Haplochromine Cichlids Research Articles

Progressive invasion and allopatric speciation can also explain distribution patterns of rock-dwelling cichlids from southern Lake Victoria: a comment on Seehausen and van Alphen (1999)

I show that distribution patterns of rock-dwelling haplochromine cichlids in the south-eastern part of Lake Victoria can be explained by allopatric speciation alone. Observed patterns are consistent with a progressive invasion of different lineages from older ( = deeper) parts of the lake, after which some lineages speciate more frequently than others. Based on a quantitative analysis of distribution data, Seehausen and van Alphen conclude that a high percentage of sympatric speciation (17.5%) is essential to explain the patterns. In my view this conclusion has its origins in an unjustifiable assumption. Seehausen and van Alphen assume that the unresolved phylogeny is balanced. However, allopatric speciation would typically result in imbalanced phylogenies.

DIVERGENCE WITH GENE FLOW IN THE ROCK-DWELLING CICHLIDS OF LAKE MALAWI

Within the past two million years, more than 450 species of haplochromine cichlids have diverged from a single common ancestor in Lake Malawi. Several factors have been implicated in the diversification of this monophyletic clade, including changes in lake level and low levels of gene flow across limited geographic scales. The objectives of this study were to determine the effect of recent lake-level fluctuations on patterns of allelic diversity in the genus Metriaclima, to describe the patterns of population structure within this genus, and to identify barriers to migration. This was accomplished through an analysis of allele frequencies at four microsatellite loci. Twelve populations spanning four species within Metriaclima were surveyed. The effect of lake-level fluctuations can be seen in the reduced genetic diversity of the most recently colonized sites; however, genetic diversity is not depressed at the species level. Low levels of population structure exist among populations, yet some gene flow persists across long stretches of inhospitable habitat. No general barrier to migration was identified. The results of this study are interpreted with respect to several speciation models. Divergence via population bottlenecks is unlikely due to the large allelic diversity observed within each species. Genetic drift and microallopatric divergence are also rejected because some gene flow does occur between adjacent populations. However, the reduced levels of gene flow between populations does suggest that minor changes in the selective environment could cause the divergence of populations.Corresponding Editor: S. Edwards

Rapid Morphological Changes Following Niche Shift in the Zooplanktivorous Cyprinid Rastrineobola Argentea From Lake Victoria

During the 1980s, the zooplanktivorous cyprinid dagaa (Rastrineobola argentea) expanded its habitat in Lake Victoria. After the eradication of the zooplanktivorous haplochromine cichlids from the sublittoral waters of the Mwanza Gulf (Tanzania) by introduced Nile perch (Lates niloticus), adult dagaa started to explore the bottom zone during daytime. This main daytime habitat for zooplankton and macrobenthic invertebrates was formerly occupied by the haplochromines. Besides extending its range of vertical distribution, dagaa started to include macrobenthic invertebrates in its diet. In this paper, we present two rapid morphological adaptations of dagaa to its new niche. Samples from 1988, only one year after daytime bottom dwelling became a common habit in dagaa, showed a higher number of gill filaments in comparison with samples from 1983. In contrast, the same samples showed a decrease in the number of gill rakers. The observed increase in the number of gill filaments is postulated to have improved the capacity of dagaa to extract oxygen from the water, which may be crucial to survive the relatively poor oxygen conditions in the new habitat. By decreasing the number of gill rakers dagaa has probably increased its efficiency of feeding on relatively large prey in a benthic habitat.

