Recent sympatric speciation involving habitat-associated nuptial colour polymorphism in a crater lake cichlid

Even though the idea that modes of speciation other than allopatric speciation are possible in nature is now widespread, compelling examples of ecological speciation in sympatry remain rare. We studied an undescribed radiation of haplochromine cichlids in a young crater lake in western Uganda, and in the small river that is nearby but has currently no known surface connection to the lake. We describe two different modes of speciation that occurred in this cichlid lineage within the past 1,500–10,000 years. Not constrained by gene flow, allopatric divergence between river and lake cichlids affects many different morphological traits as well as nuptial colouration—muted in the river, but intensified and polymorphic in lake cichlids—and neutral genetic differentiation. More surprisingly, we demonstrate a case for sympatric speciation within the small lake that is associated with dramatic differences in male breeding colouration (yellow with bright red-chest versus bright blue) and subtle differences in microhabitat, feeding regime and morphology. Reproductive isolation by assortative mating is suggested by significant differentiation between yellow and blue males in neutral markers of gene flow despite complete sympatry. We hypothesize speciation is mediated by divergent selection on sexual signalling between microhabitats.

     

Reticulate sympatric speciation in Cameroonian crater lake cichlids

BACKGROUND: Traditionally the rapid origin of megadiverse species flocks of extremely closely related species is explained by the combinatory action of three factors: Disruptive natural selection, disruptive sexual selection and partial isolation by distance. However, recent empirical data and theoretical advances suggest that the diversity of complex species assemblages is based at least partially on the hybridization of numerous ancestral allopatric lineages that formed hybrids upon invasion of new environments. That reticulate speciation within species flocks may occur under sympatric conditions after the primary formation of species has been proposed but not been tested critically. RESULTS: We reconstructed the phylogeny of a complex cichlid species flock confined to the tiny Cameroonian crater lake Barombi Mbo using both mitochondrial and nuclear (AFLP) data. The nuclear phylogeny confirms previous findings which suggested the monophyly and sympatric origin of the flock. However, discordant intra-flock phylogenies reconstructed from mitochondrial and nuclear data suggest strongly that secondary hybridization among lineages that primarily diverged under sympatric conditions had occurred. Using canonical phylogenetic ordination and tree-based tests we infer that hybridization of two ancient lineages resulted in the formation of a new and ecologically highly distinct species, Pungu maclareni. CONCLUSIONS: Our findings show that sympatric hybrid speciation is able to contribute significantly to the evolution of complex species assemblages even without the prior formation of hybrids derived from allopatrically differentiated lineages.     

Habitat use and ecological specialization within lake Daphnia populations

Many species of planktonic cladocerans display substantial variation in habitat use (mean depth and diel vertical migration), both among and within populations. We examined whether clonal segregation and specialization contributes to such behavioral variation within several lake populations of the cladoceran, Daphnia pulicaria. Electrophoretic and quantitative genetic analysis of clonal lines isolated from different depths at night revealed that clonal habitat specialization was common. Clones that utilized shallow water at night were genetically smaller at maturity and lower fecundity under standard laboratory conditions than the deep-water clones. The magnitude of this clonal habitat specialization varied among lakes: populations displaying broad use of depth habitats contained greater genetic variance than populations with more constrained habitat use. These results are consistent with known differences in selective factors in different depth habitats and suggest that substantial clonal specialization can occur within single populations. Since previous work has discovered a heritable basis to habitat selection in several Daphnia species, including D. pulicaria in our study lakes, it is likely that clonal/depth specialization is an important factor affecting the trophic ecology of Daphnia. Received: 18 April 1996 / Accepted: 25 September 1996     

Morphometric differentiation among haplochromine cichlid fish species of a satellite lake of Lake Victoria

Lake Victoria holds a young but species‐rich assemblage of cichlid fishes, which form a monophyletic assemblage with additional species from surrounding water bodies, termed the Lake Victoria superflock. Lake Victoria is surrounded by smaller lakes that are somewhat disconnected from the main lake. Lake Kanyaboli is such a small lake, having markedly reduced species diversity, in part comprised of Lake Victoria species and endemics. Here, we studied the modern haplochromine component of the cichlid fauna, represented by Lipochromis maxillaris, Astatotilapia nubila, Xystichromis phytophagus and Astatotilapia sp. ‘Bigeye’, as well as a number of unidentified modern haplochromine specimens. We used landmark‐based geometric morphometrics to study the degree of morphological divergence among those young entities. Twenty landmarks and 14 interlandmark distances were used for shape analysis. Multivariate analysis revealed significant differences between all four species, but principal component analysis and canonical variate analysis did not clearly discriminate between A. nubila and X. phytophagus, demonstrating great overall morphological similarity despite clear dietary differences. Besides coloration there was sexual dimorphism in body proportions, so that only male individuals were analysed further. In all four species, the observed similarities and differences in body shape conform to the type of ecological specialization of the fish. Most unidentified specimens overlapped the range of A. nubila and X. phytophagus, while the assignment test based on the canonical variate analysis suggested 70% of the three overlapping entities as separate units. To test their reproductive distinctness and to demonstrate potential hybridization, nuclear genetic data are needed.     

