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Ecology Letters, (1999) 2 : 262271


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, 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 : 262271 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
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Lake Victoria cichlid sympatric speciation? 263

polygynous and have conspicuous sexual colour dimorphisms (Dominey 1984). Elevated speciation rates might then be expected anyway due to strong selection on mate choice traits (Fisher 1930; Lande 1981; West-Eberhard 1983; Dominey 1984; Mitra et al. 1996; Mller & Cuervo 1998). However, there are many more cichlid lineages with the same polygynous mating system that have not undergone rapid speciation. These include the direct sister groups of the explosive taxa that live under identical conditions in the same lakes (Serranochromis Regan, Astatoreochromis Pellegrin, Pseudocrenilabrus Fowler, Tropheini). Price (1998) considered sexual selection not necessarily suitable to explain elevated speciation rates. 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, 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. Alone, sexual selection may therefore not be sufficient to explain rapid speciation. We hypothesize that rapid speciation in haplochromine cichlids is explained by the possession of intrinsic properties, not shared by other sexually selected cichlid lineages, that, despite open-ended preference rules, make sexual selection disruptive and cause sympatric speciation. Simulation studies have shown that when disruptive, sexual selection can cause sympatric speciation within a very short time (Turner & Burrows 1995; van Doorn et al. 1998). 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. But even without change in preference rule, sexual selection can become disruptive when mate choice is based on the intensity with which individuals emit a signal, and when equivalent signal intensities can be achieved in more than one way (e.g. equally conspicuous colouration might be achieved by reflectance of different parts of the light spectrum). These conditions for disruptiveness of sexual selection occur in the explosive cichlid clades. 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. 1999). In one polymorphism males are either blue or yellow to red and all females are cryptically brownish, but prefer either blue or yellow to red males (Seehausen 1997; Knight et al. 1998; Seehausen & van Alphen 1998). If females choose the mate that they perceive as brightest, 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, will trigger disruptive sexual selection without change in the preference rule, and could lead to the origin of the blue/yellow-red male colour polymorphism. Variation in visual properties of the predicted kind has been demonstrated between haplochromine species (Van der Meer & Bowmaker 1995; Smit & Anker 1997). 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, may allow the maintenance of the genetical basis of the polymorphism despite sexual selection (Seehausen et al. 1999). In the other kind of colour polymorphism females are either cryptically plain brown or conspicuously orange or white with black blotches, and the female colour variation is associated with male mate preference variation (Holzberg 1978; Konings 1995; Knight & Turner, in press; Seehausen, van Alphen and Lande, unpublished). In this case variation in mate preferences is due to genotypespecific preference rules. Female colour polymorphism is associated with sex ratio distorting genes. 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. submitted). Because females of many Lake Victoria cichlids guard their fry, it is possible that sexual imprinting (Immelmann 1972; Ten Cate and Vos 1999) plays a role in the determination of these male mate preferences. On the other hand, 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. We hypothesize that disruptive sexual selection on these two colour polymorphisms has caused frequent and rapid sympatric speciation. The hypothesis that colour polymorphisms are incipient stages in sympatric speciation is not new (Holzberg 1978; Marsh et al. 1981), but a body of supporting evidence is now available for the polymorphisms we have described. Experimental (Knight et al. 1998; Seehausen & van Alphen 1998; Knight and Turner in press; Seehausen, van Alphen and Lande, unpublished), field ecological (Seehausen et al. 1997), genetical (Seehausen, van Alphen and Lande, unpublished) and modelling studies (Turner & Burrows 1995; R. Lande, unpublished; Seehausen, van Alphen and Lande, unpublished), together with earlier and recent molecular population genetical studies (McKaye et al. 1982, 1984; Van Oppen et al. 1998), now provide a rather complete picture of most facets of the hypothesized speciation process. The important question to be asked is whether it has played any important role in the origin of
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haplochromine species diversity, and thereby helps explain their unusual speciation rates. Here we test the hypothesis that sympatric speciation by disruptive sexual selection upon polymorphic colouration has frequently occurred, 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. If dispersal was entirely unrestricted within the lake, and had not been restricted in the past, all intralacustrine speciation would be sympatric. However, dispersal is restricted in the species that we studied. These were species of rocky bottoms. They are stenotopic, and stretches of soft or sand bottom often bar gene flow between their populations (Dorit 1990; Van Oppen et al. 1997). Hence, we expect allopatric speciation in this group, but if sympatric speciation by disruptive sexual selection on polymorphic colouration contributed significantly to the origin of species diversity in the group too, 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; (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. Note that with respect to the geography of speciation, the second prediction that the proportion of colour heteromorphic sister species pairs is higher in sympatric pairs, 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. Alone, the second prediction would be inconclusive because allopatric divergence followed by dispersal with selective local extinction, due to introgression of populations with the same body colouration, would result in the same distribution pattern. Ideally one would study the proportion of nodes on a phylogenetic tree, across which sister species attained/ maintained the attributes associated with the speciation mechanism in question (Lynch 1989; Barraclough et al. 1998), i.e. sympatry and colour heteromorphy. To do so, 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. The latter is not available (Meyer et al. 1990). In the absence of such information, 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. This procedure adds noise to the signal by
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diluting the distribution patterns that result from speciation, with those that result from secondary range extension, but, unless the speed of range extension greatly differs between sister species or the real phylogeny is very unbalanced, is unlikely to produce a bias with respect to testing the null hypothesis that all speciation is allopatric, and that the proportion of colour heteromorphic species pairs is the same among allopatric and sympatric species pairs. If sympatric speciation is common, the phylogeographic signal that it produces should be detectable.