Trophic shifts in predatory catfishes following the introduction of Nile perch into Lake Victoria

This study looked for evidence of trophic shifts in the diet of two predatory catfishes (Bagrus docmac and Schilbe intermedius) following the establishment of introduced Nile perch (Lates niloticus) into lakes of the Lake Victoria basin. Bagrus docmac exhibited a shift from a primarily piscivorous diet dominated by haplochromine cichlids to a broader diet that included a significant proportion of invertebrates and the cyprinid fish, Rastrineobola argentea, which became abundant following depletion of the haplochromines. Schilbe intermedius exhibited a trophic shift from a piscivorous diet dominated by haplochromines to an insectivorous diet. The flexibility in diet exhibited by these two catfishes may have permitted these species to persist, albeit in reduced numbers, subsequent to the introduction of Nile perch and may facilitate resurgence as fishing pressure reduces numbers of large Nile perch.

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

Rapid speciation can occur on ecological time scales and interfere with ecological processes, resulting in species distribution patterns that are difficult to reconcile with ecological theory. The haplochromine cichlids in East African lakes are an extreme example of rapid speciation. We analyse the causes of their high speciation rates. Various studies have identified disruptive sexual selection acting on colour polymorphisms that might cause sympatric speciation. Using data on geographical 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.

Isolation and sequencing of cDNA clones coding for the catalytic unit of glucose-6-phosphatase from two haplochromine cichlid fishes.

Complementary DNA clones coding for the catalytic unit of the enzyme glucose-6-phosphatase (G6Pase) were obtained from Haplochromis nubilus and Haplochromis xenognathus, two cichlid fish species from Lake Victoria. The translated sequence of these two cDNAs identifies a polypeptide consisting of 352 amino acid residues and showing a 54.4% similarity to the human form of G6Pase. The amino acid sequences of the two fish species are identical. The comparison of the fish amino acid sequence with the corresponding sequences of rat, mouse, and human G6Pase revealed that the amino acid residues, which are involved in G6Pase catalysis in humans, are also conserved in fish G6Pase. Northern blot analysis showed that G6Pase is expressed at the same level in 6- and 10-day-old fish. A three base pair insertion/deletion polymorphism was found in the 3'-untranslated region of the fish G6Pase gene. The polymorphism will be a useful marker in a phylogenetic study of Lake Victoria cichlids.

Direct mate choice maintains diversity among sympatric cichlids in Lake Victoria

Mate choice may play an important role in animal speciation. The haplochromine cichlids of Lake Victoria are suitable to test this hypothesis. Diversity in ecology, coloration and anatomy evolved in these fish faster than postzygotic barriers to gene flow, and little is known about how this diversity is maintained. It was tested whether recognizable forms are selection‐maintained morphs or reproductively isolated species by investigating in the field reproductive timing, location of spawning sites, and mate choice behaviour. There was a large interspecific overlap in timing of breeding and location of spawning sites, which was largest in members of the same genus. Behavioural mate choice of such closely related taxa was highly assortative, such that it is likely that they are sexually isolated species and that direct mate choice is the major force that directs gene flow and maintains form diversity. The results differ from what is known about recent radiations of other lacustrine fish groups where speciation seems to be driven by diverging microhabitat preferences or diverging timing of reproduction, but are in agreement with predictions from models of speciation by diverging mate preferences.

Direct mate choice maintains diversity among sympatric cichlids in Lake Victoria

Mate choice may play an important role in animal speciation. The haplochromine cichlids of Lake Victoria are suitable to test this hypothesis. Diversity in ecology, coloration and anatomy evolved in these fish faster than postzygotic barriers to gene flow, and little is known about how this diversity is maintained. It was tested whether recognizable forms are selection-maintained morphs or reproductively isolated species by investigating in the field reproductive timing, location of spawning sites, and mate choice behaviour. There was a large interspecific overlap in timing of breeding and location of spawning sites, which was largest in members of the same genus. Behavioural mate choice of such closely related taxa was highly assortative, such that it is likely that they are sexually isolated species and that direct mate choice is the major force that directs gene flow and maintains form diversity. The results differ from what is known about recent radiations of other lacustrine fish groups where speciation seems to be driven by diverging microhabitat preferences or diverging timing of reproduction, but are in agreement with predictions from models of speciation by diverging mate preferences.

