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Evolution in Darwin’s Dreampond: The genomic substrate for adaptive radiation in Lake Tanganyika cichlid fish Walter Salzburger Zoological Institute drawings: Julie Johnson drawings: !Charles R. Darwin’s (1809-1882) journey onboard of the HMS Beagle lasted from 27 December 1831 until 2 October 1836 Adaptive Radiation !Darwin’s specimens were classified as “an entirely new group” of 12 species by ornithologist John Gould (1804-1881) African Great Lakes taxonomic diversity at the species level L. Turkana 1 5 50 500 species 0 50 100 % endemics 4°N L. Tanganyika L. Tanganyika L. Albert 2°N L. Malawi L. Malawi L. Edward L. Victoria L. Victoria 0° L. Edward L. Edward L. Kivu L. Victoria 2°S L. Turkana L. Turkana L. Albert L. Albert 4°S L. Kivu L. Kivu L. Tanganyika 6°S taxonomic diversity at the genus level 10 20 30 40 50 genera 0 50 100 % endemics 8°S Rungwe L. Tanganyika L. Tanganyika Volcanic Field L. Malawi 10°S L. Malawi L. Victoria L. Victoria 12°S L. Malawi L. Edward L. Edward L. Turkana L. Turkana 14°S cichlid fish non-cichlid fish L. Albert L. Albert gastropods bivalves 28°E 30°E 32°E 34°E 36°E L. Kivu L. Kivu ostracods ••• W Salzburger, B Van Bockxlaer, AS Cohen (2017), AREES | AS Cohen & W Salzburger (2017) Scientific Drilling Cichlid Fishes Fotos: Angel M. Fitor Angel M. Fotos: !About every 20th fish species on our planet is the product of the ongoing explosive radiations of cichlids in the East African Great Lakes taxonomic~Diversity Victoria [~500 sp.] Tanganyika [250 sp.] Malawi [~1000 sp.] ••• ME Santos & W Salzburger (2012) Science ecological morphological~Diversity zooplanktivore insectivore piscivore algae scraper leaf eater fin biter eye biter mud digger scale eater ••• H Hofer & W Salzburger (2008) Biologie III ecological morphological~Diversity ••• W Salzburger (2009) Molecular Ecology astbur Astbur.:1-90001 Alignment 1 neobri 100% Neobri. (-) 1-89776 Criteria: 70%, 100 bp Regions: 61 50% 100% Alignment 2 orenil orenil. (+) 13819-106755 50% Criteria: 70%, 100 bp 100% genomic~Diversity Regions: 78 Alignment 3 psenye 50% psenye (+) 0k 2k 4k 6k 8k 10k 12k 14k 16k 18k 20k 9404-106232 Criteria: 70%, 100 bp Regions: 49 C7orf57 X-axis: astbur Resolution: 31 100% Window size: 100 bp gene exon UTR 50% CNS 100% mRNA 50% 100% 50% 20k 22k 24k 26k 28k 30k 32k 34k 36k 38k 40k C7orf57 Fhl2 (2of2) 100% 50% 100% 50% 100% 50% 40k 42k 44k 46k 48k 50k 52k 54k 56k 58k 60k non-coding element divergence miRNAs standing variation gene duplication transposable elements ••• D Brawand et al. (2014) Nature Cichlid~X 15 N ð ðC 13 ecology (N>2300) morphology (N>1000) genomes (N>500) ••• F Ronco, et al. (unpublished) Taxon C (donor) mean MRCA (B,C) mean acei MRCA sp. sp. (A,C) sp. ‘Chipwa’ 'stone' B A C polylepis Tylochromis Oreochromis tanganicae nigrifrons Trematocara Boulengerochromis microlepis Bathybates graueri Lamprologus callipterus Neolamprologus caudopunctatus Lepidiolamprologus elongatus Altolamprologus compressiceps Julidochromis ornatus Neolamprologus prochilus moorii Variabilichromis Neolamprologus pulcher dhonti Telmatochromis Neolamprologus modestus Neolamprologus tetracanthus Cyprichromis leptosoma Haplotaxodon microlepis Perissodus microlepis Gnathochromis permaxillaris Limnochromis abeelei Cyphotilapia frontosa benthicola Trematochromis Xenotilapia spiloptera Grammatotria lemairii Callochromis macrops Aulonocranus dewindti Ophthalmotilapia ventralis Eretmodus cyanostictus Pseudocrenilabrus philander Serranochromis macrocephalus moorii Tropheus Lobochilotes labiatus Gnathochromis pfefferi Ctenochromis horei Astatotilapia burtoni Labidochromis caeruleus Rhamphochromis Pseudotropheus Cynotilapia pulpican Haplochromis Neochromis rufocaudalis Haplochromis rockkribensis