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Paper 082 e-mail

Ecology Letters, (1999) 2 : 262±271

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Can sympatric speciation by disruptive sexual selection explain rapid evolution of cichlid diversity in Lake Victoria?

Abstract Rapid speciation can occur on ecological time scales and interfere with ecological processes, resulting in species distribution patterns that are difficult to reconcile with Institute of Evolutionary and ecological theory. The haplochromine cichlids in East African lakes are an extreme Ecological Sciences, University of example of rapid speciation. We analyse the causes of their high speciation rates. Leiden, PO Box 9516, 2300 RA Various studies have identified disruptive sexual selection acting on colour Leiden, The Netherlands. polymorphisms that might cause sympatric speciation. Using data on geographical E-mail: distribution, colouration and relatedness from 41 species endemic to Lake Victoria, seehausen@rulsfb.leidenuniv.nl we test predictions from this hypothesis. Plotting numbers of pairs of closely related species against the amount of distributional overlap between the species reveals a bimodal distribution with modes on allopatric and sympatric. The proportion of sister species pairs that are heteromorphic for the traits under disruptive selection is higher in sympatry than in allopatry. These data support the hypothesis that disruptive sexual selection on colour polymorphisms has caused sympatric speciation and help to explain the rapid radiation of haplochromine species flocks. Ahed Bhed Keywords Ched Adaptive radiation, cichlids, colouration, disruptive selection, haplochromines, Lake Dhed Ref marker Victoria, polymorphism, rapid evolution, sexual selection, sympatric speciation Fig marker Table marEcology Letters (1999) 2 : 262±271 ker Ref end explain the phenomenon. Understanding rapid speciation Ref start INTRODUCTION is therefore essential to understanding community ecology of cichlid species flocks. Research in evolutionary ecology has shown that evoluRapid speciation is observed in several fish groups tion often proceeds more rapidly than was hitherto under lacustrine conditions. It has been suggested that thought (Thompson 1998). When evolutionary processes sympatric speciation accounts for the phenomenon (Turnoccur on ecological time scales, they may interfere with er 1994; Schluter 1996; McCune 1997). Sympatric ecological processes in ways that are not usually speciation, if it does occur, proceeds faster than allopatric considered in ecological theory. Rapid evolution can speciation because in sympatric speciation the mating include rapid cladogenesis. A striking example is the system must be under disruptive selection (Maynard haplochromine cichlid fishes in East African lakes (Galis Smith 1966). Model studies show convincingly that & Metz 1998; Turner 1999). More than 500 haplochrosympatric speciation is a plausible and, under particular mine species have evolved in Lake Victoria in about 12 conditions, even a likely scenario (Maynard Smith 1966; 500 years (Johnson et al. 1996), and massive haplochroTauber & Tauber 1977; Wu 1985; Kondrashov 1986; mine speciation has occurred in Lake Malawi within 200 Turner & Burrows 1995; Doebeli 1996; Payne & years (Owen et al. 1990). Although haplochromine species Krakauer 1997; Kondrashov 1998; Van Doorn et al. flocks are overall ecologically diverse, ecologists have 1998). It is these conditions, however, that many been puzzled by the existence of complexes of closely evolutionary biologists see as too constraining for related species that are ecologically very similar and sympatric speciation to be an important factor in the appear to defy the principle of competitive exclusion evolution of animal species diversity. (Genner et al., 1999). Rapid speciation at rates high Sexual selection has also been suggested to explain the enough to outrun rates of extinction by competitive rapid speciation in haplochromine cichlids. They are exclusion or divergence by character displacement might
Ole Seehausen and Jacques J.M. van Alphen
#1999 Blackwell Science Ltd/CNRS

van Alphen and Lande. But even without change in preference rule. submitted). Knight & Turner. In the other kind of colour polymorphism females are either cryptically plain brown or conspicuously orange or white with black blotches. 