Genetic mapping of the Midas cichlid GOLD locus
Final Report Abstract
Ever since Henry Ford defined color polymorphisms as the occurrence of two or more distinct and genetically determined forms of a species it has been debated how such discontinuous variation can be caused and maintained. In fact, the maintenance of genetic polymorphisms underlies some of the greatest debates involving the most prominent figures in population genetics. Would polymorphisms be frequent or rare? If present, are they maintained by selection? Would this come in the form of disruptive selection and ecological niche partitioning? Or perhaps, by balancing selection in a single population? Could even neutral or intrinsic factors (e.g. mutation rates) play a role? It is widely recognized that, to persist within a population, polymorphisms must be subject to balancing selective forces. Even the slightest differential would be sufficient to lead alleles to loss or fixation. Several mechanisms have been proposed to explain how polymorphisms can be maintained. They include, but are not limited to, negative frequency-dependent selection (advantage of rare morph), heterosis (advantage of heterozygote individuals), divergent selection (gene-flow between locally adapted populations) and disruptive selection (extremes being favored). They give key insights into processes maintaining genetic variation in populations. “Golden” and “dark” morphs in the Midas cichlid species complex (Amphilophus sp.) are a particularly striking example of a balanced polymorphism. Both morphs coexist at similar frequencies in populations several independently colonized Nicaraguan crater lakes. The main goal of the proposed research was to (1) determine the genomic basis of this conspicuous color morphism. As this part of the project was more challenging than anticipated and resulted in significant delays we formulated two additional goals addressing (2) genome-wide divergence between gold and dark Midas cichlids and (3) analyzing the selective pressures shaping gold/dark frequency. This project made important contributions to a better understanding of the Midas cichlid gold/dark polymorphism, as we could show that: 1) Differently expressed genes between gold and dark Midas cichlids include pigmentation genes as well as genes involved in immune function suggesting a complex molecular basis of the gold-dark polymorphism. 2) Experimental evidence for negative‐frequency dependent selection having a role for the maintenance of the dark-gold color polymorphism and that different predators impact color morphs differently. 3) Golden fish (using goldfish, Carassius carassius auratus as proxy) are attacked more often, suggesting a significant cost of being conspicuously colored. 4) The golden and dark morphs differ in differed in eco-morphology, which might promote ecological and evolutionary divergence in Midas cichlids. 5) Young golden Midas cichlids exhibit a rare morph advantage as young gold Midas cichlids are extremely rare as most individuals transform at larger sizes. 6) The gold phenotype is caused by a single dominant locus on Chromosome 11 as shown by genome-wide association mapping and hybrid cross mapping. Yet, although the phenotype is supposedly caused by the same interval across populations, lakes and species, different (combinations of) nucleotide variants seem to be responsible for the expression of the trait. In summary, despite the combination of a wealth of genomic resources (new Midas cichlid high-quality genome with N50>1Mb; >280 re-sequenced genomes, half of it from populations with gold/dark polymorphism), a wide variety of complementary experimental approaches (hybrid crosses, genomewide-association mapping, RNA-seq and molecular biology methods) and a perfect setting for pinpointing causal variants (Mendelian Trait, polymorphism with ongoing gene-flow between individuals with different phenotypes, natural independent replicates from different lakes with partially strong bottlenecks), finding the causal genomic variant(s) of the gold phenotype remains challenging. At the same time, the complexity of this phenotype and the involvement of immune genes we revealed in our RNA-seq analysis leads to the interpretation that in fact also other traits including immune system function are affected by variants of a highly pleiotropically acting golds locus. Our results therefore bear the interesting possibility that much more traits might be affected by the gold locus than previously anticipated and that further analysis of the underlying molecular bases will therefore provide clearer insights into these cryptic changes and the selective pressures that act upon them to maintain this conspicuous polymorphism. The main results reported here are currently being prepared for a comprehensive publication on the genetic mapping results and the impact of this locus to population-level genomic divergence. This project also generated large amounts of molecular data of a very high level of resolution, including a high-order assembly of the Midas cichlid genome, high-resolution genetic map and cross data and a large number of population re-sequencing data. These are extremely useful resources to foster further investigations on this exciting biological system in the future. We are planning to continue along those lines of research in this exciting ecological and evolutionary model systemp.
Publications
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2013. Transcriptomics of morphological color change in polychromatic Midas cichlids. BMC Genomics 14:171
Henning, F., Jones, J.C., Franchini, P. and A. Meyer
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2014. Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish: implications for the maintenance of its gold-dark polymorphism. Biological Journal of the Linnean Society 112: 123-131
Torres-Dowdall, J., Machado-Schiaffino, G., Kautt, A.F., Kusche, H. and A. Meyer
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2014. Evolutionary genomics of cichlid fishes: Explosive speciation and adaptation in the postgenomic era. Annual Review of Genomics and Human Genetics 15: 417-441
Henning F. and A. Meyer
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2014. One cost of being gold: selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae). Biological Journal of the Linnean Society 111: 350-358
Kusche, H. and A. Meyer
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2015. Sympatric ecological divergence associated with a color polymorphism. BMC Biology 13: 82
Kusche, H., Elmer, K.R. and A. Meyer
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2017. The role of rare morph advantage and conspicuousness in the stable gold-dark colour polymorphism of a crater lake Midas cichlid fish. Journal of Animal Ecology 86: 1044–1053
Torres-Dowdall, J., Golcher-Benavides, J., and A. Meyer
