many of its species have van- three retinal cone pigments that cover the Light conditions constrain this choice. Eu- ished within two decades (5, 6), which can light spectrum from blue to red (13). trophication causes a decrease in light pen- only partly be explained by predation by the Sympatrically living, closely related spe- etration and a narrowing of the light spec- introduced Nile perch (Lates spp.). Steno- cies usually have male coloration at oppo- trum due to strong loss of shortwave light topic rock-dwelling cichlids, of which there site ends of the color spectrum, one being (20). Therefore, it must pose constraints on are more than 200 species (7), are rarely eaten by Nile perch (8). Yet, many such species have disappeared in the past 10 years Fig. 1. Hue of body colors as a function of light 10 Nyererei (6, 7). Because gene flow between island transmission. The redness of male nuptial colora- Neochromis populations of these cichlids is effectively tion of H. nyererei and the blueness of Neochro- 7 limited by stretches of sand and mud bottom mis “velvet black”/“blue scraper” in 13 popula- (9), populations underlie local selection re- tions along the south-north transect is quantified as the ratio of reflectance 610 nm/515 nm and gimes. Here we demonstrate that increasing 4 515 nm/610 nm, respectively, at each island (H. turbidity, by curbing the impact of sexual nyererei was absent from one). The horizontal line selection on sexual isolation, is responsible represents equal reflectance of red (610 nm) and 1 for the decline in cichlid diversity. blue (515 nm). Above the line, red is more reflect- The seven Great Lake basins of tropical ed than blue; below it, blue is more reflected than -4

Africa in which haplochromine cichlids red (negative ratio on the y axis). Three kinds of Ratio of reflectance formed endemic species flocks have dis- data are presented: (i) The brightest males (filled tinctly clearer waters than the five in which circles and open squares). Brightness (relative to -7 they did not (300 to 2200 versus 20 to 130 population average) indicates sexual activity cm maximum Secchi disc readings; n ϭ 12, (Spearman rank correlation coefficient between brightness and gonadal development within a -10 t ϭ 2.99, P ϭ 0.015). Significance increases population of H. nyererei, both scored on a 5- 0 100 200 300 400 500 when the three very large lakes Victoria, point scale: r ϭ 0.67, P Ͻ 0.00001, n ϭ 42). (ii) Width of transmission spectrum (nm) Malawi, and Tanganyika are excluded (n ϭ Population means Ϯ SE for two extreme and one 9, t ϭ 3.83, P ϭ 0.009), ruling out the intermediate population of each species. They were obtained by measuring (from left to right) 5, 5, 7 alternative hypothesis that lake size ex- individuals of H. nyererei (red points) and 6, 3, 5 of Neochromis (blue points), covering the range of plains the difference. Lake Victoria has rap- variation of sexually active males in each population. (iii) Means Ϯ SE for laboratory-bred stocks of the idly eutrophied (10) and become turbid. same three populations of H. nyererei (bars). Populations were spawned and raised separately under Water transparency decreased in deep open standardized conditions. After the fishes had attained maturity, they were kept in three groups of 10 waters from 5.5 to8minthe1920s to 1.3 males. Of each group, the five most intensely colored ones that became sexually active were eventually photographed for measurements (31). The difference (y) in hue between wild males of the red and the 2 Institute of Evolutionary and Ecological Sciences, Univer- blue species is related to spectral bandwidth (x)asyϭϪ1.83 ϩ 0.02x, r ϭ 0.88, F ϭ 71.54, P Ͻ sity of Leiden, Post Office Box 9516, NL-2300 RA Leiden, 0.00001. The difference between the mean values for wild males from dull and colorful populations is in The Netherlands. both species significant (H. nyererei: Z ϭ 1.95, P ϭ 0.05; Neochromis: Z ϭ 2.65, P Ͻ 0.01) and is *To whom correspondence should be addressed. E-mail: significant between the captive-bred fishes as well (Z ϭ 2.10, P Ͻ 0.05). The larger standard errors in [email protected] more colorful populations reflect the larger color diversity found in clear-water populations. 