Sympatric speciation and extinction driven by environment dependent sexual selection

A theoretical model is studied to investigate the possibility of sympatric speciation driven by sexual selection and ecological diversification. In particular we focus on the rock–dwelling haplochromine cichlid species in Lake Victoria. The high speciation rate in these cichlids has been explained by their apparent ability to specialize rapidly to a large diversity of feeding niches. Seehausen and colleagues however, demonstrated the importance of sexual selection in maintaining reproductive barriers between species. Our individual–orientated model integrates both niche differentiation and a Fisherian runaway process, which is limited by visibility constraints. The model shows rapid sympatric speciation or extinction of species, depending on the strength of sexual selection.

Hypoxia Tolerance of the Mormyrid Petrocephalus catostoma: Implications for Persistence in Swamp Refugia

changes in fish faunal structure and diversity. Though catches of many species had declined by the 1960s due to overexploitation (Kudhongania et al., 1992), the dramatic increase in Nile perch in the 1980s in Lake Victoria was followed by a drastic decline in the populations of several indigenous species (Kaufman, 1992). Most notable has been the disappearance of over 50% of the endemic haplochromine cichlids from Lake Victoria (Kaufman, 1992; Kaufman et al., 1997). However, many indigenous noncichlids, some of which were important in the pre-Nile perch fishery, have also declined or disappeared (Kaufman, 1992; Kudhongania et al., 1992). Similar trends have been observed in other

Phylogeny of African cichlid fishes as revealed by molecular markers.

The species flocks of cichlid fish in the three great East African Lakes, Victoria, Malawi, and Tanganyika, have arisen in each lake by explosive adaptive radiation. Various questions concerning their phylogeny have not yet been answered. In particular, the identity of the ancestral founder species and the monophyletic origin of the haplochromine cichlids from the East African lakes have not been established conclusively. In the present study, we used the anonymous nuclear DNA marker DXTU1 as a step towards answering these questions. A 280 bp-fragment of the DXTU1 locus was amplified by the polymerase chain reaction from East African lacustrine species, the East African riverine cichlid species Haplochromis bloyeti, H. burtoni and H. sparsidens, and other African cichlids. Sequencing revealed several indels and substitutions that were used as cladistically informative markers to support a phylogenetic tree constructed by the neighbor-joining method. The topology, although not supported by high bootstrap values, corresponds well to the geographical distribution and previous classification of the cichlids. Markers could be defined that: (i) differentiate East African from West African cichlids; (ii) distinguish the riverine and Lake Victoria/Malawi haplochromines from Lake Tanganyika cichlids; and (iii) indicate the existence of a monophyletic Lake Victoria cichlid superflock which includes haplochromines from satellite lakes and East African rivers. In order to resolve further the relationship of East African riverine and lacustrine species, mtDNA cytochrome b and control region segments were sequenced. The mtDNA-based trees support the notion of the monophyly of the Lake Victoria superflock but are ambiguous with respect to the phylogenetic position of the Lake Malawi flock.

Phylogeny of African cichlid fishes as revealed by molecular markers

The species flocks of cichlid fish in the three great East African Lakes, Victoria, Malawi, and Tanganyika, have arisen in each lake by explosive adaptive radiation. Various questions concerning their phylogeny have not yet been answered. In particular, the identity of the ancestral founder species and the monophyletic origin of the haplochromine cichlids from the East African lakes have not been established conclusively. In the present study, we used the anonymous nuclear DNA marker DXTU1 as a step towards answering these questions. A 280 bp-fragment of the DXTU1 locus was amplified by the polymerase chain reaction from East African lacustrine species, the East African riverine cichlid species Haplochromis bloyeti, H. burtoni and H. sparsidens, and other African cichlids. Sequencing revealed several indels and substitutions that were used as cladistically informative markers to support a phylogenetic tree constructed by the neighbor-joining method. The topology, although not supported by high bootstrap values, corresponds well to the geographical distribution and previous classification of the cichlids. Markers could be defined that: (i) differentiate East African from West African cichlids; (ii) distinguish the riverine and Lake Victoria/Malawi haplochromines from Lake Tanganyika cichlids; and (iii) indicate the existence of a monophyletic Lake Victoria cichlid superflock which includes haplochromines from satellite lakes and East African rivers. In order to resolve further the relationship of East African riverine and lacustrine species, mtDNA cytochrome b and control region segments were sequenced. The mtDNA-based trees support the notion of the monophyly of the Lake Victoria superflock but are ambigious with respect to the phylogenetic position of the Lake Malawi flock.