Weak disruptive selection and incomplete phenotypic divergence in two classic examples of sympatric speciation: cameroon crater lake cichlids

Abstract Recent documentation of a few compelling examples of sympatric speciation led to a proliferation of theoretical models. Unfortunately, plausible examples from nature have rarely been used to test model predictions, such as the initial presence of strong disruptive selection. Here I estimated the form and strength of selection in two classic examples of sympatric speciation: radiations of Cameroon cichlids restricted to Lakes Barombi Mbo and Ejagham. I measured five functional traits and relative growth rates in over 500 individuals within incipient species complexes from each lake. Disruptive selection was prevalent in both groups on single and multivariate trait axes but weak relative to stabilizing selection on other traits and most published estimates of disruptive selection. Furthermore, despite genetic structure, assortative mating, and bimodal species-diagnostic coloration, trait distributions were unimodal in both species complexes, indicating the earliest stages of speciation. Long waiting times or incomplete sympatric speciation may result when disruptive selection is initially weak. Alternatively, I present evidence of additional constraints in both species complexes, including weak linkage between coloration and morphology, reduced morphological variance aligned with nonlinear selection surfaces, and minimal ecological divergence. While other species within these radiations show complete phenotypic separation, morphological and ecological divergence in these species complexes may be slow or incomplete outside optimal parameter ranges, in contrast to rapid divergence of their sexual coloration.     

Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake

A recent study of a pair of sympatric species of cichlids in Lake Apoyo in Nicaragua is viewed as providing probably one of the most convincing examples of sympatric speciation to date. Here, we describe and study a stochastic, individual-based, explicit genetic model tailored for this cichlid system. Our results show that relatively rapid (<20,000 generations) colonization of a new ecological niche and (sympatric or parapatric) speciation via local adaptation and divergence in habitat and mating preferences are theoretically plausible if: (i) the number of loci underlying the traits controlling local adaptation, and habitat and mating preferences is small; (ii) the strength of selection for local adaptation is intermediate; (iii) the carrying capacity of the population is intermediate; and (iv) the effects of the loci influencing nonrandom mating are strong. We discuss patterns and timescales of ecological speciation identified by our model, and we highlight important parameters and features that need to be studied empirically to provide information that can be used to improve the biological realism and power of mathematical models of ecological speciation.     

A single mitochondrial haplotype and nuclear genetic differentiation in sympatric colour morphs of a riverine cichlid fish

Some of the diversity of lacustrine cichlid fishes has been ascribed to sympatric divergence, whereas diversification in rivers is generally driven by vicariance and geographic isolation. In the riverine Pseudocrenilabrus philander species complex, several morphologically highly distinct populations are restricted to particular river systems, sinkholes and springs in southern Africa. One of these populations consists of a prevalent yellow morph in sympatry with a less frequent blue morph, and no individuals bear intermediate phenotypes. Genetic variation in microsatellites and AFLP markers was very low in both morphs and one single mtDNA haplotype was fixed in all samples, indicating a very young evolutionary age and small effective population size. Nevertheless, the nuclear markers detected low but significant differentiation between the two morphs. The data suggest recent and perhaps sympatric divergence in the riverine habitat.     

Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon

Although there is mounting evidence that speciation can occur under sympatric conditions, unambiguous examples from nature are rare and it is almost always possible to propose alternative allopatric or parapatric scenarios. To identify an unequivocal case of sympatric speciation it is, therefore, necessary to analyse natural settings where recent monophyletic species flocks have evolved within a small and confined spatial range. We have studied such a case with a cichlid species flock that comprises five Tilapia forms endemic to a tiny lake (Lake Ejagham with a surface area of approximately 0.49 km2) in Western Cameroon. Analysis of mitochondrial D-Loop sequences shows that the flock is very young (approximately 10(4) years) and has originated from an adjacent riverine founder population. We have focused our study on a particular pair of forms within the lake that currently appears to be in the process of speciation. This pair is characterized by an unique breeding colouration and specific morphological aspects, which can serve as synapomorphic characters to prove monophyly. It has differentiated into a large inshore and a small pelagic form, apparently as a response to differential utilization of food resources. Still, breeding and brood care occurs in overlapping areas, both in time and space. Analysis of nuclear gene flow on the basis of microsatellite polymorphisms shows a highly restricted gene flow between the forms, suggesting reproductive isolation between them. This reproductive isolation is apparently achieved by size assortative mating, although occasional mixed pairs can be observed. Our findings are congruent with recent theoretical models for sympatric speciation, which show that differential ecological adaptations in combination with assortative mating could easily lead to speciation in sympatry.     

Alternative life-history styles of some African cichlid fishes

Synopsis About 50% of African cichlid species have been described. Little is known about cichlid ecology, behaviour or about the evolution and interactions of communities. Nevertheless, trends which provide an insight into cichlid life histories, into evolutionary alternatives and into behavioural alternatives which may be followed during the life time of these fishes are emerging. Cichlids which spend their entire life history in a single habitat belong to species flocks that have spectated greatly. In contrast, those groups which live in a variety of habitats during their life history have spectated little. Despite the trophic specializations that have occurred among cichlids, many and perhaps all species, have the ability to feed upon alternative food resources. They do so by switching or by markedly modifying their behaviour and all are particularly opportunistic. The extensive adaptive radiation of cichlids with regard to those attributes of morphology and behaviour that are associated with survival and growth, is apparently not matched by similar radiations in reproductive behaviour. The perceived evolutionary conservatism with regard to reproductive behaviour is attributed to the effects of stabilizing selection, but this still needs to be tested. The constraints of stabilizing selection appear to be lifted with regard to coloration. If colour is an important component of the specific-mate recognition system then it should also be subjected to stabilizing selection so the readiness with which colour variation occurs within and between populations needs explanation. Parental care in cichlids has followed a variety of evolutionary alternatives, all of which are geared to improve the chances of survival of offspring in their specific micro-habitats.     

Evolutionary history of Lake Tanganyika's scale-eating cichlid fishes

Although Lake Tanganyika is not the most species-rich of the Great East African Lakes it comprises by far the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. Our study focuses on the Tanganyikan cichlid tribe Perissodini, which exhibits one of the most peculiar feeding strategies found in cichlids-scale-eating. Their evolutionary history was reconstructed from 1416 bp DNA sequence of two mitochondrial genes (ND2 and partial control region) and from 612 AFLP markers. We confirm the inclusion of the zooplanktivorous genus Haplotaxodon in the tribe Perissodini, and species status of Haplotaxodon trifasciatus. Within the Perissodini, the major lineages emerged within a short period roughly 1.5-2 MYA, which makes their radiation slightly younger than that of other Tanganyikan cichlid tribes. Most scale-eaters evolved in deep-water habitat, perhaps associated with the previously documented radiations of other deep-water dwelling cichlid lineages, and colonized the shallow habitat only recently.     

Repeated parallel evolution of parental care strategies within Xenotilapia, a genus of cichlid fishes from Lake Tanganyika

The factors promoting the evolution of parental care strategies have been extensively studied in experiment and theory. However, most attempts to examine parental care in an evolutionary context have evaluated broad taxonomic categories. The explosive and recent diversifications of East African cichlid fishes offer exceptional opportunities to study the evolution of various life history traits based on species-level phylogenies. The Xenotilapia lineage within the endemic Lake Tanganyika cichlid tribe Ectodini comprises species that display either biparental or maternal only brood care and hence offers a unique opportunity to study the evolution of distinct parental care strategies in a phylogenetic framework. In order to reconstruct the evolutionary relationships among 16 species of this lineage we scored 2,478 Amplified Fragment Length Polymorphisms (AFLPs) across the genome. We find that the Ectodini genus Enantiopus is embedded within the genus Xenotilapia and that during 2.5 to 3 million years of evolution within the Xenotilapia clade there have been 3-5 transitions from maternal only to biparental care. While most previous models suggest that uniparental care (maternal or paternal) arose from biparental care, we conclude from our species-level analysis that the evolution of parental care strategies is not only remarkably fast, but much more labile than previously expected.     

Functional diversity in the color vision of cichlid fishes

Background  

Color vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed.     