1808 SCIENCE ⅐ VOL. 277 ⅐ 19 SEPTEMBER 1997 ⅐ www.sciencemag.org REPORTS the functional diversity of color signals. It ble 1 and Fig. 1). Male coloration is more P ϭ 0.086). A natural selection hypothesis, should limit the number of species that can distinctly red or blue where visual condi- therefore, would make the prediction that is be sexually isolated and the number of color tions enhance the effect of red and blue opposed to the observations, that less bright morphs that are maintained merely by pref- color signals: namely, in clear, broad spec- fish occur in more transparent water. erences for different color signals. trum–illuminated water that contains suffi- Hence, male coloration is most likely deter- We studied the effect of light on cichlid ciently red and blue downwelling light to mined by sexual selection (22, 23). Direc- color and diversity on a south-north transect make a contrast against the yellowish side- tional sexual selection for conspicuously red of 13 rocky islands in southern Lake Victoria welling light. Breeding three populations of or blue males, however, can exist only (70 km across Mwanza and Speke Gulf). We H. nyererei in aquaria for one to three gen- where such colors are visible. The drab measured physical and biotic variables, in- erations demonstrated that the differences colors of males in turbid water indicate that cluding light, and spectral composition of in hue among populations are heritable male coloration is costly and is lost when male nuptial coloration in a red and a blue (Fig. 1). This experiment rules out the al- color visibility decreases (17, 23–25). species of rock-dwelling haplochromines, H. ternative hypothesis that dull coloration is Aquatic light conditions also explained nyererei and Neochromis “velvet black,” in- induced by correlated phenotypic effects of most of the variation in intraspecific color cluding its offshore replacement Neochromis turbidity such as lack of carotenoids in the morph diversity and in species number (Ta- “blue scraper” (7). We determined color diet. ble 1). The clearer the water and the broad- morph diversity in Neochromis “velvet Cichlids are more easily spotted by their er the spectrum of transmitted light, the black,” overall species diversity of rock- main predators, visually hunting birds (cor- more color morphs of a species (Fig. 2B) dwelling haplochromines, and diversity morants and egrets) and otters, in clear and the more species of a (Figs. 2 and within the most speciose genera (Neochro- waters than in turbid waters. Cormorants 3) coexist at a site. We obtained similar mis, Nyererei complex, Paralabidochromis). catch predominantly brightly colored cich- results on a 53-km-long east-west transect The largest part of interpopulation vari- lids (21), and piscivorous birds tended to be of nine rocky habitat islands that was mea- ation in hue of male nuptial coloration was more abundant where the water was clear sured in 1996 only, along which the gradi- explained by the aquatic light regime (Ta- (y ϭ 0.05 ϩ 0.0057x, F ϭ 3.55, r2 ϭ 0.24, ents of water transparency and light trans-

Table 1. Minimum adequate regression models required to explain variation in the regression model design procedure. Therefore, 11 environmental vari- in cichlid coloration, color morph, and species diversity. Fourteen environ- ables plus sampling effort were included. Cichlid diversity, resource abun- mental variables were measured: habitat patch size, distance from the main- dance, and abundance of Nile perch and birds were determined over three land, maximum water depth, mean size of rock boulders and its variation, 3-month periods spread over 3 years, water transparency and light trans- mean steepness of shore slope and its variation, resource abundance (mea- mission of the water were measured twice with an interval of 1 year. Fish sured as cichlid fish abundance), predator abundance: Nile perch and pis- coloration and light transmission were measured and quantified as described civorous birds, water transparency, bandwidth of the transmission light in (31) and Fig. 1. Regression models were calculated by a stepwise variable- spectrum, transmission of 400 nm light, and the ratio of transmission 580 nm selection procedure (32) with forward selection and a minimum F value of 4 by 400 nm. Of the last four, being different measures of the light environment, for variables to enter the model. Significance levels: *P Ͻ 0.05, **P Ͻ 0.01, only one, which correlated highest with the dependent variable, was included ***P Ͻ 0.001, ****P Ͻ 0.0001.

