The Utility of Geometric Morphometrics to Elucidate Pathways of Cichlid Fish Evolution

Fishes of the family Cichlidae are famous for their spectacular species flocks and therefore constitute a model system for the study of the pathways of adaptive radiation. Their radiation is connected to trophic specialization, manifested in dentition, head morphology, and body shape. Geometric morphometric methods have been established as efficient tools to quantify such differences in overall body shape or in particular morphological structures and meanwhile found wide application in evolutionary biology. As a common feature, these approaches define and analyze coordinates of anatomical landmarks, rather than traditional counts or measurements. Geometric morphometric methods have several merits compared to traditional morphometrics, particularly for the distinction and analysis of closely related entities. Cichlid evolutionary research benefits from the efficiency of data acquisition, the manifold opportunities of analyses, and the potential to visualize shape changes of those landmark-based methods. This paper briefly introduces to the concepts and methods of geometric morphometrics and presents a selection of publications where those techniques have been successfully applied to various aspects of cichlid fish diversification

Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus

<p>Abstract</p> <p>Background</p> <p>Cichlid fishes are notorious for their wealth of intra- and interspecific colour pattern diversity. In Lake Tanganyika, the endemic genus <it>Tropheus </it>represents the most impressive example for geographic variation in the pattern and hue of integument colouration, but the taxonomy of the over 100 mostly allopatric colour morphs remains to a large degree unresolved. Previous studies of mitochondrial DNA sequence data revealed polyphyly of the six nominally described species and complex phylogeographic patterns influenced by lake level fluctuations and population admixture, and suggested the parallel evolution of similar colour patterns in divergent evolutionary lineages. A gene tree of a rapidly radiating group may be subject to incomplete and stochastic lineage sorting, and to overcome this problem we used multi-locus, nuclear AFLP data in comparison with mtDNA sequences to study diversification, migration and introgression in <it>Tropheus </it>colour morphs in Lake Tanganyika.</p> <p>Results</p> <p>Significant incongruence between phylogenetic reconstructions from mitochondrial and AFLP data suggested incomplete sorting of mitochondrial haplotypes as well as frequent introgression between differentiated lineages. In contrast to the mitochondrial phylogeny, the AFLP phenogram was largely congruent with species classifications, colour pattern similarities, and in many cases also with the current geographic distribution of populations, and did not produce evidence of convergent colour pattern evolution. Homoplasy in the AFLP data was used to identify populations that were strongly affected by introgression.</p> <p>Conclusion</p> <p>Different evolutionary processes were distinguished by the combination of mitochondrial and AFLP data. Mitochondrial phylogeographic patterns retained signals of large-scale migration events triggered by historical, major lake level fluctuations, whereas AFLP data indicated genetic cohesion among local groups of populations resulting from secondary contact of adjacent populations in the course of the more frequently occurring, minor lake level fluctuations. There was no support for the parallel evolution of similar colour patterns in the AFLP data. Genetic signatures of introgression and hybridisation detected in several populations suggest that lake level fluctuations drove the stunning diversification of <it>Tropheus </it>morphs not only through population fragmentation, but also by promoting hybridisation between differentiated morphs in secondary contact.</p

Morphological distinctness despite large-scale phenotypic plasticity—analysis of wild and pond-bred juveniles of allopatric populations of Tropheus moorii

Cichlids are an excellent model to study explosive speciation and adaptive radiation. Their evolutionary success has been attributed to their ability to undergo rapid morphological changes related to diet, and their particular breeding biology. Relatively minor changes in morphology allow for exploitation of novel food resources. The importance of phenotypic plasticity and genetically based differences for diversification was long recognized, but their relationship and relative magnitude remained unclear. We compared morphology of individuals of four wild populations of the Lake Tanganyika cichlid Tropheus moorii with their pond-raised F1 offspring. The magnitude of morphological change via phenotypic plasticity between wild and pond-bred F1 fish exceeds pairwise population differences by a factor of 2.4 (mean Mahalanobis distances). The genetic and environmental effects responsible for among population differentiation in the wild could still be recognized in the pond-bred F1 fish. All four pond populations showed the same trends in morphological change, mainly in mouth orientation, size and orientation of fins, and thickness of the caudal peduncle. As between population differentiation was lower in the wild than differentiation between pond-raised versus wild fish, we suggest the narrow ecological niche and intense interspecific competition in rock habitats is responsible for consistent shape similarity, even among long-term isolated populations

Ancestral state reconstruction reveals multiple independent evolution of diagnostic morphological characters in the "Higher Oribatida" (Acari), conflicting with current classification schemes

