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PubMed1997

Molecular systematics of Middle American cichlid fishes and the evolution of trophic-types in 'Cichlasoma (Amphilophus)' and 'C. (Thorichthys)'.

The majority of Middle American cichlids are placed in the informal assemblage 'Cichlasoma.' The group is divided into eight sections which appear to be based primarily on trophic morphology. Although several members of 'Cichlasoma' have been used in ecomorphological, behavioral, and biogeographic studies, no phylogenetic hypotheses for the group exist. In an attempt to develop a better understanding of the phylogenetic relationships of 'cichlasomine' cichlids, we examined the evolution of the trophic specialization, substratum-sifting, in two sections, 'Cichlasoma (Thorichthys)' and 'C. (Amphilophus),' to determine whether the trait reflects common ancestry. We sequenced the complete mitochondrial cytochrome b gene for 19 cichlids representing six sections of 'Cichlasoma,' and representatives of other Neotropical Cichlidae. Additional cichlid, and noncichlid outgroup sequences were included for a total of 22 taxa. The molecular phylogeny supports the recognition of the section 'C. (Thoricthys)' as a natural group, and we place those cichlids in the genus Thorichthys. The phylogeny also depicts 'C. (Amphilophus)' as paraphyletic, with substratum-sifters and generalized predators forming separate nonsister clades. We recommend that the substratum-sifting clade of the section 'C. (Amphilophus)' be placed in the resurrected genus Astatheros. The generalized predator clade of 'C. (Amphilophus)' contains only two species, 'C. (A.) citrinellum' and 'C. (A.) labiatum,' which we place in the genus Amphilophus. The phylogenetic hypotheses generated indicate that the substratum-sifting genera Thorichthys and Amphilophus do not share a common ancestor. Reconstruction of the evolution of substratum-sifting is equivocal, requiring either the independent evolution of the trait on two separate occasions or its presence in a more inclusive clade and subsequent loss in nonsubstratum sifting species.

Americas↗

PubMed2003

Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes.

East African cichlid fishes represent one of the most striking examples of rapid and convergent evolutionary radiation among vertebrates. Models of ecological speciation would suggest that functional divergence in feeding morphology has contributed to the origin and maintenance of cichlid species diversity. However, definitive evidence for the action of natural selection has been missing. Here we use quantitative genetics to identify regions of the cichlid genome responsible for functionally important shape differences in the oral jaw apparatus. The consistent direction of effects for individual quantitative trait loci suggest that cichlid jaws and teeth evolved in response to strong, divergent selection. Moreover, several chromosomal regions contain a disproportionate number of quantitative trait loci, indicating a prominent role for pleiotropy or genetic linkage in the divergence of this character complex. Of particular interest are genomic intervals with concerted effects on both the length and height of the lower jaw. Coordinated changes in this area of the oral jaw apparatus are predicted to have direct consequences for the speed and strength of jaw movement. Taken together, our results imply that the rapid and replicative nature of cichlid trophic evolution is the result of directional selection on chromosomal packages that encode functionally linked aspects of the craniofacial skeleton.

Animals↗

PubMed1996

Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika.

The spectacularly diverse cichlid fish species flocks of the East African Rift Lakes have elicited much debate on the potential evolutionary mechanisms responsible for the origin of these adaptive radiations. An historical perspective on population structure may offer insights into the processes driving population differentiation and possibly speciation. Here, we examine mitochondrial DNA (mtDNA) sequence variation in two endemic species of rock-dwelling cichlids, Simochromis babaulti and S. diagramma, from Lake Tanganyika. Phylogeographic analyses were used to infer what factors might have been important in the genetic structuring of Simochromis populations. Patterns of mtDNA differentiation in Simochromis were compared to those of other rock-dwelling cichlids to distinguish between competing hypotheses concerning the processes underlying their evolution. In striking contrast to previous findings, populations of Simochromis, even those separated by up to 300 km, were found to share mitochondrial DNA haplotypes. There is no correspondence between mtDNA genealogies and the geographical distribution of populations. Only S. babaulti, but not S. diagramma was found to have a significant association between genetic and geographic distance. These phylogeographic patterns suggest that the evolutionary effects of abiotic and biotic factors shaping population genetic structure may differ substantially even among closely related species of rock-dwelling cichlids. Physical events and barriers to gene flow that are believed to have had a major impact on the geographical distribution and intralacustrine speciation of Tropheus do not seem to have equally strongly affected its close relative Simochromis. These findings emphasize that no single mechanism can be responsible for the formation of population structure, speciation, and the adaptive radiation of all cichlid fishes.