1984. Lande 1981. equally conspicuous colouration might be achieved by reflectance of different parts of the light spectrum). Epistasis by which the expression of structural genes is affected by regulatory genes such that a structural gene is not expressed unless a specific allele constellations occurs at the regulatory loci. make sexual selection disruptive and cause sympatric speciation. will trigger disruptive sexual selection without change in the preference rule. sexual selection can become disruptive when mate choice is based on the intensity with which individuals emit a signal. now provide a rather complete picture of most facets of the hypothesized speciation process. Ten Cate and Vos 1999) plays a role in the determination of these male mate preferences. he argues that the fact that mate preference rules are usually open-ended defies the hypothesized potential of sexual selection to directly create reproductive isolation between populations. but a body of supporting evidence is now available for the polymorphisms we have described. The important question to be asked is whether it has played any important role in the origin of #1999 Blackwell Science Ltd/CNRS . unpublished. Mitra et al. Because females of many Lake Victoria cichlids guard their fry. Seehausen & van Alphen 1998).Paper 082 e-mail Lake Victoria cichlid sympatric speciation? 263 polygynous and have conspicuous sexual colour dimorphisms (Dominey 1984). together with earlier and recent molecular population genetical studies (McKaye et al. In one polymorphism males are either blue or yellow to red and all females are cryptically brownish. it is possible that sexual imprinting (Immelmann 1972. Changes in the direction of open-ended mate choice preference rules is likely where the quality of a mate for the choosing sex depends on the genotype of the chooser. unpublished). and when equivalent signal intensities can be achieved in more than one way (e. Alone. Smit & Anker 1997). However. 1998). van Alphen and Lande. genetical (Seehausen. Van Oppen et al. imprinting is unlikely in the female mate preference polymorphisms because juvenile females do not see their father and split from their brothers before the development of nuptial colouration. field ecological (Seehausen et al. These include the direct sister groups of the explosive taxa that live under identical conditions in the same lakes (Serranochromis Regan. 1998. 1998. despite open-ended preference rules. van Alphen and Lande. These clades exclusively share two kinds of genetical polymorphisms in colouration that are associated with mate preference polymorphism and commonly occur within populations as well as across closely related sympatric and allopatric species that do not otherwise differ in any discrete morphological character (Seehausen et al. Seehausen. R. van Alphen and Lande. Although he considers that sexual selection can lead to the evolution of much diversity in male traits that could then be used in species recognition. These conditions for disruptiveness of sexual selection occur in the explosive cichlid clades. Knight et al. and could lead to the origin of the blue/yellow-red male colour polymorphism. Lande. Simulation studies have shown that when disruptive. The preference rule that males apply (``most conspicuous is best'' or ``least conspicuous is best'') depends on the presence of resistance genes in the choos-ing males (Seehausen et al. 1999). 1996. unpublished). Female colour polymorphism is associated with sex ratio distorting genes. but prefer either blue or yellow to red males (Seehausen 1997. West-Eberhard 1983. sexual selection can cause sympatric speciation within a very short time (Turner & Burrows 1995. in press.g. sexual selection may therefore not be sufficient to explain rapid speciation. Konings 1995. Variation in visual properties of the predicted kind has been demonstrated between haplochromine species (Van der Meer & Bowmaker 1995. that. may allow the maintenance of the genetical basis of the polymorphism despite sexual selection (Seehausen et al. Pseudocrenilabrus Fowler. van Doorn et al. Elevated speciation rates might then be expected anyway due to strong selection on mate choice traits (Fisher 1930. Seehausen & van Alphen 1998. Dominey 1984. there are many more cichlid lineages with the same polygynous mating system that have not undergone rapid speciation. On the other hand. and the female colour variation is associated with male mate preference variation (Holzberg 1978. 1981). If females choose the mate that they perceive as brightest. Tropheini). not shared by other sexually selected cichlid lineages. unpublished). Experimental (Knight et al. 1997). 1998). Seehausen. Seehausen. Price (1998) considered sexual selection not necessarily suitable to explain elevated speciation rates. Astatoreochromis Pellegrin. We hypothesize that rapid speciation in haplochromine cichlids is explained by the possession of intrinsic properties. In this case variation in mate preferences is due to genotypespecific preference rules. unpublished) and modelling studies (Turner & Burrows 1995. Mùller & Cuervo 1998). 1999). 1982. We hypothesize that disruptive sexual selection on these two colour polymorphisms has caused frequent and rapid sympatric speciation. Knight and Turner in press. Marsh et al. the occurrence of a deviant male colour morph in a population that contains variation in visual properties affecting the relative sensitivity to blue and yellow-red light. The hypothesis that colour polymorphisms are incipient stages in sympatric speciation is not new (Holzberg 1978.

