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Downloaded From bioRxiv preprint doi: https://doi.org/10.1101/852368; this version posted November 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Intra-Species Differences in Population Size shape Life History and Genome Evolution 2 Authors: David Willemsen1, Rongfeng Cui1, Martin Reichard2, Dario Riccardo Valenzano1,3* 3 Affiliations: 4 1Max Planck Institute for Biology of Ageing, Cologne, Germany. 5 2The Czech Academy of Sciences, Institute of Vertebrate Biology, Brno, Czech Republic. 6 3CECAD, University of Cologne, Cologne, Germany. 7 *Correspondence to: [email protected] 8 Key words: life history, evolution, genome, population genetics, killifish, Nothobranchius 9 furzeri, lifespan, sex chromosome, selection, genetic drift 10 11 1 bioRxiv preprint doi: https://doi.org/10.1101/852368; this version posted November 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 12 Abstract 13 The evolutionary forces shaping life history trait divergence within species are largely unknown. 14 Killifish (oviparous Cyprinodontiformes) evolved an annual life cycle as an exceptional 15 adaptation to life in arid savannah environments characterized by seasonal water availability. The 16 turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate known to science and 17 displays differences in lifespan among wild populations, representing an ideal natural experiment 18 in the evolution and diversification of life history. Here, by combining genome sequencing and 19 population genetics, we investigate the evolutionary forces shaping lifespan among turquoise 20 killifish populations. We generate an improved reference assembly for the turquoise killifish 21 genome, trace the evolutionary origin of the sex chromosome, and identify genes under strong 22 positive and purifying selection, as well as those evolving neutrally. We find that the shortest- 23 lived turquoise killifish populations, which dwell in fragmented and isolated habitats at the outer 24 margin of the geographical range of the species, are characterized by small effective population 25 size and accumulate throughout the genome several small to large-effect deleterious mutations 26 due to genetic drift. The genes most affected by drift in the shortest-lived turquoise killifish 27 populations are involved in the WNT signalling pathway, neurodegenerative disorders, cancer 28 and the mTOR pathway. As the populations under stronger genetic drift are the shortest-lived 29 ones, we propose that limited population size due to habitat fragmentation and repeated 30 population bottlenecks, by causing the genome-wide accumulation of deleterious mutations, 31 cumulatively contribute to the short adult lifespan in turquoise killifish populations. 2 bioRxiv preprint doi: https://doi.org/10.1101/852368; this version posted November 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 32 Main 33 Killifish are a highly successful teleost group, dwelling in a range of diverse habitats and, 34 uniquely among teleosts, evolved an annual life cycle to survive in arid climates characterized by 35 cycles of rainfalls and drought1. While on the one hand intermittent precipitation and periodic 36 drought pose strong selective pressures leading to the evolution of embryonic diapause, an 37 adaptation that enables killifish to survive in absence of water2,3, on the other hand they cause 38 habitat and population fragmentation, promoting genetic drift. The co-occurrence of strong 39 selective pressure for early-life and extensive drift characterizes life history evolution in African 40 annual killifishes4. 41 The turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate with a thoroughly 42 documenteda post-embryonic life, which, in the shortest-lived strains, amounts to four 43 months2,3,5,6. Turquoise killifish has recently emerged as a powerful new laboratory model to 44 study experimental biology of aging due to its short lifespan and to its wide range of aging- 45 related changes, which include neoplasias7, decreased regenerative capacity8, cellular 46 senescence9,10, and loss of microbial diversity11. At the same time, while sharing physiological 47 adaptations that enable embryonic diapause and rapid sexual maturation, different wild turquoise 48 killifish populations display differences in lifespan, both in the wild and in captivity12-14, making 49 this species an ideal evolutionary model to study the genetic basis underlying life history trait 50 divergence within species. a Eviota sigillata has been reported to be the shortest-known living vertebrate5, but no information is available regarding the duration of its larval stage and its complete post-hatching lifespan in laboratory conditions. 3 bioRxiv preprint doi: https://doi.org/10.1101/852368; this version posted November 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 51 Characterisation of life history traits in wild-derived laboratory strains of turquoise killifish 52 revealed that while different populations have similar rates of sexual maturation6, populations 53 from arid regions exhibit the shortest lifespans, while populations from more semi-arid regions 54 exhibit longer lifespans6,12. Hence, speed of sexual maturation and adult lifespan appear to be 55 independent in turquoise killifish populations. The evolutionary mechanisms responsible for the 56 lifespan differences among turquoise killifish populations are not yet clearly understood. 57 Mapping genetic loci associated with lifespan differences among turquoise killifish populations 58 showed that adult survival has a complex genetic architecture13,15. Here, combining genome 59 sequencing and population genetics, we investigate to what extent genomic divergence in natural 60 turquoise killifish populations that differ in lifespan is driven by adaptive or neutral evolution. 61 Genome assembly improvement and gene annotation 62 To identify the genomic mechanism that led to the evolution of differences in lifespan between 63 natural populations of the turquoise killifish (Nothobranchius furzeri), we combined the currently 64 available reference genomes13,16 into an improved reference turquoise killifish genome assembly. 65 Due to the high repeat content, assembly from short reads required a highly integrated and multi- 66 platform approach. We ran Allpaths-LG with all the available pair-end sequences, producing a 67 combined assembly with a contig N50 of 7.8kb, corresponding to a ~2kb improvement from the 68 previous versions. Two newly obtained 10X Genomics linked read libraries were used to correct 69 and link scaffolds, resulting in a scaffold N50 of 1.5Mb, i.e. a three-fold improvement from the 70 best previous assembly. With the improved continuity, we assigned 92.2% of assembled bases to 71 the 19 linkage groups using two RAD-tag maps13. Gene content assessment using the BUSCO 72 method improved “complete” BUSCOs from 91.43%13 and 94.59%16 to 95.20%. We mapped 4 bioRxiv preprint doi: https://doi.org/10.1101/852368; this version posted November 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 73 Genbank N. furzeri RefSeq RNA to the new assembly to predict gene models. The predicted gene 74 model set is 96.1% for “complete” BUSCOs. 75 Population genetics of natural turquoise killifish populations 76 Natural populations of turquoise killifish occur along an aridity gradient in Zimbabwe and 77 Mozambique and populations from more arid regions are associated with shorter captive 78 lifespan6,12. A QTL study performed between short-lived and long-lived turquoise killifish 79 populations showed a complex genetic architecture of lifespan (measured as age at death), with 80 several genome-wide loci associated with lifespan differences among long-lived and short-lived 81 populations13. To further investigate the evolutionary forces shaping genetic differentiation in the 82 loci associated with lifespan among wild turquoise killifish populations, we performed pooled 83 whole-genome-sequencing (WGS) of killifish collected from four sampling sites within the 84 natural turquoise killifish species distribution, which vary in altitude, annual precipitation and 85 aridity (Figure S1, Table S1). Population GNP is located within the Gonarezhou National Park 86 at high altitude and in an arid climate (Koeppen-Geiger classification “BWh”, Figure S1), in a 87 region at the outer edge of the turquoise killifish distribution (Figure S1)17-19, which corresponds 88 to the place of origin of the “GRZ” laboratory strain, which has the shortest lifespan of all 89 laboratory strains
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