Precise sister species relationships among haplochromine cichlids of Lake Victoria are notoriously difficult to establish (Greenwood 1980; Meyer et al. 1990; Lippitsch 1993). However, well-differentiated clades are present, and those among the rock-dwelling haplochromines proved robust to different approaches (Greenwood 1980; Lippitsch 1993; Seehausen 1996; Seehausen et al. 1998; Lippitsch & Seehausen, unpublished). Using the four well-defined clades among rock-dwelling haplochromines that have been described as genera (Greenwood 1980; Seehausen et al. 1998; Fig. 1), and considering all congeneric species as each other's sister species, 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. Data on geographical distribution of 41 rock-dwelling species are based on several years of research, summarized by Seehausen (1996) and Seehausen et al. (1998). Due to the patchy distribution of rocky habitat, 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. Our distribution data are based on 47 habitat patches sampled in an area of roughly 5000 km2. Data on colouration of the same species were collected in the field and were recorded immediately upon capture of specimens. More than 10 000 specimens have been inspected, and a subsample of about 1000 have been photographed upon capture (colours fade quickly in preserved specimens). About 300 colour photos of all species are published, as well as colour descriptions of all species, which are based on the inspection of many more live fish and many more unpublished colour photos (Seehausen 1996; Seehausen et al. 1998). The data matrix is provided in the Appendix. 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, in the case of Neochromis (the only genus in this study with polymorphic

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Lake Victoria cichlid sympatric speciation? 265

Figure 1 Phylogenetic tree of the studied monophyletic rock-dwelling lineage of haplochromine cichlids. The tree is based on a cladistic analysis of morphological characters (scale surface morphology, squamation, dentition; Seehausen et al. 1998). The four polytomies represent the four genera. By making each species within a genus ``sister species'' of each other species in the same genus, the branching sequence between the genera does not enter into our analysis.

female colouration), female colouration had to be known from at least five individuals. Proportions of geographical overlaps were calculated between any two species within each of the four genera, as the proportion of the recording sites of the less widely distributed species in a pair where the ``sister species'' was also found. If speciation occurred in sympatry, the distribution range of the less widely distributed species is predicted to be nested within the range of the more widely distributed sister species. Proportions of geographical overlaps were assigned to five categories: 0%20%, 21% 40%, 41%60%, 61%80% and 81%100%. Male nuptial colouration was assigned to four categories, ``blue'', ``yellow'', ``red'' and ``melanic'', referring to the colouration of the body (Seehausen et al. 1999). 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). Dark fish were assigned to ``blue'', ``yellow'', or ``red'' if the hue under the melanophore layer could be identified, and to ``melanic'' if not. In species that are polymorphic for male nuptial colouration, the numerically dominant colour morph was determined (w2-test, P 5 0.05). The minimum number n of males to assign male colouration to a

population of a species that is known as polymorphic from other populations, was therefore 4. Note that different species with the same body colouration can differ in details of fin colouration, which is not considered here. Female colouration was assigned to two categories, ``plain'' and ``blotched''. Except for one individual of Lithochromis xanthopteryx, ``blotched'' occurred in the studied clade only in species of Neochromis Regan, many of which are polymorphic for female colouration. 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, (b) five or more females had been inspected, among which were no ``blotched'' individuals, or (c) in cases of n 5 5, all better sampled populations of the species are exclusively ``plain''. In one species (Neochromis ``yellow anal scraper'') less than five females were known from all populations together. Female colouration of its populations was scored as unknown. In all other cases, populations of Neochromis were assigned ``blotched''.

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tion with modes on fully allopatric and fully sympatric in the genera Mbipia Lippitsch & Seehausen, Neochromis Regan and Pundamilia Seehausen & Lippitsch, as predicted if sympatric speciation accounts for some of the speciation events. Bimodality is not apparent in Lithochromis Lippitsch & Seehausen (Fig. 2 and 3). To rule out that this pattern is caused by few widely distributed species that might produce much secondary sympatry with local endemics, 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. This does by definition exclude more sympatric than allopatric pairs, but the bimodality of geographical overlap with modes on fully allopatric and fully sympatric in three genera remained distinct.