Species had to fulfil two criteria to be considered in the analysis: (a) to be recorded from more than one locality or from only one locality that is not at the periphery of the survey area. (b) male colouration or. Seehausen 1996. Alone. is conclusive only in combination with the first prediction that the proportions of overlap between species has a bimodal frequency distribution with modes on fully allopatric and fully sympatric. Meyer et al. its signature should be traceable in the phylogeographic record: (a) The proportions of closely related species pairs plotted against geographical distribution overlap between the species should have a bimodal frequency distribution with modes on the fully allopatric and fully sympatric. Fig. Data on geographical distribution of 41 rock-dwelling species are based on several years of research. sympatry and colour heteromorphy. well-differentiated clades are present. is unlikely to produce a bias with respect to testing the null hypothesis that all speciation is allopatric. we propose that a robust approximation is helpful by which each species within a phylogenetically well-defined clade is treated as the sister species of each other species in the same clade. would result in the same distribution pattern. Hence. i. which are based on the inspection of many more live fish and many more unpublished colour photos (Seehausen 1996. About 300 colour photos of all species are published. but. we test the two predictions yielded by the hypothesis that sympatric speciation by disruptive selection on two specific kinds of colour polymorphism contributed to the origin of species diversity. but if sympatric speciation by disruptive sexual selection on polymorphic colouration contributed significantly to the origin of species diversity in the group too. dispersal is restricted in the species that we studied. van Alphen haplochromine species diversity. Note that with respect to the geography of speciation. More than 10 000 specimens have been inspected. (1998). 1997). Lippitsch 1993. Our distribution data are based on 47 habitat patches sampled in an area of roughly 5000 km2. Ideally one would study the proportion of nodes on a phylogenetic tree. and that the proportion of colour heteromorphic species pairs is the same among allopatric and sympatric species pairs. To do so. Seehausen and J. unpublished). with those that result from secondary range extension. They are stenotopic. Barraclough et al. 1998. all intralacustrine speciation would be sympatric. 1990. Van Oppen et al. and thereby helps explain their unusual speciation rates. we expect allopatric speciation in this group. Seehausen et al. and considering all congeneric species as each other's sister species. Lippitsch 1993). However. Seehausen et al. the second prediction would be inconclusive because allopatric divergence followed by dispersal with selective local extinction. the second prediction that the proportion of colour heteromorphic sister species pairs is higher in sympatric pairs. The latter is not available (Meyer et al. Here we test the hypothesis that sympatric speciation by disruptive sexual selection upon polymorphic colouration has frequently occurred. Using the four well-defined clades among rock-dwelling haplochromines that have been described as genera (Greenwood 1980. The data matrix is provided in the Appendix. In the absence of such information. These were species of rocky bottoms. If sympatric speciation is common. and those among the rock-dwelling haplochromines proved robust to different approaches (Greenwood 1980. Seehausen et al. This procedure adds noise to the signal by #1999 Blackwell Science Ltd/CNRS diluting the distribution patterns that result from speciation. 1998. Data on colouration of the same species were collected in the field and were recorded immediately upon capture of specimens. unless the speed of range extension greatly differs between sister species or the real phylogeny is very unbalanced. If dispersal was entirely unrestricted within the lake.Paper 082 e-mail 264 O.M. due to introgression of populations with the same body colouration. 1998). all these stenotopic species have patchy distributions and overlap between two species is most accurately measured as the proportion of patches on which both occur. and a subsample of about 1000 have been photographed upon capture (colours fade quickly in preserved specimens). as well as colour descriptions of all species. summarized by Seehausen (1996) and Seehausen et al.J. sufficiently detailed knowledge on the attributes of each species (colouration and geographical distribution in our case) and robust information on phylogenetic sister species relationships is required. 