Ecological Consequences of Alternative Gill Net Fisheries for Nile Perch in Lake Victoria

Both harvest rates and food web interactions may be altered through use of different gill net mesh sizes in the fisheries of Lake Victoria, East Africa. Thus, conservation of the native ichthyofauna is intimately linked to patterns of exploitation in the fisheries. We used bioenergetics modeling to estimate the harvest rates of introduced Nile perch (Lates cf. niloticus) and changes in their predation rates on other important fishes that would result from the implementation of various restrictions on gill net mesh size. Total mass of harvested Nile perch was predicted to vary more than three‐fold over the range of minimum gill net mesh size from 3 to 16 inches. Maximum harvest is expected to result from minimum mesh size restrictions between 6 and 10 inches. Predation rates on all prey fishes would increase with all increases in minimum mesh size. Universal enforcement of a 5‐inch minimum mesh size would reduce both Nile perch cannibalism and predation on other important fishes, such as tilapiines, haplochromine cichlids, and Rastrineobola argentea by as much as 44%, with little decrease (10%) in Nile perch yield. But, if fishers respond to a 5‐inch minimum mesh size by concentrating all fishing effort on the smallest gill nets (5‐ and 6‐inch mesh), a substantially larger reduction in predation on native haplochromines will result, but at the expense of large (~35%) decreases in Nile perch harvest. Our analyses demonstrate that fisheries in Lake Victoria will play an active role in the restoration of a diverse fish community and fishery resource, thus benefiting both many native fish species and the sustainability of the fishery.Consecuencias Ecológicas de Pesquerìas de Redes Agalleras Alternativas para la Perca del Nilo en el Lago VictoriaTanto las tasas de cosecha como las interacciones de la cadena alimenticia pueden ser alteradas mediante el uso de diferentes tamaños de luz de malla de las redes agalleras en las pesquerías del lago Victoria, en el este de Africa. Por lo tanto, la conservación de la ictiofauna nativa esta íntimamente ligada a los patrones de explotación de las pesquerías. Utilizamos un modelado bioenergético para estimar las tasa de cosecha de la perca del Nilo introducida (Lates cf. niloticus) y los cambios en sus tasas de depredación sobre otras especies de peces importantes, mismos que podrìan resultar de la implementación de varias restricciones en el tamaño de la luz de malla de redes agalleras. Se predijo que la masa total cosechada de perca del Nilo variará mas de tres veces sobre un rango mìnimo de luz de malla de entre 3 y 16 pulgadas. Las cosechas máximas se esperan como resultado de restricciones en el tamaño mìnimo de luz de malla entre 6 y 10 pulgadas. Las tasas de depredación en todas las presas de peces podría incrementarse con todos los incrementos en el tamaño de luz de malla. La aplicación estricta de un mínimo de luz de malla de 5 pulgadas podría reducir tanto el canibalismo de la perca del Nilo así como su depredación sobre otras especies importantes de peces, como son las tilapias, los cíclidos haplocrominos y Rastrineobola argenta por hasta un 44%, con una pequeña disminución (10%) en la cosecha de la perca. Sin embargo, si los pescadores responden a un tamaño mínimo de luz de malla de 5 pulgadas al concentrar todo el esfuerzo pesquero en las redes mas pequeñas (i.e., 5 y 6 pulgadas de luz de malla), podría obtenerse una reducción sustancialmente grande en la depredación de los peces haplocrominos, pero a expensas de un disminución considerable (~35%) en la cosecha de la perca. Nuestro análisis demuestra que las pesquerías del lago Victoria jugarán un papel activo en la restauración de la comunidad diversa de peces y recursos pesqueros,beneficiando tanto a varias especies nativas de peces, como a la sustentabilidad de la pesquería.