<p>Abstract</p> <p>Background</p> <p>The use of molecular genetic data in phylogenetic systematics has revolutionized this field of research in that several taxonomic groupings defined by traditional taxonomic approaches have been rejected by molecular data. The taxonomic classification of the oribatid mite group Circumdehiscentiae ("Higher Oribatida") is largely based on morphological characters and several different classification schemes, all based upon the validity of diagnostic morphological characters, have been proposed by various authors. The aims of this study were to test the appropriateness of the current taxonomic classification schemes for the Circumdehiscentiae and to trace the evolution of the main diagnostic traits (the four nymphal traits scalps, centrodorsal setae, sclerits and wrinkled cuticle plus octotaxic system and pteromorphs both in adults) on the basis of a molecular phylogenetic hypothesis by means of parsimony, likelihood and Bayesian approaches.</p> <p>Results</p> <p>The molecular phylogeny based on three nuclear markers (28S rDNA, <it>ef-1α</it>, <it>hsp82</it>) revealed considerable discrepancies to the traditional classification of the five "circumdehiscent" subdivisions, suggesting paraphyly of the three families Scutoverticidae, Ameronothridae, Cymbaeremaeidae and also of the genus <it>Achipteria</it>. Ancestral state reconstructions of six common diagnostic characters and statistical evaluation of alternative phylogenetic hypotheses also partially rejected the current morphology-based classification and suggested multiple convergent evolution (both gain and loss) of some traits, after a period of rapid cladogenesis, rendering several subgroups paraphyletic.</p> <p>Conclusions</p> <p>Phylogenetic studies revealed non-monophyly of three families and one genus as a result of a lack of adequate synapomorphic morphological characters, calling for further detailed investigations in a framework of integrative taxonomy. Character histories of six morphological traits indicate that their evolution followed a rather complex pattern of multiple independent gains (and losses). Thus, the observed pattern largely conflicts with current morphological classifications of the Circumdehiscentiae, suggesting that the current taxonomic classification schemes are not appropriate, apart from a recently proposed subdivision into 24 superfamilies.</p

Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: Synodontis)

BACKGROUND: Squeaker catfishes (Pisces, Mochokidae, Synodontis) are widely distributed throughout Africa and inhabit a biogeographic range similar to that of the exceptionally diverse cichlid fishes, including the three East African Great Lakes and their surrounding rivers. Since squeaker catfishes also prefer the same types of habitats as many of the cichlid species, we hypothesized that the East African Synodontis species provide an excellent model group for comparative evolutionary and phylogeographic analyses. RESULTS: Our analyses reveal the existence of six major lineages of Synodontis in East Africa that diversified about 20 MYA from a Central and/or West African ancestor. The six lineages show a clear geographic patterning. Two lineages are endemic to Lake Tanganyika (plus one non-endemic representative), and these are the only two Synodontis lineages that diversified further into a small array of species. One of these species is the cuckoo catfish (S. multipunctatus), a unique brood parasite of mouthbrooding haplochromine cichlids, which seems to have evolved in parallel with the radiation of its cichlid host lineage, the Tropheini. We also detect an accelerated rate of molecular evolution in S. multipunctatus, which might be the consequence of co-evolutionary dynamics. CONCLUSION: We conclude that the ancestral lineage of today's East African squeaker catfish fauna has colonized the area before the Great Lakes have formed. This ancestor diversified rapidly into at least six lineages that inhabit lakes and rivers in East Africa. Lake Tanganyika is the only lake harboring a small species flock of squeaker catfishes

Evolutionary History of Lake Tanganyika's Predatory Deepwater Cichlids

Hybridization among littoral cichlid species in Lake Tanganyika was inferred in several molecular phylogenetic studies. The phenomenon is generally attributed to the lake level-induced shoreline and habitat changes. These allow for allopatric divergence of geographically fragmented populations alternating with locally restricted secondary contact and introgression between incompletely isolated taxa. In contrast, the deepwater habitat is characterized by weak geographic structure and a high potential for gene flow, which may explain the lower species richness of deepwater than littoral lineages. For the same reason, divergent deepwater lineages should have evolved strong intrinsic reproductive isolation already in the incipient stages of diversification, and, consequently, hybridization among established lineages should have been less frequent than in littoral lineages. We test this hypothesis in the endemic Lake Tanganyika deepwater cichlid tribe Bathybatini by comparing phylogenetic trees of Hemibates and Bathybates species obtained with nuclear multilocus AFLP data with a phylogeny based on mitochondrial sequences. Consistent with our hypothesis, largely congruent tree topologies and negative tests for introgression provided no evidence for introgressive hybridization between the deepwater taxa. Together, the nuclear and mitochondrial data established a well-supported phylogeny and suggested ecological segregation during speciation

Introgressive Hybridization between Color Morphs in a Population of Cichlid Fishes Twelve Years after Human-Induced Secondary Admixis