Explanatory variables P-value r 2 Dependent variable r 2 F (and the sign of correlation) model model

Coloration Redness of H. nyererei Width of tranmission spectrum (ϩ) 0.89 161.94**** Ͻ0.0001 0.95 Bird density (ϩ) 0.04 10.64* Mean rock size (ϩ) 0.03 5.74 Blueness of VBL* Water transparency (ϩ) 0.65 35.32*** 0.0001 0.86 Maximum depth† (ϩ) 0.17 9.71* Shore slope (Ϫ) 0.04 4.01 Color morph diversity

VBL color morph T400 nm‡ (ϩ) 0.85 59.05*** Ͻ0.0001 0.99 number* Maximum depth† (ϩ) 0.10 42.09*** Distance to the mainland (ϩ) 0.03 30.96*** Area size (ϩ) 0.009 10.02* Nile perch abundance (Ϫ) 0.006 10.70*

Shannon-Wiener index T400 nm‡ (ϩ) 0.79 80.99**** Ͻ0.0001 0.91 of VBL morph diversity* Variation in boulder size (ϩ) 0.12 17.25** Species diversity Total species number Width of transmission spectrum (ϩ) 0.70 36.04**** 0.0003 0.77 Sampling effort (ϩ) 0.07 4.26 Neochromis spp. number Water transparency (ϩ) 0.79 89.69**** Ͻ0.0001 0.95 Shore slope (Ϫ) 0.09 29.36*** Variation in shore slope (ϩ) 0.04 6.33* Sampling effort (ϩ) 0.03 5.70* Nyererei spp. number§ Width of transmission spectrum (ϩ) 0.60 19.14** 0.0011 0.60

Paralabidochromis T 580 nm/T 400 nm‡ (Ϫ) 0.50 34.66*** 0.0002 0.83 spp. number Sampling effort (ϩ) 0.28 23.24*** Nile perch abundance (Ϫ) 0.05 4.27 Shannon-Wiener index Ϫ (No variable with F Ͼ 4) – – – – of species diversityʈ *VBL, Neochromis “velvet black”/“blue scraper”. †Maximum depth is the depth of the deepest point within 100 m around each station and a measure of the time for which the area around each station is flooded again after the desiccation of the lake. ‡T400 nm, transmission at 400 nm; T580 nm, transmission at 580 nm. §Nyererei complex is an undescribed genus (7, 33). ʈSee (27). www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 277 ⅐ 19 SEPTEMBER 1997 1809 mission were much shallower (26). Finally, found in each of three genera that were where bandwidth was less than 190 nm, a similar relation occurs across water depths species rich and colorful at places with suggesting amalgamation of gene pools un- at one site between the number of syntopi- broad light spectra [Neochromis (shallow- der monochromatic light conditions at cally breeding species (y, as measured by dwelling algivores), Nyererei complex places with turbid water (28). underwater mapping of spawning sites at (deeper-dwelling planktivores), Paralabido- The effect of light conditions on colora- the island with maximum transparency) chromis (shallow- and deep-dwelling insec- tion by way of sexual selection had been and spectral width [1/y ϭ 0.23 ϩ tivores)], and only one color morph in a demonstrated before for other fish (17, 29) (Ϫ0.0003x), F ϭ 20.54, r2 ϭ 0.91, P ϭ species that was polymorphic under broad and it had been shown that populations are 0.045]. In all three instances, color morph spectra (Neochromis “velvet black”). At the more diverse when sexual selection is stron- and species numbers increased with the same time, species number was not corre- ger (23). Here, we have linked these effects breadth of the light spectrum. Under mono- lated with overall population density (Pear- to patterns of species diversity. Speciation chromatic light conditions in very turbid son’s product moment correlation coeffi- by sexual selection can explain the large waters, only one drab-colored species was cient ϭ 0.40, P ϭ 0.18). number of cichlid species (in different col- The effect of light conditions on mate ors) of each ecological and anatomical type choice based on coloration is the most like- in Lake Victoria (2, 3). Because other traits ly explanation for our results. Increasing that might function as mating barriers water turbidity reduces the diversity of color evolved less rapidly, coexistence of several signals on both sides of the color spectrum. hundred species relies on visual mate The reduced effectiveness of signals causes choice. Where eutrophication turns the relaxation of sexual selection for