The effect of male coloration on female mate choice in closely related Lake Victoria cichlids ( Haplochromis nyererei complex)

We studied the effect of male coloration on interspecific female mate choice in two closely related species of haplochromine cichlids from Lake Victoria. The species differ primarily in male coloration. Males of one species are red, those of the other are blue. We recorded the behavioral responses of females to males of both species in paired male trials under white light and under monochromatic light, under which the interspecific differences in coloration were masked. Females of both species exhibited species-assortative mate choice when colour differences were visible, but chose non-assortatively when colour differences were masked by light conditions. Neither male behaviour nor overall female response frequencies differed between light treatments. That female preferences could be altered by manipulating the perceived colour pattern implies that the colour itself is used in interspecific mate choice, rather than other characters. Hence, male coloration in haplochromine cichlids does underlie sexual selection by direct mate choice, involving the capacity for individual assessment of potential mates by the female. Females of both species responded more frequently to blue males under monochromatic light. Blue males were larger and displayed more than red males. This implies a hierarchy of choice criteria. Females may use male display rates, size, or both when colour is unavailable. Where available, colour has gained dominance over other criteria. This may explain rapid speciation by sexual selection on male coloration, as proposed in a recent mathematical model.

Why are there so many cichlid species?

The explosive speciation of cichlid fishes in the African great lakes has intrigued biologists for many decades. Interest was revitalized in 1996 after the publication in Science of geological data[1]indicating that the youngest lake, Lake Victoria, must have been completely dry during the most recent Ice Age—perhaps as recently as 12 400 years ago. This implies that the approximately 500 haplochromine cichlid species must have evolved within this extremely short timespan from a single ancestral species[2]. But even with lower estimates of species number and higher estimates of the age of the species flock, the haplochromine cichlids still present one of the most dramatic examples of speciation and diversification in vertebrates.

Unusually fine–scale genetic structuring found in rapidly speciating Malawi cichlid fishes

Mechanisms behind the explosive radiation of over 500 cichlid fish species from a single founding population in Lake Malawi during the last 700 000 years are poorly understood. Recent studies have suggested that the degree of population subdivision among the habitat patches within the lake may be responsible, but the evidence has been circumstantial: lack of a dispersal stage in haplochromine cichlids; genetic and colour variation among populations separated by large-scale geographical barriers; and fluctuating lake levels. One reason for the rapidity of speciation in these fishes may be that population subdivision is on a much finer scale than previously thought. Here we quantify the level of population subdivision and estimate migration at a scale of 700-1400 m, in order to investigate whether cichlid populations are sufficiently isolated from each other for allopatric divergence and perhaps speciation to take place. Using six microsatellite loci, we demonstrate the existence of highly significant genetic differentiation between subpopulations on adjacent headlands in each of four rock-dwelling haplochromine cichlid species. Our results suggest that these fish populations are divided into thousands of subunits among which genetic divergence is currently occurring, and that this may provide unprecedented opportunities for allopatric speciation.

Resource partitioning among rock‐dwelling haplochromines (Pisces: Cichlidae) from Lake Victoria

Abstract— Resource partitioning was studied on four assemblages of haplochromine cichlids at rocky islands in the southern part of Lake Victoria. The emphasis was put on diet segregation, while data on microhabitat segregation were mainly used to determine potential competitors for food. Diet and microhabitat segregation were demonstrated in all four assemblages. In one of the assemblages we observed little partitioning of resources among two filamentous algae feeders. The role of competition for food is discussed on the basis of fluctuations in diet overlap in relation to seasonal changes in food supply. Diet overlap proved to be highest in periods of food abundance. This is in concordance with the hypothesis that competition decreases in case of food abundance. Furthermore, we compared fish densities between assemblages, because competition would regulate density. We found that diets were most diverse in the assemblage with lowest fish density, while interspecific differences in diet were smallest. Food seems not to be limiting in this particular assemblage, and factors other than competition for food are probably more important in regulating density here.