Africa, Eastern↗

PubMed1996

Hierarchical sensory guidance of mauthner-mediated escape responses in goldfish (Carassius auratus) and cichlids (Haplochromis burtoni).

Acoustically-evoked escape behaviors were compared between goldfish (Carassius auratus), a hearing specialist, and the cichlid Haplochromis burtoni, a hearing nonspecialist. Fish were startled with compressive and rarefying, stimuli presented alone or together, and with compressive pulses preceded by a visual cue or after exposure to cobalt, an inhibitor of lateral line-innervated neuromast hair cells. These acoustic startle stimuli can evoke Mauthner neuron firing and are similar to but weaker than those produced by a largemouth bass (Micropterus salmoides) feeding on guppies. When sound stimuli were presented alone, both species avoided the direction of either the compressive or rarefying stimulus. If a light preceded and was contralateral to the compressive sound pulse, goldfish continued to avoid the sound source; cichlids avoided the visual cue and turned toward the sound. Goldfish performance improved significantly when the visual cue was in the same direction as the sound source. Goldfish performance also improved significantly after exposure to 0.1 mmol l-1 cobalt solution for 24 hours before testing, but cichlids would not startle after cobalt acclimation. A compressive pulse presented to one side of a fish simultaneously with a rarefying pulse on the other side causes the entire fish to accelerate with the water current. This strongly and directly accelerates the ear but tends to reduce both the pressure changes transduced by the swimbladder and activation of the mechanosensory lateral line. In this test, goldfish reliably avoided the compressive pulse. Cichlids, however, randomly avoided either speaker polarity but significantly avoided the speaker which had a faster onset. With more closely matched speakers, cichlids also preferentially avoided the compressive stimulus. Thus, the primitive sensory condition for auditory activation and guidance of Mauthner-neuron-initiated escape responses may have evolved to detect the initially compressive sounds associated with ram-type predators.

Acoustic Stimulation↗

PubMed2005

Comparative phylogenetic analyses of the adaptive radiation of Lake Tanganyika cichlid fish: nuclear sequences are less homoplasious but also less informative than mitochondrial DNA.

Over 200 described endemic species make up the adaptive radiation of cichlids in Lake Tanganyika. This species assemblage has been viewed as both an evolutionary reservoir of old cichlid lineages and an evolutionary hotspot from which the modern cichlid lineages arose, seeding the adaptive radiations in Lakes Victoria and Malawi. Here we report on a phylogenetic analysis of Lake Tanganyika cichlids combining the previously determined sequences of the mitochondrial ND2 gene (1047 bp) with newly derived sequences of the nuclear RAG1 gene (approximately 700 bp of intron 2 and approximately 1100 bp of exon 3). The nuclear data-in agreement with mitochondrial DNA-suggest that Lake Tanganyika harbors several ancient lineages that did not undergo rampant speciation (e.g., Bathybatini, Trematocarini). We find strong support for the monophyly of the most species-rich Tanganyikan group, the Lamprologini, and we propose a new taxonomic group that we term the C-lineage. The Haplochromini and Tropheini both have an 11-bp deletion in the intron of RAG1, strongly supporting the monophyly of this clade and its derived position. Mapping the phylogenetically informative positions revealed that, for certain branches, there are six times fewer apomorphies in RAG1. However, the consistency index of these positions is higher compared to the mitochondrial ND2 gene. Nuclear data therefore provide, on a per-base pair basis, less but more reliable phylogenetic information. Even if in our case RAG1 has not provided as much phylogenetic information as we expected, we suggest that this marker might be useful in the resolution of the phylogeny of older groups.

