East African cichlid fishes

Abstract

Cichlid fishes are a very diverse and species-rich family of teleost fishes that inhabit lakes and rivers of India, Africa, and South and Central America. Research has largely focused on East African cichlids of the Rift Lakes Tanganyika, Malawi, and Victoria that constitute the biodiversity hotspots of cichlid fishes. Here, we give an overview of the study system, research questions, and methodologies. Research on cichlid fishes spans many disciplines including ecology, evolution, physiology, genetics, development, and behavioral biology. In this review, we focus on a range of organismal traits, including coloration phenotypes, trophic adaptations, appendages like fins and scales, sensory systems, sex, brains, and behaviors. Moreover, we discuss studies on cichlid phylogenies, plasticity, and general evolutionary patterns, ranging from convergence to speciation rates and the proximate and ultimate mechanisms underlying these processes. From a methodological viewpoint, the last decade has brought great advances in cichlid fish research, particularly through the advent of affordable deep sequencing and advances in genetic manipulations. The ability to integrate across traits and research disciplines, ranging from developmental biology to ecology and evolution, makes cichlid fishes a fascinating research system.

Fig. 1

Evolution and Development of East African cichlid fishes. A Representatives of East African cichlids for which genomic information is available (Note: the Astatotilapia genus contains multiple paraphyletic species and is therefore found in both Lake Malawi and Lake Tanganyika). B Simplified phylogeny of East African cichlids with the radiations of Lakes Tanganyika (green), Malawi (blue), and Victoria (orange). C Life cycle of a substrate-brooding cichlid from Lake Tanganyika (Julidochromis ornatus) and a mouth-brooding, haplochromine cichlid from Lake Malawi (Melanochromis auratus). Photo credits: Ralf Schneider (A. burtoni in A)

Fig. 2

Habitat of East African rift lake cichlid fishes. A–C Lakes Victoria (A), Malawi (B), and Tanganyika (C) are the hotspots of cichlid fish diversity with over 1200 mostly endemic species. D–F The waters of the three large rift lakes largely differ in visibility, with Lake Victoria being quite turbid (D) and Lake Tanganyika (F) and especially Lake Malawi (E) being much clearer. Note that the shown habitats are not fully representative of the rich diversity of lake habitats. Photo credits: Joanna Meier and Florian Moser (A, D), Hannes Svardal (B, E), Leo Lorber (C, F)

Fig. 3

Laboratory culture. A Example of a cichlid fish facility with 240-L aquaria and a zebrafish rack for raising juveniles (right) (University of Helsinki). B An Astatotilapia calliptera male with hiding tubes and an egg tumbler for raising embryos and juveniles (University of Cambridge)

Fig. 4

Coloration phenotypes in cichlid fishes. A Horizontal stripe patterns in Melanochromis auratus (stripes). B Vertical bar patterns and egg-spots in Maylandia zebra. C Spot patterns in Otopharynx sp. “heterodon nankhumba”. D The orange blotch (OB) phenotype in Labeotropheus trewavasae. E Amelanism in Maylandia callainos. F Sexual dimorphism in Pseudotropheus saulosi with a blue male and yellow female. Photo credits: Hannes Svardal (A–E), Muktai Kuwalekar (F)

Fig. 5

Axes of divergence in cichlid fishes. A selection of phenotypic traits and their variation in cichlid fishes. For example, highly diverse traits include trophic adaptations such as head shape (including the evolution of hypertrophied lips in crevice-feeding insect eaters) and teeth and jaw variation. Moreover, cichlids exhibit great variation in body shapes and fin morphology and variation in color patterns (including egg-spots) and behaviors, such as mating rituals and social behaviors

Fig. 6

From cichlid phenotypes to genotypes to functional validation. Over the last decade, cichlid fishes have become a prime model to study genotype–phenotype relationships. The ability to collect samples from the field and to conduct hybrid crosses (even between species) makes it possible to identify the genetic bases of traits using genome-wide association (GWA) mapping and qualitative/quantitative trait loci (QTL) mapping, respectively. In combination with other methodologies (especially approaches that include functional validation) candidate genes and mutations can be identified and functionally validated as genes underlying phenotypic variation. Note that for simplicity a simple (qualitative) trait was used in this figure; both analyses can be and are also performed with complex (quantitative) traits

Fig. 7

Genetic manipulation techniques. A–C Over the last two decades, techniques such as Tol2 transgenesis and CRISPR–Cas9 genome editing have been successfully adapted in cichlid fishes. A challenge compared to traditional model teleost fishes (such as zebrafish and medaka) is the small number of eggs per clutch (usually 15–50 eggs), the oval egg shape, and the difficulty in timing fertilization. As in zebrafish, eggs are microinjected using an air pressure-driven microinjector (A). Eggs can be held with forceps or put into a supporting agarose mold (B). After microinjection, eggs are kept individually in well plates until larvae are free swimming (C). Photo credits: Bettina Fischer (B)

Fig. 8

Experimental and phenotyping approaches in cichlids. (A–I) A wide variety of methodological approaches, including methods available in cichlid fishes that are comparable to other teleost fish model systems. These include methods for genetic manipulations (A–C), gene expression and protein localization (D–F), and phenotyping in embryos and adults G, H. A Transgenic cichlid fish of the species Astatotilapia burtoni constitutively expressing GFP under the elongation factor 1 alpha, ef1a promotor. B Stable CRISPR–Cas9 knockout of the pigmentation gene oculocutaneous albinism II, oca2 in Astatotilapia calliptera leading to loss of melanin in melanophores. C Transient CRISPR–Cas9 knockout of the “stripe gene” agrp2 in Pundamilia nyererei, resulting in the appearance of horizontal stripe patterns in this usually non-striped species. D Fluorescent in situ hybridization (ISH) for rhobdopsin 2b, rh2b and longwave-sensitive (lws) opsin in the Malawi cichlid Maylandia zebra. E In situ DNA-hybridization chain reaction (HCR) for pax7 (orange) and SRY-box transcription factor 10, sox10 (magenta) in Rhamphochromis sp. ‘chilingali’. F Immunohistochemistry (IHC) for nerve fibers on scales of Melanochromis auratus using an acetylated tubulin antibody. G Cartilage staining of an embryo of Tropheops sp. ‘mauve’. H MicroCT 3D visualization of Aulonocara stuartgranti. I Microscopic analysis of melanophore development and patterning in an embryo of the Lake Victoria basin cichlid Haplochromis latifasciatus. Photo credits: Scott Juntti (A), Joel Elkin / Bethan Clark (B), Brian Dalton / Karen Carleton (D), Aleksandra Marconi (E, G), Duncan Edgley (H), Jan Gerwin (I)