color, with lights off, ecological and species diversity consequent loss of male nuptial coloration erode rapidly. and erosion of species diversity due to As a consequence of deforestation and breakdown of reproductive barriers. Effects agricultural practices, water transparency in usually associated with eutrophication that Lake Victoria has probably been decreasing are detrimental to fish diversity, such as since the 1920s (10), and loss of diversity changes in resource abundance and diversi- possibly occurred already before the inten- ty or reduction in oxygen concentrations, sive investigations into the lake’s fauna. Pre- cannot explain the highly correlated pat- dation of Nile perch on primary consumers terns of diversity in trophically different and detritus feeders now adds to the eu- genera of cichlid fish. Nor can they explain trophication rate (30), and the industrializa- why niche width and interspecific niche tion and urbanization that has followed the overlap are larger at islands with fewer spe- Nile perch fishing boom is causing further cies (27). The sexual selection explanation deterioration of water quality. Pollution also is consistent with these and other field ob- threatens the other African Great Lakes and, servations: We found a negative correlation if not counteracted by management policies, between spectral bandwidth and the pro- will indeed destroy large parts of the unique portion of phenotypes that are intermediate example of vertebrate evolution that the in coloration between the red and the blue lacustrine cichlids represent. species in a widely distributed pair of sym- Fig. 2. Relation between bandwidth of the trans- REFERENCES AND NOTES patric sibling species (Pearson’s correlation ______mission spectrum and cichlid diversity. (A) Spec- n P coefficient ϭϪ0.85, ϭ 12 islands, ϭ 1. R. B. Owen et al., Proc. R. Soc. London Ser. B 240, tral bandwidth at 2 m water depth (31) and the 0.0005). Whereas intermediate types were number of coexisting haplochromine cichlid spe- 519 (1990); T. C. Johnson et al., Science 273, 1091 absent from all six places with bandwidth (1996). cies. Each point represents one of 13 rocky is- above 320 nm, 3 to 50% of the individuals 2. G. Fryer and T. D. Iles, The Cichlid Fishes of the Great lands along a south-north transect. (B) The same Lakes of Africa (Oliver and Boyd, Edinburgh, 1972); relation for the genera Neochromis (I), Nyererei were intermediate at the three sites where P. H. Greenwood, Bull. Br. Mus. Nat. Hist. ( Zool.). complex (II), Paralabidochromis (III), and for the bandwidth was between 310 and 190 nm, Suppl. 6 (1974). number of color morphs of Neochromis “velvet and the majority (68 to 88%) of the indi- 3. O. Seehausen, F. Witte, E. F. Katunzi, J. Smits, N. Bouton, Conserv. Biol. 11 (no. 4), 890 (1997). black”/“blue scraper” (IV ). viduals were intermediate at the three sites 4. A. Meyer, T. D. Kocher, P. Basasibwaki, A. C. Wil- son, Nature 347, 550 (1990). 5. C. D. N. Barel et al., ibid. 315, 19 (1985); R. Ogutu- Ohwayo, Env. Biol. Fish. 27, 81 (1990); L. Kaufman Fig. 3. Transmission spectra at a 60 and P. Ochumba, Conserv. Biol. 7, 719 (1993). water depth of2matthe13re- 6. F. Witte et al., Env. Biol. Fish. 34, 1 (1992). search stations. Numerals indicate 7. O. Seehausen, Lake Victoria Rock Cichlids, Taxono- the number of coexisting haplo- my, Ecology and Distribution ( Verduijn Cichlids, chromine species for each station. Zevenhuizen, Netherlands, 1996). Each curve is based on the mean 8. G. W. Coulter, J. Fish. Biol. 9, 235 (1976); G. W. Coulter, Ed., Lake Tanganyika and Its Life (Oxford from 10 spectral scans measured in 18 Univ. Press, Oxford, 1991). 19 1996. The width of spectra at 10% 14 9. R. L. Dorit, in Causes of Evolution, A Paleontological 15 transmission (nanometers) is relat- 11 Perspective, R. M. Ross and W. D. Ollmon, Eds. 17 ed to turbidity (centimeter Secchi 13 (Univ. of Chicago Press, Chicago, IL, 1990), pp.