1998). MATERIALS AND METHODS Precise sister species relationships among haplochromine cichlids of Lake Victoria are notoriously difficult to establish (Greenwood 1980. across which sister species attained/ maintained the attributes associated with the speciation mechanism in question (Lynch 1989. However. the phylogeographic signal that it produces should be detectable. (b) the proportion of sister species pairs that are heteromorphic for one of the two colour polymorphisms associated with disruptive selection should be higher in sympatric pairs than in allopatric pairs. and had not been restricted in the past.e. 1). Due to the patchy distribution of rocky habitat. in the case of Neochromis (the only genus in this study with polymorphic . Lippitsch & Seehausen. and stretches of soft or sand bottom often bar gene flow between their populations (Dorit 1990. 1990). by inferring geographical modes of speciation and their association with colour variation from patterns of geographical distribution in relation to phylogeny of 41 haplochromine species in Lake Victoria.

dentition. Note that different species with the same body colouration can differ in details of fin colouration. The tree is based on a cladistic analysis of morphological characters (scale surface morphology. 1998). Proportions of geographical overlaps were calculated between any two species within each of the four genera. P 5 0. and to ``melanic'' if not. RESULTS The proportion of congeneric species pairs plotted against geographical distribution overlap has a bimodal distribu#1999 Blackwell Science Ltd/CNRS . The minimum number n of males to assign male colouration to a population of a species that is known as polymorphic from other populations. A population of Neochromis was assigned ``plain'' if: (a) in larger samples (n 4 10) blotched morphs made up less than 10% of the individuals. In one species (Neochromis ``yellow anal scraper'') less than five females were known from all populations together. In all other cases. referring to the colouration of the body (Seehausen et al. The darkness of cichlids is determined by a system of small melanophores that cover the nonmelanic colours produced by deeper laying chromatophores (Baerends & Baerends-van Roon 1950). ``blotched'' occurred in the studied clade only in species of Neochromis Regan. Female colouration was assigned to two categories. Female colouration of its populations was scored as unknown. the distribution range of the less widely distributed species is predicted to be nested within the range of the more widely distributed sister species. all better sampled populations of the species are exclusively ``plain''. In species that are polymorphic for male nuptial colouration. If speciation occurred in sympatry. Seehausen et al. was therefore 4. 41%±60%. Proportions of geographical overlaps were assigned to five categories: 0%±20%. female colouration had to be known from at least five individuals. ``yellow''. among which were no ``blotched'' individuals. The four polytomies represent the four genera. or ``red'' if the hue under the melanophore layer could be identified. 1999). female colouration).05). ``yellow''. 21%± 40%. squamation. the numerically dominant colour morph was determined (w2-test. By making each species within a genus ``sister species'' of each other species in the same genus. as the proportion of the recording sites of the less widely distributed species in a pair where the ``sister species'' was also found. 61%±80% and 81%±100%. ``blue''.Paper 082 e-mail Lake Victoria cichlid sympatric speciation? 265 Figure 1 Phylogenetic tree of the studied monophyletic rock-dwelling lineage of haplochromine cichlids. the branching sequence between the genera does not enter into our analysis. Except for one individual of Lithochromis xanthopteryx. (b) five or more females had been inspected. ``plain'' and ``blotched''. populations of Neochromis were assigned ``blotched''. Dark fish were assigned to ``blue''. or (c) in cases of n 5 5. ``red'' and ``melanic''. Male nuptial colouration was assigned to four categories. many of which are polymorphic for female colouration. which is not considered here.