Animals↗

PubMedDate not supplied

Retroposition of the AFC family of SINEs (short interspersed repetitive elements) before and during the adaptive radiation of cichlid fishes in Lake Malawi and related inferences about phylogeny.

Lake Malawi is home to more than 450 species of endemic cichlids, which provide a spectacular example of adaptive radiation. To clarify the phylogenetic relationships among these fish, we examined the presence and absence of SINEs (short interspersed repetitive elements) at orthologous loci. We identified six loci at which a SINE sequence had apparently been specifically inserted by retroposition in the common ancestor of all the investigated species of endemic cichlids in Lake Malawi. At another locus, unique sharing of a SINE sequence was evident among all the investigated species of endemic non-Mbuna cichlids with the exception of Rhamphochromis sp. The relationships were in good agreement with those deduced in previous studies with various different markers, demonstrating that the SINE method is useful for the elucidation of phylogenetic relationships among cichlids in Lake Malawi. We also characterized a locus that exhibited transspecies polymorphism with respect to the presence or absence of the SINE sequence among non-Mbuna species. This result suggests that incomplete lineage sorting and/or interspecific hybridization might have occurred or be occurring among the species in this group, which might potentially cause misinterpretation of phylogenetic data, in particular when a single-locus marker, such as a sequence in the mitochondrial DNA, is used for analysis.

Animals↗

PubMed2004

Mitochondrial phylogeny of the Cyprichromini, a lineage of open-water cichlid fishes endemic to Lake Tanganyika, East Africa.

We present a phylogeny of the Cyprichromini, a lineage of cichlid fishes from Lake Tanganyika, showing progressive adaptation towards pelagic life style. Our study is based upon three mitochondrial gene segments, 443 bp of the control region, 402 bp of the cytochrome b gene and the entire NADH dehydrogenase subunit 2 gene (1047 bp). The topologies obtained by different tree building methods subdivide the Cyprichromini into four distinct lineages: the Paracyprichromis-, the Cyprichromis zonatus-, the Cyprichromis microlepidotus-lineage, and a lineage comprising Cyprichromis pavo and Cyprichromis leptosoma. Our study thus corroborates the distinctness of C. zonatus which was recently described formally. Concerning ecology and mating behavior, a clear evolutionary trend towards progressive adaptation to the pelagic zone emerges during the evolution of the Cyprichromini. The linearized tree analysis further shows that the four lineages have split almost contemporaneously. The mean Kimura-2-parameter distance among the four lineages emerging from the primary radiation of the Cyprichromini amounts to 7.21% and is in close agreement to that previously found for the primary radiation of the tribe Tropheini (7.01%), a lineage of rock-dwelling cichlids endemic to Lake Tanganyika. To date, the influence of lake level fluctuations as promoters of diversification has been demonstrated only for rock-dwelling cichlids. Based on the agreement in temporary patterns of diversification, we suggest that Pleistocene lake level changes have left a similar genetic imprint in a group of cichlid fishes that progressively colonized the open water during their radiation.

Africa, Eastern↗

PubMedDate not supplied

The cusp of evolution and development: a model of cichlid tooth shape diversity.