Transmission (%) Transmission 12 2 322–353. disc) as y ϭ 59.73 ϩ 1.91x, r ϭ 16 9 10. R. E. Hecky, Verh. Int. Ver. Limnol. 25, 39 (1993); 7 0.88, F ϭ 77.1, P Ͻ 0.00001. 7 7 J. T. Lehman and D. K. Branstrator, ibid., p. 850. 11. M. M. A. Graham, The Victoria Nyanza and Its Fish- eries ( Waterlow, London, 1929); R. Mugidde, Verh. Int. Ver. Limnol. 25, 846 (1993); Secchi disc readings 361 464 572 684 799 decreased at two rocky littoral stations in the Tanza- Wavelength (nm) nian Mwanza Gulf from 3.2 and 2.7 m in February to

1810 SCIENCE ⅐ VOL. 277 ⅐ 19 SEPTEMBER 1997 ⅐ www.sciencemag.org REPORTS

March 1986 [M. De Beer, Ann. Mus. R. Afr. Cent. 24. A. Zahavi, J. Theor. Biol. 67, 603 (1977); A. J. Po- 30. T. Goldschmidt, F. Witte, J. Wanink, Conserv. Biol. Sci. Zool. 257, 57 (1989)] to 1.2 and 1.6 m in Febru- miankowski, ibid. 128, 195 (1987); A. P. Møller, Na- 7, 686 (1993). ary to March 1995 and February to March 1996 (O. ture 339, 132 (1989); P. H. Luyten and N. R. Liley, 31. Fish color and light transmission were measured with Seehausen, J. J. M. van Alphen, F. Witte, unpub- Behaviour 95, 164 (1985); Behav. Ecol. Sociobiol. a microspectrometer (Ocean Optics PS 1000) and lished data). 28, 329 (1991). Ocean Optics Acquisition software on a portable 12. In an experiment that was started in 1994, we 25. We compared the male coloration of the H. nyererei computer. Color was measured on the flanks of live crossed two females of Platytaeniodus degeni with population at Nyegezi rocks (Mwanza Gulf) in 1986 fishes photographed (Kodak Elite 100 ISO) under one male H. nyererei. A phylogenetic analysis con- with that of the same population in 1993 through daylight immediately after capture (reference: gray firmed that they belong to two different genera (E. 1995. The red/blue ratio [610 nm/515 nm (31)] was card). Light penetration was measured as the band- Lippitsch, O. Seehausen, N. Bouton, unpublished significantly higher in the earlier year (1.18, SE ϭ 0.14, width of the transmission spectrum at 2 m water data). The F1’s were fully viable and did not suffer n ϭ 6 versus 0.75, SE ϭ 0.17, n ϭ 11; Z ϭϪ1.96, P depth (reference: surface light). Data points for color decreased fertility: nine females of the two F1’s pro- ϭ 0.05). Two males photographed in 1978 had an are means from 10 spectral scans; those for light are duced clutch sizes of 2.64 Ϯ 1.77 (n ϭ 5) and 4.84 Ϯ even higher red/blue ratio than those from 1986. Be- means from 2 ϫ 10 spectral scans, taken with an 2.57 (n ϭ 4) fry per gram of body weight, versus tween 1986 and 1995 the water transparency at interval of 1 year. 1.14 Ϯ 1.29 (n ϭ 10) in the P. degeni F1 and 3.47 Ϯ Nyegezi rocks had dropped from 3.2 to 1.2 m (11). 32. M. J. Crawley, GLIM for Ecologists (Blackwell, Lon- 2.43 (n ϭ 7) in the H. nyererei F1. The hybrid F2 was 26. Minimum adequate regression model (and sign of don, 1993). also fully viable and fertile. Two females produced correlation) for species number: area size (ϩ) r 2 ϭ 33. E. Lippitsch, O. Seehausen, N. Bouton, unpublished clutch sizes of 3.44 Ϯ 3.34 fry per gram of body 0.62, F ϭ 19.48, spectral width (ϩ) r 2 ϭ 0.19, F ϭ data. 2 weight, and the first F3 nest is now about to reach 6.72; model r ϭ 0.81, P ϭ 0.007; model for color 34. We thank the Tanzanian Government and P. O. J. 2 maturity. Sex ratios were 2:1 female biased in F1 and morph number: water transparency (ϩ) r ϭ 0.69, F Bwathondi for research permits; the Mwanza center 2 2 F2 hybrids as well as in both parental species. M. D. ϭ 28.68, slope (Ϫ) r ϭ 0.13, F ϭ 6.45; model r ϭ of TAFIRI (E. F. B. Katunzi) for hospitality and support; Crapon de Caprona and B. Fritzsch [Neth. J. Zool. 0.82, P ϭ 0.002. M. Kayeba, R. Enoka, A. Samwel Terry, and M. Hal- 34, 503 (1984)] found no difference in fertility be- 27. The Shannon-Wiener index of species diversity is una for assistance; L. Assembe for technical realiza- tween Astatotilapia nubila ϫ Haplochromis “black calculated from the number of species and the eq- tion; L. Schadhauser, A. Samwel Terry, H. Nielsen, R. lividus” hybrids and the parent species. Three further uitability of allotment of individuals among the spe- Kiteri, H. G. Mbilinyi, C. C. Schaefer, G. De Leeuw, P. laboratory hybridizations that we did and three done cies [C. J. Krebs, Ecology, the Experimental Analysis Swelderwaard, R. Stawikowski, and R. R. Mapunda elsewhere [M. D. Crapon de Caprona, Ann. Mus. R. of Distribution and Abundance (Harper & Row, New for logistic support; T. Reimchen for discussion; K. Afr. Cent. Sci. Zool. 251, 117 (1996)] yielded viable York, 1972)]. The absence of a correlation with light Barel, N. Bouton, P. Brakefield, S. Collins, G. Fryer, F. and, where tested (two intergeneric crosses in our conditions is explained by an inverse relation be- Galis, J. Deutsch, T. Goldschmidt, I. Hardy, R. Lande, lab), fertile offspring. Successful hybridization be- tween species number and abundance equitability, P. Mayhew, H. Proehl, U. Schliewen, J. Sevenster, H. tween genera of haplochromine cichlids, resulting in indicating that resources are more equally alloted Slabbekoorn, J. de Visser, and an anonymous review- viable offspring, has also been reported from Lake among species where species number is lower. This er for comments on the manuscript; and M. Brittijn for Malawi [J. R. Stauffer, N. J. Bowers, T. D. Kocher, is supported by results of a study on resource utili- the figures. We particularly acknowledge J. Yo- K. R. McKaye, Copeia (1996), p. 203]. zation, which showed that niche width and interspe- shimura for stimulating discussions. Supported by 13. All haplochromines, the retina of which has been cific niche overlap are larger were species number is grants from the Netherlands Foundation for the Ad- studied, have one absorbance peak on blue and one lower (N. Bouton, O. Seehausen, J. J. M. van Al- vancement of Tropical Research, German Cichlid As- on yellow to red [H. J. van der Meer and J. K. Bow- phen, Ecol. Freshw. Fish, in press). sociation, TETRA, EHEIM, and with diving equipment maker, Brain Behav. Evol. 45, 232 (1995)]. 28. O. Seehausen, Ecol. Freshw. Fish 6, 59 (1997). from SCUBAPRO and SEAWAY. 14. We have recorded seven sympatric blue/yellow-red 29. T. E. Reimchen, Evolution 43, 450 (1989); J. A. En- sibling species pairs in three genera of rock-restrict- dler, Vision Res. 31, 587 (1991). 10 June 1997; accepted 6 August 1997 ed haplochromines (7) and many more in eight gen- era that inhabit other habitats [for example, R. J. C. Hoogerhoud, F. Witte, C. D. N. Barel, Neth. J. Zool. 33, 283 (1983)]. We have also found blue and yellow- red sympatric male color morphs in 11 rock-restrict- Structure and Function of a Squalene Cyclase ed species of five genera (7). 