The proportion of species pairs whose member species differ in being fixed for, or dominated by, alternative colour morphs of one of the two described polymorphisms (blue versus yellow-red male colouration, plain brown versus blotched female colouration) is higher among sympatric species pairs (81%100% geographical overlap) than among allopatric pairs (Fig. 4), as predicted if sympatric speciation is mostly caused by disruptive sexual selection upon these polymorphisms, while allopatric speciation can be caused by a variety of events. There are 2.7 times more heteromorphic species pairs in sympatry than in allopatry when all species pairs are considered, and still 2.4 times more when pairs of species with very different distribution range sizes (see above) are excluded. The total proportion of species pairs with (almost) entirely overlapping (81%100%) geographical distributions is 14% (Mbipia 67%, Neochromis 22%, Pundamilia 12%, Lithochromis 7%; in total 33 species pairs), as opposed to 66% with purely or almost purely allopatric distributions (in total 160 species pairs). Despite the low proportions of sympatric pairs in Pundamilia and Lithochromis, the actual number of sympatric pairs is not lower than in the other two genera (Fig. 3). At the same time, the number of allopatric pairs is higher, suggesting that divergence in allopatry occurs more often in Pundamilia and Lithochromis than in the other lineages.

Figure 2 The proportions of congeneric species pairs plotted against geographical distribution overlap, for four genera of rock-dwelling Lake Victoria haplochromines.

Figure 3 The numbers of congeneric species pairs plotted against geographical distribution overlap.
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Patterns of geographical distribution in relation to colour variation and phylogeny of haplochromine cichlid species from rocky shores in Lake Victoria, support predictions yielded by the hypothesis that some of the speciation events occurred in sympatry due to disruptive sexual selection on existing colour polymorphisms. There are more predominantly allopatric and predominantly sympatric species pairs than pairs with intermediate proportions of geographical overlap. This is best explained if there are two modes of speciation: speciation caused by geographical isolation of populations, and speciation caused by the evolution of behavioural or other forms of isolation within populations. 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, and to re-establish sympatry with more slowly spreading species after allopatric speciation, could produce a distribution pattern similar to that produced if widely distributed species repeatedly gave rise to daughter species in sympatry. In the case of Lake Victoria cichlids, this may be less of a problem than in many other cases, because the extreme recency of the species flock formation sets narrow limits to the time that

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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, ``plain brownish'' versus ``blotched'' females), plotted against geographical distribution overlap. 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), which caused ambiguity over whether to count lack of overlap with these species as lack of overlap with a ``blue'' or a ``red'' population. Furthermore, the species pair Neochromis greenwoodi/ N. ``short head nigricans'' was excluded because of similar ambiguity. This case of no overlap could be counted as lack of overlap with the ``blotched'' populations of N. greenwoodi that occur south-west of Vesi Islands (the locality to which N. ``short head nigricans'' is endemic), or with the ``plain'' populations that occur north-east of Vesi Islands. Top: all species pairs are considered. Bottom: pairs of species with very different distribution range sizes (see text) are excluded.

