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 100%
50% 100% astbur Astbur.:1-90001
50% Alignment 1 100% neobri Neobri. (-) 1-89776 Criteria: 70%, 100 bp 50% Regions: 61 20k 18k Alignment 2 16k orenil 14k C7orf57 orenil. (+) 12k 13819-106755 10k Criteria: 70%, 100 bp 8k 100% Regions: 78 6k 4k 2k Alignment 3 0k psenye 50% psenye (+) 100% 9404-106232 Criteria: 70%, 100 bp Regions: 49 50% genomic~DiversityX-axis: astbur 100% Resolution: 31 Window size: 100 bp gene exon 50% UTR 40k CNS 38k mRNA 36k 34k 32k 30k 28k 100% 26k 24k 22k Fhl2 (2of2) 20k 50% 100% C7orf57
50% 100%
50% 60k 58k 56k 54k 52k 50k 48k 46k 44k 42k miRNAs 40k non-coding element divergence
standing variation
gene duplication transposable elements
••• D Brawand et al. (2014) Nature
Cichlid~X 15 N ð
ðC 13
ecology morphology genomes (N>2300) (N>1000) (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)
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