Labrochromis Pundamilia nyererei Maximum Tylochromis polylepis Oreochromis tanganicae Trematocara nigrifrons Bathybatini Boulengerochromini & Boulengerochromis microlepis Bathybates graueri Lamprologus callipterus Neolamprologus caudopunctatus H1 Lepidiolamprologus elongatus Altolamprologus compressiceps Julidochromis ornatus Neolamprologus prochilus Variabilichromis moorii Neolamprologus pulcher Telmatochromis dhonti Neolamprologus modestus H2 Neolamprologus tetracanthus Cyprichromini Perissodini & Cyprichromis leptosoma Haplotaxodon microlepis Perissodus microlepis Gnathochromis permaxillaris Limnochromis abeelei Cyphotilapia frontosa Trematochromis benthicola Xenotilapia spiloptera Grammatotria lemairii Callochromis macrops Aulonocranus dewindti Taxon A (recipient) A Taxon Ophthalmotilapia ventralis Eretmodus cyanostictus riverine species & “Tropheini” Pseudocrenilabrus philander Serranochromis macrocephalus Tropheus moorii Lobochilotes labiatus Gnathochromis pfefferi Ctenochromis horei Astatotilapia burtoni Labidochromis caeruleus H3 Rhamphochromis sp. Pseudotropheus sp. acei Haplochromini Cynotilapia pulpican Haplochromis sp. ‘Chipwa’ Neochromis rufocaudalis Haplochromis rockkribensis Labrochromis 'stone' 40 genes Pundamilia nyererei 45 species 0 0.5 1.0 1.5 2.0 myr 522 individuals max[ mean MRCA(B,C) - mean MRCA(A,C) ] ••• B Meyer, M Matschiner & W Salzburger (2017) Systematic Biology A Haplochromini B Haplochromini C Haplochromini H1: ‘H-lineage’ H2: H3: Δln(lik) = 28.5 Eretmodini Δln(lik) = 14.2 Eretmodini ‘H-lineage’ Δln(lik) = 2.9 Pseudocrenilabrus ‘H-lineage’ 9% Cyphotilapiini Cyphotilapiini Cyphotilapiini Limnochromini Limnochromini Limnochromini Ectodini 21% Perissodus Eretmodini 24% Lamprologini Ectodini Ectodini Boulengerochromis Lamprologini Lamprologini Trematocarini Trematocarini Trematocarini Oreochromini Oreochromini Oreochromini Tylochromini Tylochromini Tylochromini 40 genes 45 species 522 individuals ••• B Meyer, M Matschiner & W Salzburger (2017) Systematic Biology N. brichardi N. pulcher N. olivaceous number of SAGUARO segments 2000 1000 N. marunguensis 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 topology nr. N. gracilis ••• HF Gante, M Matschiner, M Malmstrøm, S Jentøft & W Salzburger (2016) Molecular Ecology LG 01 LG 02 LG 03 LG 04 LG 05 LG 06 LG 07 LG 08/24 LG 09 LG 10 LG 11 LG 12 LG 13 Tilapia chromosomee Tilapia LG 14 LG 15 LG 16/21 LG 17 LG 18 LG 19 LG 20 LG 22 LG 23 ••• HF Gante, M Matschiner, M Malmstrøm, S Jentøft & W Salzburger (2016) Molecular Ecology SNP~phylogenies 20.4 % 45.2 % 22.8 % (11.5 % unresolved) ••• D Brawand et al. (2014) Nature Convergence Lake Tanganyika Lake Malawi mage: M Stiassny & A Meyer (1999) Sci Am A Meyer (1999) Sci M Stiassny & mage: I !Thick-lipped cichlid species, as shown in the last row, have also evolved in Central American species flocks Convergence “Ctenochromis” benthicola Neolamprologus prochilus ••• M Muschick, A Indermaur & W Salzburger (2012) Current Biology Convergence ••• M Muschick, A Indermaur & W Salzburger (2012) Current Biology “Barcode” of Cichlid Life genotype (whole genomes) (stableenvironment isotopes) phenotype (CT scanning) salzburgerlab Daniel Berner (group leader) Barbara Berli Brigitte Aeschbach Mirjam Bissegger Astrid Böhne (group leader) Quiterie Haenel Nicolas Boileau Anna Boila Bernd Egger Telma Laurentino Adrian Indermaur Anna Eberhard Milan Malinsky Nicolas Lichilin Yuri Kläfiger Riccardo Lamano Michael Matschiner Fabrizia Ronco Daniel Lüscher Alexandra Weber Jelena Rajkov Attila Rüegg post-docs Madlen Stange Athimed El Taher Lukas Zimmermann Lukas Widmer PhD students technical staff master students European Research Council FCT Fundaçao para a Ciência e a Tecnologia !www.salzburgerlab.org www.facebook.com/waltersalzburgerlab.