2 and 3). the number of allopatric pairs is higher. for four genera of rock-dwelling Lake Victoria haplochromines.Paper 082 e-mail 266 O. This is best explained if there are two modes of speciation: speciation caused by geographical isolation of populations. plain brown versus blotched female colouration) is higher among sympatric species pairs (81%±100% geographical overlap) than among allopatric pairs (Fig.4 times more when pairs of species with very different distribution range sizes (see above) are excluded. in total 33 species pairs). this may be less of a problem than in many other cases. or dominated by. Lithochromis 7%.7 times more heteromorphic species pairs in sympatry than in allopatry when all species pairs are considered. #1999 Blackwell Science Ltd/CNRS Patterns of geographical distribution in relation to colour variation and phylogeny of haplochromine cichlid species from rocky shores in Lake Victoria. 3). Bimodality is not apparent in Lithochromis Lippitsch & Seehausen (Fig. Pundamilia 12%. we considered in a second analysis only pairs of species in which the geographical distribution range sizes (measured as the area between record localities) differed by no more than the factor 5. alternative colour morphs of one of the two described polymorphisms (blue versus yellow-red male colouration. Despite the low proportions of sympatric pairs in Pundamilia and Lithochromis. A general difficulty with testing sympatric speciation from species distribution patterns is that a situation in which species that acquire novel features allowing them to extend their range faster and/or more widely than others.M. van Alphen tion with modes on fully allopatric and fully sympatric in the genera Mbipia Lippitsch & Seehausen. At the same time. because the extreme recency of the species flock formation sets narrow limits to the time that . suggesting that divergence in allopatry occurs more often in Pundamilia and Lithochromis than in the other lineages. as opposed to 66% with purely or almost purely allopatric distributions (in total 160 species pairs). could produce a distribution pattern similar to that produced if widely distributed species repeatedly gave rise to daughter species in sympatry. Neochromis 22%. DISCUSSION Figure 2 The proportions of congeneric species pairs plotted against geographical distribution overlap. 4). This does by definition exclude more sympatric than allopatric pairs. as predicted if sympatric speciation accounts for some of the speciation events. and speciation caused by the evolution of behavioural or other forms of isolation within populations. The total proportion of species pairs with (almost) entirely overlapping (81%±100%) geographical distributions is 14% (Mbipia 67%. Seehausen and J. In the case of Lake Victoria cichlids. as predicted if sympatric speciation is mostly caused by disruptive sexual selection upon these polymorphisms. but the bimodality of geographical overlap with modes on fully allopatric and fully sympatric in three genera remained distinct. while allopatric speciation can be caused by a variety of events. support predictions yielded by the hypothesis that some of the speciation events occurred in sympatry due to disruptive sexual selection on existing colour polymorphisms. Neochromis Regan and Pundamilia Seehausen & Lippitsch.J. There are more predominantly allopatric and predominantly sympatric species pairs than pairs with intermediate proportions of geographical overlap. There are 2. To rule out that this pattern is caused by few widely distributed species that might produce much secondary sympatry with local endemics. and still 2. and to re-establish sympatry with more slowly spreading species after allopatric speciation. The proportion of species pairs whose member species differ in being fixed for. the actual number of sympatric pairs is not lower than in the other two genera (Fig. Figure 3 The numbers of congeneric species pairs plotted against geographical distribution overlap.

