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Non-haplochromines and basal haplochromine P. Haplochromine egg-spots (upper panel) vary in size, shape, number and colouration.
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( b) Examples of male anal fin patterns in East African cichlids. Substr-br, substrate brooders mouthbr, mouthbrooders spp.: species. philander, does not show this characteristic trait 9, 33. Note that one of the ancestral lineages, represented here by P. One of the common features of haplochromines is the presence of egg-spots on the anal fin of males. The haplochromines are the most species-rich and derived group of cichlids in East Africa. ( a) Phylogeny of the East African cichlid fishes based on a new multimarker data set. The mother subsequently broods and carries her progeny in the oral cavities for several weeks after fertilization. Immediately upon spawning, a haplochromine female gathers up her eggs into the mouth the male then presents his egg-spots to which the female responds by snatching and bringing her mouth close to the male’s genital opening upon discharging sperm, the eggs become fertilized inside the female’s mouth ( Fig. The function of egg-spots has been implicated with the mating behaviour of the female-mouthbrooding haplochromines 12, 13. In some species, also females show egg-spots, which are then much less pronounced and colourful. 1b), and even within species a certain degree of variation is observed. Haplochromine egg-spots vary substantially in colour, shape, number and arrangement between species ( Fig. Adult males of ~1,500 cichlid species feature this pigmentation trait in the form of conspicuously coloured circular markings 9, 11, 12. 1), the most species-rich group of cichlid fishes, best known for their spectacular adaptive radiations in the East African lakes Victoria and Malawi 10, 11. Uncovering the mechanisms of how these developmental modules are co-opted or newly evolved is one of the primary goals of evo-devo research 2, 3, 5, 7, 8.Īnal fin egg-spots are an evolutionary innovation in the so-called ‘haplochromines’ 9 ( Fig. Most of the available evidence suggests that new developmental programs emerge largely through co-option of pre-existing regulatory gene networks via changes in their regulation and deployment (‘old genes playing new tricks’ 5). The emergence of evolutionary innovations, that is, lineage-restricted traits linked to qualitatively new functions, involves the origin of new developmental modules that are responsible for the identity of these novel characters 4, 5. While selection explains adaptation and speciation in an adequate manner 6, it is more difficult to conceive how selection would trigger the origin of evolutionary novelties such as insect wings, feathers, tetrapod limbs, flowers, the mammalian placenta, beetle horns or butterfly eye-spots 1, 4, 5, 7, 8.
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The de novo evolution of complex phenotypic traits poses a challenge to evolutionary biology 1, 2, 3, 4, 5. Using transgenic zebrafish, we finally demonstrate that this region shows specific enhancer activities in iridophores, a type of pigment cells found in egg-spots, suggesting that a cis-regulatory change is causally linked to the gain of expression in egg-spot bearing haplochromines. We further find that egg-spot bearing haplochromines, but not other cichlids, feature a transposable element in the cis-regulatory region of fhl2b.
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Applying a combination of RNAseq, comparative genomics and functional experiments, we identify two novel pigmentation genes, fhl2a and fhl2b, and show that especially the more rapidly evolving b-paralog is associated with egg-spot formation. Here we examine the origin of egg-spots, an evolutionary innovation of the most species-rich group of cichlids, the haplochromines, where these conspicuous male fin colour markings are involved in mating. The origin of novel phenotypic characters is a key component in organismal diversification yet, the mechanisms underlying the emergence of such evolutionary novelties are largely unknown.