was available for range extension after speciation. 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, such as traits that allow life under a wider range of ecological conditions, or traits that enhance dispersal. Two examples of species that cause many cases of sympatry are Pundamilia pundamilia and Neochromis gigas. Pundamilia pundamilia is a widely distributed species and engulfs the ranges of more (10) congeneric species than any other species does. However, it has quite specific habitat demands, and is outnumbered by its congeners at most of its record localities (Seehausen 1996; Bouton et al. 1997). Neochromis gigas is a wide spread species that causes the second largest number of sympatric cases (three) with congeners. Neochromis gigas is one of the most stenotopic algae scrapers in the genus, with certainly no less specific habitat demands than its fully sympatric congeners (Seehausen 1996). (b) Excluding species pairs with very asymmetric distribution range sizes (including eight of the 10 cases of sympatry with P. pundamilia, and two of the three with N. gigas) did not remove the bimodality of distribution overlap. 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, is not surprising. 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. 1997). When that is the case, and when evolutionary change within island populations is fast relative to genetical exchange between islands, 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). The second prediction, which is supported by the data, 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. While the proportion of heteromorphic pairs is larger in sympatry, their absolute number is not larger in sympatry than in allopatry. The best explanation is that speciation in sym- and allopatry can be associated with the same intraspecific colour polymorphisms. However, while geographically isolated populations can diverge in various other ways to species status too (e.g. changes in colouration of the fins), speciation by disruptive sexual selection on polymorphic body colouration is the major mechanism in sympatry. Distribution patterns of most species that occur nested within the range of a conspecific can be explained by
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limited dispersal after speciation (e.g. Neochromis rufocaudalis has a continuous distribution range nested within the range of N. greenwoodi; Seehausen et al. 1998). However, there are some species with very disjunct distribution ranges (Mbipia lutea, Pundamilia nyererei, P. ``all red''/``red flank'', P. macrocephala; Seehausen 1996; Seehausen et al. 1998), all of which overlap fully with a more widely distributed congener, that except in the case of P. macrocephala belongs to an alternative colour morph. The possibility that some parallel speciation has occurred at several sites cannot therefore currently be excluded. In the latter case we would underestimate the number of sympatric speciation events. A rough approximation of the contribution of sympatric speciation to the origin of rock-dwelling haplochromine species diversity yields 17.5% of the speciation events (no. sympatric pairs/[no. sympatric pairs + no. allopatric pairs]). 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. That assumption is untested in species pairs without distribution overlap, and may in some cases be wrong. 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. 1998). Its effects on mate choice remain to be tested. (b) Some of the sympatric colour morphs that we considered conspecific because they differ in male or female colouration, but in nothing else, are partly reproductively isolated incipient species (Seehausen et al. submitted), and some may actually be fully isolated sibling species. (c) The rock-dwelling haplochromines appear to be the most stenotopic and philopatric of all lacustrine haplochromines. They should hence be more prone to allopatric speciation than any other group (van Oppen et al. 1997), reducing the proportion of sympatric speciation events. To test this prediction, our study should be repeated on other clades of Lake Victoria haplochromines that inhabit open waters, sandy and muddy bottoms. To date no accurate distribution records are available for such groups. In conclusion, the distribution data from rock-dwelling Lake Victoria haplochromines studied here, lend support to a hypothesis that was based on field ecological, behavioural and genetical evidence: that haplochromine cichlids can speciate in sympatry by disruptive sexual selection on polymorphic colouration. The data suggest that among rock-dwelling cichlids allopatric speciation is very common too. The relative importance of the two speciation modes predictably depends on the amount of
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gene flow between populations in a patchy environment. It is predicted to differ not only between habitats but to have changed also in the course of the history of the lake. 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, when distances between habitat patches are small, species are unspecialized and populations are panmictic. A property that causes sympatric speciation in that situation could jump-start the evolutionary radiation. 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. It would explain why rapid radiations occurred only in lakes with relatively good visual conditions (Seehausen et al. 1997). Where colour vision is constrained, this property becomes ineffective as a cause of speciation and, hence, as a jump-starter of radiation. 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, such as the three sibling species of Lake Malawi haplochromines studied by Genner et al. (1999) that represent both presently studied colour polymorphisms [blue males and plain females in Pseudotropheus zebra (Boulenger), yellow males and plain females in P. ``zebra gold'', blue males and blotched females in P. callainos Stauffer & Hert].

We thank the Tanzanian Commission for Science and Technology for the research permit for OS, the Tanzanian Fisheries Research Institute (Prof. P.O.J. Bwathondi, E.F.B. Katunzi) for hospitality and support, the Tanzanian Fisheries Division for permits to export live fishes; M.K.Kayeba, R. Enoka, A. Samwel-Terry, M. Haluna, P. Snelderwaard, S. Ober and A. Rozier for technical assistance; E. Lippitsch, F. Witte, N. Bouton and F. Galis for pleasant collaboration; R. Lande, T. Price, G. Turner, A. Mors, and F. Witte for comments on the manuscript; P. Brakefield, J. Endler for fruitful discussions; C.D.N. Barel for starting the Mwanza based cichlid research; A. Samwel-Terry, C. Schaefer, L. Schadhauser, R. Kitery, H. Gonza Mbilinyi, H. Nielsen for logistical support; M. Brittijn for Fig. 1; and WOTRO (grant no. 84282) and NWO (grant no. 80536.025) for financial support.
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Ole Seehausen's main subject of interest is evolutionary ecology, in particular speciation and ecological and evolutionary processes that regulate species diversity. His main study object is the radiation of cichlid fishes in Lake Victoria. He is currently a postdoctoral research fellow working with Jacques van Alphen and Frans Witte on the behavioural and genetical basis of speciation, and on the roles of intrinsic and environmental properties in speciation and coexistence of cichlids.

Editor, M.E. Hochberg Manuscript received 9 March 1999 First decision made 20 April 1999 Manuscript accepted 11 May 1999

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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

Location2 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 B B B B R B* B R B 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

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In populations that are polymorphic for male body coloration (*), the numerically dominant colour morph (w2-test, P 5 0.05) is reported, except in Neochromis, where female coloration is reported and the dominant male coloration is blue in all species except N. ``yellow anal scraper''. B, blue body in males, brown in females; R, Y, red or yellow body in males, brown in females; M, males completely melanic; O, 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; ?, occurrence of species uncertain.