Furthermore. while geographically isolated populations can diverge in various other ways to species status too (e. ``plain brownish'' versus ``blotched'' females). There are two additional reasons why we think that the secondary sympatry model does not explain the patterns that we found: (a) There is no evidence that the widely distributed species possess any features that would allow them to undergo range extension more quickly than other species. which is supported by the data. pundamilia. 1997). speciation by disruptive sexual selection on polymorphic body colouration is the major mechanism in sympatry. (b) Excluding species pairs with very asymmetric distribution range sizes (including eight of the 10 cases of sympatry with P. greenwoodi that occur south-west of Vesi Islands (the locality to which N. However. is not surprising. Distribution patterns of most species that occur nested within the range of a conspecific can be explained by #1999 Blackwell Science Ltd/CNRS . Neochromis gigas is one of the most stenotopic algae scrapers in the genus. While the proportion of heteromorphic pairs is larger in sympatry. The second prediction. the species pair Neochromis greenwoodi/ N. and two of the three with N. Top: all species pairs are considered. is that species of sympatric pairs ± more often than species of allopatric pairs ± exhibit alternative morphs of the colour polymorphisms that are associated with disruptive sexual selection. Bouton et al.Paper 082 e-mail Lake Victoria cichlid sympatric speciation? 267 Figure 4 The proportion of species pairs that are heteromorphic with respect to one of the two body colour polymorphisms (``blue'' versus ``yellow'' to ``red'' males. That the data do not reveal evidence for frequent speciation in clines that might be expected to result in a higher number of species pairs with intermediate proportions of overlap. When that is the case. This case of no overlap could be counted as lack of overlap with the ``blotched'' populations of N. such as traits that allow life under a wider range of ecological conditions. However. ``short head nigricans'' was excluded because of similar ambiguity. and when evolutionary change within island populations is fast relative to genetical exchange between islands. or traits that enhance dispersal. their absolute number is not larger in sympatry than in allopatry. Cases of no overlap with the species Pundamilia ``big blue'' and Lithochromis ``pseudoblue'' are excluded from the count because populations of these species were about equally often ``blue'' and ``red'' (see Appendix). Rocky outcrops are isolated by stretches of soft bottoms that often effectively bar gene flow between populations of rock-dwelling cichlids (Van Oppen et al. Two examples of species that cause many cases of sympatry are Pundamilia pundamilia and Neochromis gigas.and allopatry can be associated with the same intraspecific colour polymorphisms. was available for range extension after speciation. which caused ambiguity over whether to count lack of overlap with these species as lack of overlap with a ``blue'' or a ``red'' population. The best explanation is that speciation in sym. plotted against geographical distribution overlap. Pundamilia pundamilia is a widely distributed species and engulfs the ranges of more (10) congeneric species than any other species does. ``short head nigricans'' is endemic). Bottom: pairs of species with very different distribution range sizes (see text) are excluded. speciation can occur only by either transformation of an entire island population into a new species (allopatric speciation) or splitting of a population within one island (sympatric speciation). it has quite specific habitat demands. 1997). gigas) did not remove the bimodality of distribution overlap. Neochromis gigas is a wide spread species that causes the second largest number of sympatric cases (three) with congeners. with certainly no less specific habitat demands than its fully sympatric congeners (Seehausen 1996). or with the ``plain'' populations that occur north-east of Vesi Islands. and is outnumbered by its congeners at most of its record localities (Seehausen 1996. changes in colouration of the fins).g.