In the extremely species-rich haplochromine cichlid fishes of the East African Great Lakes, prezygotic isolation between closely related species is often maintained by color-assortative mating. In 1998, local fisherman working for the ornamental fish trade released different color morphs of the cichlid genus Tropheus into a small harbor basin in the southern part of Lake Tanganyika. This artificial amalgamation of color morphs provides a unique possibility to study mating patterns in cichlids in a natural environment over time. In a precursor study, we analyzed genotypes and phenotypes of almost 500 individuals sampled between 1999 and 2001 and uncovered a marked degree of color-assortative mating, which depended on the level of color pattern dissimilarity between morphs. Twelve years after introduction of nonindigenous morphs, we again sampled Tropheus individuals from the harbor basin and an adjacent, originally pure population and analyzed phenotypes (coloration) and genotypes (mitochondrial control region and 9 microsatellite loci) to assess the current status of the admixed population. Principal component analyses of color score data and population assignment tests demonstrate an increasing level of introgressive hybridization between morphs but also some ongoing color-assortative mating within morphs. The observed mating pattern might have been influenced by fluctuating environmental conditions such as periodic algal blooms or increased sedimentation causing turbid conditions in an otherwise clear lak

Population dynamics with a mixed type of sexual and asexual reproduction in a fluctuating environment

<p>Abstract</p> <p>Background</p> <p><it>Carassius gibelio</it>, a cyprinid fish from Eurasia, has the ability to reproduce both sexually and asexually. This fish is also known as an invasive species which colonized almost all continental Europe, most likely originating from Asia and Eastern Europe. Populations of both sexually and asexually reproducing individuals exist in sympatry. In this study we try to elucidate the advantages of such a mixed type of reproduction. We investigate the dynamics of two sympatric populations with sexual and asexual reproduction in a periodically fluctuating environment. We define an individual-based computational model in which genotypes are represented by <it>L </it>loci, and the environment is composed of <it>L </it>resources for which the two populations compete.</p> <p>Results</p> <p>Our model demonstrates advantageous population dynamics where the optimal percentage of asexual reproduction depends on selection strength, on the number of selected loci and on the timescale of environmental fluctuations. We show that the sexual reproduction is necessary for "generating" fit genotypes, while the asexual reproduction is suitable for "amplifying" them. The simulations show that the optimal percentage of asexual reproduction increases with the length of the environment stability period and decrease with the strength of the selection and the number of loci.</p> <p>Conclusions</p> <p>In this paper we addressed the advantages of a mixed type of sexual and asexual reproduction in a changing environment and explored the idea that a species that is able to adapt itself to environmental fluctuation can easily colonize a new habitat. Our results could provide a possible explanation for the rapid and efficient invasion of species with a variable ratio of sexual and asexual reproduction such as <it>Carassius gibelio</it>.</p

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

Expression variations in ectodysplasin-A gene (eda) may contribute to morphological divergence of scales in haplochromine cichlids

Background Elasmoid scales are one of the most common dermal appendages and can be found in almost all species of bony fish differing greatly in their shape. Whilst the genetic underpinnings behind elasmoid scale development have been investigated, not much is known about the mechanisms involved in moulding of scales. To investigate the links between gene expression differences and morphological divergence, we inferred shape variation of scales from two different areas of the body (anterior and posterior) stemming from ten haplochromine cichlid species from different origins (Lake Tanganyika, Lake Malawi, Lake Victoria and riverine). Additionally, we investigated transcriptional differences of a set of genes known to be involved in scale development and morphogenesis in fish. Results We found that scales from the anterior and posterior part of the body strongly differ in their overall shape, and a separate look on scales from each body part revealed similar trajectories of shape differences considering the lake origin of single investigated species. Above all, nine as well as 11 out of 16 target genes showed expression differences between the lakes for the anterior and posterior dataset, respectively. Whereas in posterior scales four genes (dlx5, eda, rankl and shh) revealed significant correlations between expression and morphological differentiation, in anterior scales only one gene (eda) showed such a correlation. Furthermore, eda displayed the most significant expression difference between species of Lake Tanganyika and species of the other two younger lakes. Finally, we found genetic differences in downstream regions of eda gene (e.g., in the eda-tnfsf13b inter-genic region) that are associated with observed expression differences. This is reminiscent of a genetic difference in the eda-tnfsf13b inter-genic region which leads to gain or loss of armour plates in stickleback. Conclusion These findings provide evidence for cross-species transcriptional differences of an important morphogenetic factor, eda, which is involved in formation of ectodermal appendages. These expression differences appeared to be associated with morphological differences observed in the scales of haplochromine cichlids indicating potential role of eda mediated signal in divergent scale morphogenesis in fish.Peer reviewe