The Adaptive Radiation of Cichlid Fish in Lake Tanganyika: A Morphological Perspective

Lake Tanganyika is the oldest of the Great Ancient Lakes in the East Africa. This lake harbours about 250 species of cichlid fish, which are highly diverse in terms of morphology, behaviour, and ecology. Lake Tanganyika's cichlid diversity has evolved through explosive speciation and is treated as a textbook example of adaptive radiation, the rapid differentiation of a single ancestor into an array of species that differ in traits used to exploit their environments and resources. To elucidate the processes and mechanisms underlying the rapid speciation and adaptive radiation of Lake Tanganyika's cichlid species assemblage it is important to integrate evidence from several lines of research. Great efforts have been, are, and certainly will be taken to solve the mystery of how so many cichlid species evolved in so little time. In the present review, we summarize morphological studies that relate to the adaptive radiation of Lake Tanganyika's cichlids and highlight their importance for understanding the process of adaptive radiation

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

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

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

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

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

Preface: Advances in Cichlid Research V:Behavior, Ecology, and Evolutionary Biology

The current special issue is the fifth in a series of special issues published in Hydrobiologia exclusively devoted to cichlid fish research. The freshwater fish family Cichlidae accounts for approximately 10% of today’s teleost diversity and is naturally distributed from southern North America to southern South America, across most of Africa, to Madagascar and India. Their tremendous diversity in morphology, behavior, and ecology, as well as their astounding speciation rates and numerous species-rich adaptive radiations have enthralled biologists for decades (e.g., Boulenger, 1898; Kosswig, 1947; Fryer, 1960), such that cichlids are now among the prime model systems in evolutionary biology research (e.g., Salzburger, 2018). We are pleased to present a collection of 19 papers that investigate questions of taxonomy, biogeography, morphology, behavior, physiology, and parasitology. Many of the key ingredients of cichlid diversification are addressed by these studies, including mating, brood care and social interactions, color pattern, and body shape, as well as adaptations of the visual system and the trophic apparatus. Papers are summarized below in the order in which they appear in this special issue. We hope you enjoy reading the contributions

Plant species effects on soil macrofauna density in grassy arable fallows of different age

AbstractThe density of soil macrofauna groups in nine grassy arable fallows of different age were investigated in a factorial design with the factors ‘plant species’ (legume: Medicago sativa, herb: Taraxacum officinale, grass: Bromus sterilis) and ‘age class’ (A1: 2–3/3–4, A2: 6–8/7–9, A3: 12–15/13–16 years in 2008/2009). Four plots were selected randomly at each fallow. In May 2008 and May 2009, within each plot five M. sativa, T. officinale and B. sterilis plants were extracted with their associated soil using steel cylinders. The material from each plant species was used for extraction of soil macrofauna and for determination of environmental parameters.The main results were (i) the density of the saprophagous macrofauna was significantly higher in B. sterilis than in M. sativa and T. officinale samples indicating that this group possibly benefited from the particularly high amount of fine roots in the B. sterilis samples; (ii) densities of Gastropoda and predatory beetles were highest in the 7–9yr old fallows indicating that predators may have benefited from the increased availability of their prey in the medium stage of grassland succession; (iii) focusing on the results of the CCAs (2008, 2009), the water content had the strongest influence of the measured soil parameters on the structure of the soil macrofauna assemblages

Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika – the result of repeated introgressive hybridization

BACKGROUND: The tribe Lamprologini is the major substrate breeding lineage of Lake Tanganyika's cichlid species flock. Among several different life history strategies found in lamprologines, the adaptation to live and breed in empty gastropod shells is probably the most peculiar. Although shell-breeding arose several times in the evolutionary history of the lamprologines, all obligatory and most facultative shell-breeders belong to the so called "ossified group", a monophyletic lineage within the lamprologine cichlids. Since their distinctive life style enables these species to live and breed in closest vicinity, we hypothesized that these cichlids might be particularly prone to accidental hybridization, and that introgression might have affected the evolutionary history of this cichlid lineage. RESULTS: Our analyses revealed discrepancies between phylogenetic hypotheses based on mitochondrial and nuclear (AFLP) data. While the nuclear phylogeny was congruent with morphological, behavioral and ecological characteristics, several species – usually highly specialized shell-breeders – were placed at contradicting positions in the mitochondrial phylogeny. The discordant phylogenies strongly suggest repeated incidents of introgressive hybridization between several distantly related shell-breeding species, which reticulated the phylogeny of this group of cichlids. Long interior branches and high bootstrap support for many interior nodes in the mitochondrial phylogeny argue against a major effect of ancient incomplete lineage sorting on the phylogenetic reconstruction. Moreover, we provide morphological and genetic (mtDNA and microsatellites) evidence for ongoing hybridization among distantly related shell-breeders. In these cases, the territorial males of the inferred paternal species are too large to enter the shells of their mate, such that they have to release their sperm over the entrance of the shell to fertilize the eggs. With sperm dispersal by water currents and wave action, trans-specific fertilization of clutches in neighboring shells seem inevitable, when post-zygotic isolation is incomplete. CONCLUSION: From the direct observation of hybrids we conclude that hybridization between distantly related gastropod-shell-breeding cichlids of Lake Tanganyika follows inevitably from their ecological specialization. Moreover, the observed incongruence between mtDNA and nuclear multilocus phylogeny suggests that repeated hybridization events among quite distantly related taxa affected the diversification of this group, and introduced reticulation into their phylogeny