Tooth shape is a hallmark of repeated evolutionary radiations among cichlid fishes from East Africa. Cusp shape and number vary both within populations and among closely related species with different feeding behaviors and ecologies. Here, we use histology and scanning electron microscopy to chart the developmental trajectory of tooth shape differences in fishes from Lake Malawi. We demonstrate that species with bi- or tricuspid adult (replacement) teeth initially possess a first-generation unicuspid dentition. Notably, the timing of turnover from first-generation to replacement teeth differs among species and is correlated with feeding ecology. Next, we use field data for cichlid species with adult unicuspid, bicuspid, and tricuspid teeth to demonstrate a strong and positive relationship between the number of teeth in a row and tooth shape. We discuss cichlid tooth ontogeny in the context of morphogenetic models designed to explain the developmental basis of tooth shape variation in mammals. We suggest that the dramatic differences in cichlid dentitions can be explained by variation in the expression of common activators and inhibitors acting at multiple stages of odontogenesis.

Animals↗

PubMed2005

Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies.

African cichlid fishes have repeatedly evolved highly specialized modes of feeding through adaptations of their oral jaws. Here, we explore the molecular genetic basis of the opening and closing lever mechanisms of the cichlid lower jaw, which have traditionally been used to describe the mechanics of feeding behavior in bony fishes. Quantitative genetic analyses demonstrate that the opening and closing mechanisms are genetically modular and therefore free to evolve independently. Bmp4 (bone morphogenetic protein 4) is one of two loci that segregate with the mechanical advantage of closing and that together account for >30% of the phenotypic variance in this trait. Species-specific differences in jaw shape are obvious early in cichlid larval development and are correlated with patterns of bmp4 expression in the mandibular primordium. When bmp4 is overexpressed in the obligate suction feeder Danio rerio, mandibular morphology exhibits specific transformations of opening and closing lever ratios. We conclude that patterns of morphological integration of the cichlid jaw reflect a balance among conflicting functional demands. Further, we demonstrate that bmp4 has the potential to alter mandibular morphology in a way that mimics adaptive variation among fish species.

Animals↗

PubMedDate not supplied

Genetic basis of adaptive shape differences in the cichlid head.

East African cichlids exhibit an extraordinary level of morphological diversity. Key to their success has been a dramatic radiation in trophic biology, which has occurred rapidly and repeatedly in different lakes. In this report we take the first step in understanding the genetic basis of differences in cichlid oral jaw design. We estimate the effective number of genetic factors that control differences in the cichlid head through a comprehensive morphological assessment of two Lake Malawi cichlid species and their F(1) and F(2) hybrid progeny. We estimate that between one and 11 factors underlie shape difference of individual bony elements. We show that many of the skeletal differences in the head and oral jaw apparatus are inherited together, suggesting a degree of pleiotropy in the genetic architecture of this character complex. Moreover, we find that cosegregation of shape differences in different elements corresponds to developmental, rather than functional, units.

Adaptation, Physiological↗

PubMed2006

Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays.

The evolution of cone opsin genes is characterized by a dynamic process of gene birth and death through gene duplication and loss. However, the forces governing the retention and death of opsin genes are poorly understood. African cichlid fishes have a range of ecologies, differing in habitat and foraging style, which make them ideal for examining the selective forces acting on the opsin gene family. In this work, we present data on the riverine cichlid, Oreochromis niloticus, which is an ancestral outgroup to the cichlid adaptive radiations in the Great African lakes. We identify 7 cone opsin genes with several instances of gene duplication. We also characterize the spectral sensitivities of these genes through reconstitution of visual pigments. Peak absorbances demonstrate that each tilapia cone opsin gene codes for a spectrally distinct visual pigment: SWS1 (360 nm), SWS2b (423 nm), SWS2a (456 nm), Rh2b (472 nm), Rh2a beta (518 nm), Rh2a alpha (528 nm), and LWS (561 nm). Furthermore, quantitative reverse transcription polymerase chain reaction at 3 ontogenetic time points demonstrates that although only 4 genes (SWS2a, Rh2a alpha and beta, and LWS) are expressed in adults, mRNAs for the other genes are all expressed during ontogeny. Therefore, subfunctionalization through differential ontogenetic expression may be a key mechanism for preservation of opsin genes. The distinct peak absorbances of these preserved opsin genes provide a palette from which selection creates the diverse visual sensitivities found among the cichlid species of the lacustrine adaptive radiations.