(b) Some of the sympatric colour morphs that we considered conspecific because they differ in male or female colouration. P. F. M. G. reducing the proportion of sympatric speciation events. Bouton and F. the distribution data from rock-dwelling Lake Victoria haplochromines studied here. there are some species with very disjunct distribution ranges (Mbipia lutea.M. all of which overlap fully with a more widely distributed congener. sympatric pairs + no. macrocephala belongs to an alternative colour morph. Gonza Mbilinyi.J. the Tanzanian Fisheries Research Institute (Prof. sympatric pairs/[no. To test this prediction. lend support to a hypothesis that was based on field ecological. E. Schaefer. 1997). It is predicted to differ not only between habitats but to have changed also in the course of the history of the lake. when distances between habitat patches are small. Seehausen et al. A. 1. hence. Intrinsic properties that cause disruptive selection and sympatric speciation are likely to elevate speciation rates in particular in an early stage of lake and species flock formation.K. and may in some cases be wrong. N. that except in the case of P. 84±282) and NWO (grant no. but in nothing else. However. L. Witte. Schadhauser. REFERENCES Baerends. 1. 805±36.F. callainos Stauffer & Hert]. Price. and some may actually be fully isolated sibling species.M. To date no accurate distribution records are available for such groups. R. Seehausen and J. Kitery. It would explain why rapid radiations occurred only in lakes with relatively good visual conditions (Seehausen et al. the Tanzanian Fisheries Division for permits to export live fishes. In conclusion. Nielsen for logistical support. S. 1998). E. The possibility that some parallel speciation has occurred at several sites cannot therefore currently be excluded. Behaviour Suppl. Its effects on mate choice remain to be tested. Samwel-Terry.5% of the speciation events (no. An introduction to the study of the ethology of cichlid fishes. That assumption is untested in species pairs without distribution overlap. such as the three sibling species of Lake Malawi haplochromines studied by Genner et al. Rozier for technical assistance. Ober and A. P. (1950). Lande. van Alphen limited dispersal after speciation (e. Haluna. 1998).g. Colour divergence between allopatric species is often less distinct and of a different kind (affecting caudal and anal fin colouration and degree of melanism rather than hue of body colouration) than that between sympatric species (Seehausen et al. our study should be repeated on other clades of Lake Victoria haplochromines that inhabit open waters. A rough approximation of the contribution of sympatric speciation to the origin of rock-dwelling haplochromine species diversity yields 17. H. In the latter case we would underestimate the number of sympatric speciation events. greenwoodi. macrocephala. M. Galis for pleasant collaboration. Brakefield. Bwathondi. J. P. 1±242. R. as a jump-starter of radiation. blue males and blotched females in P. Moùrs. & Baerends-Van Roon. ``zebra gold''. Katunzi) for hospitality and support.J. Barel for starting the Mwanza based cichlid research. C. Neochromis rufocaudalis has a continuous distribution range nested within the range of N. The data suggest that among rock-dwelling cichlids allopatric speciation is very common too. Lippitsch. H. ACKNOWLEDGEMENTS We thank the Tanzanian Commission for Science and Technology for the research permit for OS. A. 1997). It would furthermore explain the coexistence without niche partitioning of heterochromatic recently diverged species among which character displacement has not (yet) played much of a role. Endler for fruitful discussions. allopatric pairs]). this property becomes ineffective as a cause of speciation and.B. ``all red''/``red flank''. (c) The rock-dwelling haplochromines appear to be the most stenotopic and philopatric of all lacustrine haplochromines. are partly reproductively isolated incipient species (Seehausen et al.N.025) for financial support. A.D. A property that causes sympatric speciation in that situation could jump-start the evolutionary radiation. R. submitted). Enoka. species are unspecialized and populations are panmictic. yellow males and plain females in P. Samwel-Terry.Paper 082 e-mail 268 O. . M.O. behavioural and genetical evidence: that haplochromine cichlids can speciate in sympatry by disruptive sexual selection on polymorphic colouration. Witte for comments on the manuscript. P.P. Where colour vision is constrained. sandy and muddy bottoms. Seehausen et al. 1998). P. Brittijn for Fig. C. They should hence be more prone to allopatric speciation than any other group (van Oppen et al. Snelderwaard. T. We argue that colour polymorphism associated with disruptive sexual selection is such an intrinsic property and can be the cause of the rapid evolutionary radiation of the haplochromine lineages that possess it. The relative importance of the two speciation modes predictably depends on the amount of #1999 Blackwell Science Ltd/CNRS gene flow between populations in a patchy environment. Turner. G. and F.Kayeba. Projected onto the entire haplochromine species flock in Lake Victoria (4500 species). this is likely a minimum estimate for three reasons: (a) Assignment of species status to allopatric forms relies on the assumption that forms would not introgress if they became sympatric. J. Pundamilia nyererei. (1999) that represent both presently studied colour polymorphisms [blue males and plain females in Pseudotropheus zebra (Boulenger). Seehausen 1996. and WOTRO (grant no.