Food resources of shrimp-eating cichlid fishes in Lake Tanganyika

Species, size composition, and diurnal variation in abundance of shrimp (Atyidae) were examined and compared with food habits of 14 species of shrimp-eating cichlids in Lake Tanganyika. In the daytime when the cichlids foraged actively, only one species of shrimp, Limnocaridina latipes, was present on rock surfaces. Eleven of the 14 species of shrimp-eaters examined preyed mainly on L. latipes; the shrimp-eaters foraging only on rock surfaces preyed exclusively on L. latipes, whereas shrimp-eaters also taking foods from the interstices between or under stones and debris preyed on various species of shrimp. Although three kinds of shrimp-eaters, each with a unique prey catching technique and preferred shrimp size, were recognized, all shrimp-eaters preyed on shrimp of greatly overlapping sizes. This fact confirms that partitioning of food resources takes place via different capturing techniques. Moreover, the utilization of the same food resource in a different manner may promote group foraging in some shrimp-eaters, because the shrimp is a suitable animal to hunt in groups and is a quickly renewable food of potential abundance.     

Phylogenetic analysis of cichlid fishes using nuclear DNA markers

The recent explosive adaptive radiation of cichlids in the great lakes of Africa has attracted the attention of both morphologists and molecular biologists. To decipher the phylogenetic relationships among the various taxa within the family Cichlidae is a prerequisite for answering some fundamental questions about the nature of the speciation process. In the present study, we used the random amplification of polymorphic DNA (RAPD) technique to obtain sequence differences between selected cichlid species. We then designed specific primers based on these sequences and used them to amplify template DNA from a large number of species by the polymerase chain reaction (PCR). We sequenced the amplified products and searched the sequences for indels and shared substitutions. We identified a number of such characters at three loci-- DXTU1, DXTU2, and DXTU3--and used them for phylogenetic and cladistic analysis of the relationships among the various cichlid groups. Our studies assign an outgroup position to Neotropical cichlids in relation to African cichlids, provide evidence for a sister-group relationship of tilapiines to the haplochromines, group Cyphotilapia frontosa with the lamprologines of Lake Tanganyika, place Astatoreochromis alluaudi to an outgroup position with respect to other haplochromines of Lakes Victoria and Malawi, and provide additional support for the monophyly of the remaining Lake Victoria haplochromines and the Lake Malawi haplochromines. The described approach holds great promise for further resolution of cichlid phylogeny.      

Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes)

The relationships among 53 genera of Tanganyikan cichlid fishes were analyzed based on internal and external morphological features. Comparison of the morphological cladistic tree with a previously proposed classification showed 5 of 12 tribes to be nonmonophyletic. Sixteen tribes were recognized, the changes in classification being that Trematocarini was treated as a junior synonym of Bathybatini; 5 new tribes were established for each of the following genera, Benthochromis, Boulengerochromis, Ctenochromis benthicola, Cyphotilapia, and Greenwoodochromis; Ctenochromis horei was transferred from Haplochromini to Tropheini; and Gnathochromis pfefferi was transferred from Limnochromini to Tropheini. The revised classification was supported by previously proposed molecular trees.     

Dissolved oxygen and thermal regimes of a Ugandan crater lake

This paper quantifies the temporal pattern of thermal stratification and deoxygenation in Lake Nkuruba, a small (3 ha), deep (maximum depth = 38 m) crater lake in western Uganda. Dissolved oxygen penetrated to an average depth of 9 m and a maximum depth of 15 m below which the lake was permanently anoxic over the 2 years of study. Although surface oxygen levels were correlated with both surface water temperature and rainfall, seasonal cycles of dissolved oxygen were not well-defined and may have been obscured by the high frequency of short-term fluctuations and by inter-annual variations caused by shifts in rainfall. Surface water temperature averaged 23.3±0.7 °C (S.D.) and varied directly with air temperature. Both diurnal changes and top-bottom temperature differentials were small averaging 1.7±0.7 °C and 1.6±0.8 °C, respectively. Thermal stability ranged from 101.3 to 499.9 g-cm cm^-2 and was positively related to surface water temperature suggesting that this small protected lake responds rapidly to short-term meteorological changes. Because contribution to the annual heat exchange cycle was confined to upper waters, the lake's annual heat budget was low, 1,073.8 cal cm^-2 yr^-1. However, net primary productivity was relatively high averaging 1.3 g C m^-2d^-1. The region where Lake Nkuruba is situated experienced a very strong earthquake (6.2 on the Richter scale) on 4 February, 1994. Subsequently, water levels dropped markedly in the lake, falling 3.14 m over a 5-month period. This revised version was published online in September 2006 with corrections to the Cover Date.