Animals↗

PubMed2005

Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation.

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single-gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.

Animals↗

PubMed2004

Population-structure and genetic diversity in a haplochromine cichlid fish [corrected] of a satellite lake of Lake Victoria.

The approximately 500 species of the cichlid fish species flock of Lake Victoria, East Africa, have evolved in a record-setting 100,000 years and represent one of the largest adaptive radiations. We examined the population structure of the endangered cichlid species Xystichromis phytophagus from Lake Kanyaboli, a satellite lake to Lake Victoria in the Kenyan Yala wetlands. Two sets of molecular markers were analysed--sequences of the mitochondrial control region as well as six microsatellite loci--and revealed surprisingly high levels of genetic variability in this species. Mitochondrial DNA sequences failed to detect population structuring among the three sample populations. A model-based population assignment test based on microsatellite data revealed that the three populations most probably aggregate into a larger panmictic population. However, values of population pairwise FST indicated moderate levels of genetic differentiation for one population. Eleven distinct mitochondrial haplotypes were found among 205 specimens of X. phytophagus, a relatively high number compared to the total number of 54 haplotypes that were recovered from hundreds of specimens of the entire cichlid species flock of Lake Victoria. Most of the X. phytophagus mitochondrial DNA haplotypes were absent from the main Lake Victoria, corroborating the putative importance of satellite lakes as refugia for haplochromine cichlids that went extinct from the main lake in the last decades and possibly during the Late Pleistocene desiccation of Lake Victoria.

Animals↗

PubMed2003

Origin of the superflock of cichlid fishes from Lake Victoria, East Africa.

Lake Victoria harbors a unique species-rich flock of more than 500 endemic haplochromine cichlid fishes. The origin, age, and mechanism of diversification of this extraordinary radiation are still debated. Geological evidence suggests that the lake dried out completely about 14,700 years ago. On the basis of phylogenetic analyses of almost 300 DNA sequences of the mitochondrial control region of East African cichlids, we find that the Lake Victoria cichlid flock is derived from the geologically older Lake Kivu. We suggest that the two seeding lineages may have already been lake-adapted when they colonized Lake Victoria. A haplotype analysis further shows that the most recent desiccation of Lake Victoria did not lead to a complete extinction of its endemic cichlid fauna and that the major lineage diversification took place about 100,000 years ago.

Africa, Eastern↗

PubMed2005

Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes.

BACKGROUND: The adaptive radiations of cichlid fishes in East Africa are well known for their spectacular diversity and their astonishingly fast rates of speciation. About 80% of all 2,500 cichlid species in East Africa, and virtually all cichlid species from Lakes Victoria (approximately 500 species) and Malawi (approximately 1,000 species) are haplochromines. Here, we present the most extensive phylogenetic and phylogeographic analysis so far that includes about 100 species and is based on about 2,000 bp of the mitochondrial DNA. RESULTS: Our analyses revealed that all haplochromine lineages are ultimately derived from Lake Tanganyika endemics. We find that the three most ancestral lineages of the haplochromines sensu lato are relatively species poor, albeit widely distributed in Africa, whereas a fourth newly defined lineage - the 'modern haplochromines' - contains an unparalleled diversity that makes up more than 7% of the worlds' approximately 25,000 teleost species. The modern haplochromines' ancestor, most likely a riverine generalist, repeatedly gave rise to similar ecomorphs now found in several of the species flocks. Also, the Tanganyikan Tropheini are derived from that riverine ancestor suggesting that they successfully re-colonized Lake Tanganyika and speciated in parallel to an already established cichlid adaptive radiation. In contrast to most other known examples of adaptive radiations, these generalist ancestors were derived from highly diverse and specialized endemics from Lake Tanganyika. A reconstruction of life-history traits revealed that in an ancestral lineage leading to the modern haplochromines the characteristic egg-spots on anal fins of male individuals evolved. CONCLUSION: We conclude that Lake Tanganyika is the geographic and genetic cradle of all haplochromine lineages. In the ancestors of the replicate adaptive radiations of the 'modern haplochromines', behavioral (maternal mouthbrooding), morphological (egg-spots) and sexually selected (color polymorphism) key-innovations arose. These might be - together with the ecological opportunity that the habitat diversity of the large lakes provides - responsible for their evolutionary success and their propensity for explosive speciation.