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red or yellow body in males. ?. B. where female coloration is reported and the dominant male coloration is blue in all species except N. males completely melanic. polymorphic female body coloration with 10%±60% orange or white blotched females among the otherwise brown females. colouration unknown or unknown which morph is dominant. Y. M. R. brown in females. P 5 0. +. . the numerically dominant colour morph (w2-test. except in Neochromis.Appendix Record localities and body coloration of 41 species of rock-restricted haplochromines in four genara1 Species Neochromis rufocaudalis gigas greenwoodi/black nigricans omnicaeruleus unicuspid scraper yellow anal scraper eastern blue scraper short head nigricans long black large eye nigricans Mbipia mbipi lutea red carp Pundamilia pundamilia big blue red head all black nyererei orange dorsal igneopinnis Ukerewe azurea Bwiru red anal all red/red flank pink anal red rim anal macrocephalus slender deepwater blue deepwater yellow deepwater Lithochromis rufus rubripinnis/large eye xanthopteryx black long snout yellow chin scraper pseudoblue black Ukerewe Ukerewe 1 Location2 ÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐÐ A B C D E F G H I J K L M N O P Q R S T U V W X Y Z a b c d e f g h i j k l m n o p q r s t u ± ± ± ± ± ± ± ± B B B B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B B B B B B B B B B B B B B B ± ± ± ± ± ± ± B ± ± ± ± ± ± ± B ± ± B B B B B + O B O* ± B O O* ± O* O ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± ± R M B B ± ± R ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± R B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B* ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± ± ± M ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± M ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± O ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B B B ± B B ± ± ± O ± ± O* + ± ± ± ± B ± O ± ± ± ± ± O + ± ± ± ± ± O* ± + ± ± ± ± ± B ± +* ± + ± ± ± ± ± ± B ± ± ± O ± ± B B ± ± + ± + ± ± ± ± ± ± ± ± ± ± B B B ± B ± B B ± B B ± ± ± ± ± ± ± ± ± ± + B ± ± ± ± ± ± B ± ± ± ± ± ± ± ± B ± ± ± + ± ± B ± O* ± ± ± ± B* ± ± ± ± O ± ± ± ± B ± B B B B B ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± B O O + + O + O O ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± + ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± O ± ± ± ± ± ± ± ± ± ± ± ± ± B B B B ± ± ± ± R ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± Y R ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B Y R B ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B Y R B ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B Y R B* ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B ± R B ± ± ± ± ± ± ± ± B B B B B ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B Y R B ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B ± R B ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± R B* ± ± ± ± ± B* ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± B B ± ± ± ± R ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± ± R* ± ± B ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± B R ± ± ± + ± ± ± B ± + ± ± ± ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± M ± ± ± ± ± ± ± B B B B B B B ± ± ± Y Y ± Y ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± R ± ± B ± ± ± ± B ± ± ± ± ± ± ± ± B B ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± R ± R ± ± B ± ± B B ± ± ± ± ± ± ± ± ± ± B ± ± ± B ± ± ± ± ± R ± ± B ± ± ± B ± ± ± ± ± ± ± ± ± ± B ± ± ± B ± ± ± R ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± R ± ± ± ± ± B ± ± ± ± ± B ± ± ± ± ± ± ± ± B ± ± ± ± ± B B B B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± B ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B* ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± R ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B B B ± ± ± ± Y ± ± ± ± ± B ± ± ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± B B B ± ± ± ± ± ± B ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± B B B ± ± ± R ± ± ± ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± B ± B ± ± ± R ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± B ± ± ± ± B B B B B B B B B B ± ± ± ± ± Y ± Y ± ± ± ± ± ± ± ± ± ± ± ± ± B ± M ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B* ± M ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B R ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± R ± ± ± ± ± ± ± ± ± ± B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± B ± ± ± ± B ± ± ± R ± ± ± ± ± ± ± ± ± ± ± ± ± Lake Victoria cichlid sympatric speciation? 271 #1999 Blackwell Science Ltd/CNRS Paper 082 e-mail In populations that are polymorphic for male body coloration (*). blue body in males. occurrence of species uncertain. brown in females. O. ``yellow anal scraper''.05) is reported.