Microdistribution and fluctuations in niche overlap in a rocky shore cichlid community in Lake Victoria

Abstract— The microdistribution of ten numerically dominant species in a fish community at a rocky island in Lake Victoria was studied using invasive sampling. All were haplochromine cichlids. The community was characterized by high fish densities and by a dominance of Aufwuchs feeders. Species were non‐randomly distributed, showing significant associations with water depth and other topographic parameters. Species occupied unique positions in a network of recurrent species groups. Niche partitioning through differential microdistribution was even more subtle than that reported for Lake Malawi's rock‐dwelling cichlids. Species‐specific microdistribution fitted qualitative predictions from ideal free distribution models with asymmetrical interference competition for food. No evidence was found for interspecific contest competition for space. Temporal niche shifts have been observed between periods of high and low water levels. Owing to a combination of reduced habitat availability with niche expansion in most species, niche overlap was larger during the lowwater period.

Colour diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection?

The mechanisms responsible for the explosive radiations of haplochromine cichlid fishes in Africa's great lakes remain controversial. Since species thought to be closely related often differ most apparendy in male breeding colours, I examined patterns of male colour variation in rock-dwelling cichlids from Lake Malawi to test whether initial divergence between species is likely to have been caused by adaptation to differing habitats, by selection against hybridization (reinforcement or character displacement), or by sexual selection. I found that all significant variation in overall male colour occurs within, not between, species complexes, in contrast to variation in habitat and behavioural traits, which differed significandy between complexes. Male colour does not vary significandy with habitat characteristics such as water depth, and sympatric species differ no more in colour than allopatric ones. These results fail to provide support for adaptation or reinforcement as initial causes of colour divergence, and are consistent with the possibility that divergence may instead have been caused by sexual selection, but a direct test of sexual selection is not yet possible.

Patterns of the Remnant Cichlid Fauna in Southern Lake Victoria

During the years 1984–1987 Lake Victoria in East Africa experienced what is probably the largest mass extinction of contemporary vertebrates. Within a decade about 200 endemic species of haplochromine cichlids disappeared. The extinctions that occurred in the 1980s have been documented predominantly on species of offshore and sub‐littoral waters in the Mwanza Gulf of southern Lake Victoria. Although the littoral fauna of southern Lake Victoria had not been examined in detail, their diversity seemed less affected by the changes in the ecosystem. We give results of the first comprehensive inventory of the littoral cichlid fauna in southern Lake Victoria and discuss its conservation status. We also report on new developments in the sub‐littoral fauna after 1990. More than 50 littoral and 15 sub‐littoral stations were sampled between the years 1991 to 1995. Of the littoral stations, 34 were sampled for the first time. One hundred sixty three species of haplochromines were collected. Of these, 102 species were previously unknown. About two thirds of them live in rocky areas that were sampled for the first time. Littoral rocky habitats harbored the highest diversity. Since 1990, however, 13 more species disappeared from established sampling stations in littoral habitats. Fishing practices, spreading of exotic fishes, water hyacinth, and eutrophication are considered important threats to the littoral fauna. Also in the upper sub‐littoral the number of species declined further. On deeper sub‐littoral mud bottoms individual and species numbers increased again, although they are nowhere close to those found before the Nile perch (Lates niloticus) upsurge. This fauna differs from the well studied pre‐Nile perch fauna. At well‐established sampling stations, the sub‐littoral zone is dominated by previously unknown species, and some known species have performed dramatic habitat shifts.