15. R. A. Fisher, The Genetical Theory of Natural Selec- tion (Clarendon, Oxford, 1930); A. Zahavi, J. Theor. K. Ulrich Wendt, Karl Poralla, Georg E. Schulz* Biol. 53, 205 (1975); R. Lande, Proc. Nat. Acad. Sci. U.S.A. 78, 3721 (1981); W. D. Hamilton and M. Zuk, Science 218, 384 (1982); M. Kirkpatrick, Am. Nat. The crystal structure of squalene-hopene cyclase from Alicyclobacillus acidocaldarius 36, 1 (1982); A. L. Basolo, Science 250, 808 (1990); was determined at 2.9 angstrom resolution. The mechanism and sequence of this A. Grafen, J. Theor. Biol. 144, 517 (1990); T. Gold- schmidt, Ethology 88, 177 (1991); M. Kirkpatrick and cyclase are closely related to those of 2,3-oxidosqualene cyclases that catalyze the M. J. Ryan, Nature 350, 33 (1991); M. J. Ryan, Oxf. cyclization step in cholesterol biosynthesis. The structure reveals a membrane protein Surv. Evol. Biol. 7, 157 (1991); J. A. Endler, Am. Nat. with membrane-binding characteristics similar to those of prostaglandin-H synthase, 139, s125 (1992). 2 16. S. N. Archer, J. A. Endler, J. N. Lythgoe, J. C. the only other reported protein of this type. The active site of the enzyme is located in Patridge, Vision Res. 28, 1243 (1987); A. L. Basolo a large central cavity that is of suitable size to bind squalene in its required conformation and J. A. Endler, Trends Ecol. Evol. 10, 489 (1995); and that is lined by aromatic residues. The structure supports a mechanism in which the G. F. Turner and M. T. Burrows, Proc. R. Soc. Lon- don. Ser. B. 260, 287 (1995); interspecific differenc- acid starting the reaction by protonating a carbon-carbon double bond is an aspartate es in photopic sensitivity to red and blue light have that is coupled to a histidine. Numerous surface ␣ helices are connected by characteristic been demonstrated for haplochromine cichlids [S. A. QW-motifs (Q is glutamine and W is tryptophan) that tighten the protein structure, Smit and G. CH. Anker, Neth. J. Zool. 47, 9 (1997)]. possibly for absorbing the reaction energy without structural damage. 17. J.A. Endler and A.E. Houde, Evolution 49, 456 (1995). 18. O. Seehausen and J. J. M. van Alphen, Behav. Ecol. Sociobiol., in press. 19. In one color morph, both sexes predominantly court- ed and responded to mates of their own morph The cyclization reactions catalyzed by fused-ring compounds (2, 3). Although (paired two-tailed t test: P ϭ 0.00005 for females, n squalene cyclases (S-cyclases) and 2,3-ox- these enzymes have been well studied ear- ϭ 12, t ϭϪ5.03; P ϭ 0.003 for males, n ϭ 5, t ϭ idosqualene cyclases (OS-cyclases) are high- lier (2, 4), present-day recombinant tech- Ϫ4.31). In the other morph, females were unselec- tive (P ϭ 0.24, n ϭ 12, t ϭ 1.21) but males again ly complex (1) and give rise to various niques have contributed much to the un- courted predominantly females of their own morph derstanding of their function and reactivity (P ϭ 0.021, n ϭ 4, t ϭ 2.85). In N. “blue scraper” (1, 5). Early suggestions for the reaction both sexes are polymorphic. The morphs do not K. U. Wendt and G. E. Schulz, Institut fu¨ r Organische differ in ecology, nor in anatomy [O. Seehausen and Chemie und Biochemie, Albertstrasse 21, D-79104 mechanism favored a concerted process (2), N. Bouton, Ecol. Freshw. Fish 6, 161 (1997)]. Freiburg im Breisgau, Germany. whereas current hypotheses (6, 7) dissect a K. Poralla, Biologisches Institut, Mikrobiologie/Biotech- 20. N. G. Jerlov, Marine Optics (Elsevier, Amsterdam, nologie, Auf der Morgenstelle 28, D-72076 Tu¨ bingen, series of carbocationic intermediates (Fig. 1976). Germany. 1). Recently, the OS-cyclases became tar- 21. E. Trewavas, Ann. Mag. Nat. Hist. 11, 435 (1938). 22. J. A. Endler, Evol. Biol. 11, 319 (1978). *To whom correspondence should be addressed. E-mail: gets for the development of antifungal and 23. ࿜࿜࿜࿜, Evolution 34, 76 (1980). [email protected] anticholesteremic drugs (8). The integral www.sciencemag.org ⅐ SCIENCE ⅐ VOL. 277 ⅐ 19 SEPTEMBER 1997 1811