Animals↗

PubMed1994

Intra- and interspecific mitochondrial DNA sequence variation within two species of rock-dwelling cichlids (Teleostei: Cichlidae) from Lake Malawi, Africa.

Difficulties in interpreting the evolutionary significance of Lake Malawi cichlid morphologies led us to examine molecular techniques for resolving relationships among closely related species. Mitochondrial DNA (mtDNA) sequence variation in the first half of the control region (445 bp) was examined within and between two species of Melanochromis, a genus of rock-dwelling cichlids from Lake Malawi, Africa. The mean number of pairwise differences observed within Melanochromis auratus (Boulenger) and Melanochromis heterochromis Bowers and Stauffer mtDNA haplotypes was 2.0 (0.45%) and 5.0 (1.13%), respectively, and a mean of 4.9 (1.11%) pairwise differences between the two species was observed. Mean pairwise differences between Melanochromis species and Pseudotropheus zebra (Boulenger), another species of rock-dwelling cichlid and Tramitichromis cf. liturus, a sand-dwelling genus, were 11.2 (2.52%) and 21.9 (4.93%), respectively. Species divergence and radiation within the genus Melanochromis appears to have occurred rapidly and recently. Mitochondrial DNA sequence variation within this genus was sufficient for generating hypotheses concerning the evolutionary relationships within the genus and for examining generic-level relationships within and among the major cichlid lineages in Lake Malawi.

Africa↗

PubMed2000

Visual pigments of African cichlid fishes: evidence for ultraviolet vision from microspectrophotometry and DNA sequences.

We have found evidence for ultraviolet visual capabilities in a Lake Malawi cichlid fish, Metriaclima zebra. Microspectrophotometry of single cones revealed a visual pigment with peak sensitivity at 368+/-4 nm. M. zebra also expresses a putative ultraviolet opsin gene whose sequence is closely related to the SWS-1 opsin for other fishes. Several other African cichlids have a functional copy of this UV gene in their genomic DNA, but do not appear to express this gene as adults. These results suggest that ultraviolet vision is important for some cichlid fishes. UV wavelengths should therefore be included in future studies of cichlid vision, behavior and color patterns.

Amino Acid Sequence↗

PubMed2005

An extant cichlid fish radiation emerged in an extinct Pleistocene lake.

The haplochromine cichlid fish of the East African Great Lakes represent some of the fastest and most species-rich adaptive radiations known, but rivers in most of Africa accommodate only a few morphologically similar species of haplochromine cichlid fish. This has been explained by the wealth of ecological opportunity in large lakes compared with rivers. It is therefore surprising that the rivers of southern Africa harbour many, ecologically diverse haplochromines. Here we present genetic, morphological and biogeographical evidence suggesting that these riverine cichlids are products of a recent adaptive radiation in a large lake that dried up in the Holocene. Haplochromine species richness peaks steeply in an area for which geological data reveal the historical existence of Lake palaeo-Makgadikgadi. The centre of this extinct lake is now a saltpan north of the Kalahari Desert, but it once hosted a rapidly evolving fish species radiation, comparable in morphological diversity to that in the extant African Great Lakes. Importantly, this lake seeded all major river systems of southern Africa with ecologically diverse cichlids. This discovery reveals how local evolutionary processes operating during a short window of ecological opportunity can have a major and lasting effect on biodiversity on a continental scale.

Africa, Southern↗