Intra-Species Differences in Population Size shape Life History and Genome Evolution

Abstract

12The evolutionary forces shaping life history trait divergence within species are largely unknown. 13 Killifish (oviparous Cyprinodontiformes) evolved an annual life cycle as an exceptional 14 adaptation to life in arid savannah environments characterized by seasonal water availability. The 15 turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate known to science and 16 displays differences in lifespan among wild populations, representing an ideal natural experiment 17 in the evolution and diversification of life history. Here, by combining genome sequencing and 18 population genetics, we investigate the evolutionary forces shaping lifespan among turquoise 19 killifish populations. We generate an improved reference assembly for the turquoise killifish 20 genome, trace the evolutionary origin of the sex chromosome, and identify genes under strong 21 positive and purifying selection, as well as those evolving neutrally. We find that the shortest-22 lived turquoise killifish populations, which dwell in fragmented and isolated habitats at the outer 23 margin of the geographical range of the species, are characterized by small effective population 24 size and accumulate throughout the genome several small to large-effect deleterious mutations 25 due to genetic drift. The genes most affected by drift in the shortest-lived turquoise killifish 26 populations are involved in the WNT signalling pathway, neurodegenerative disorders, cancer 27 and the mTOR pathway. As the populations under stronger genetic drift are the shortest-lived 28 ones, we propose that limited population size due to habitat fragmentation and repeated 29 population bottlenecks, by causing the genome-wide accumulation of deleterious mutations, 30 cumulatively contribute to the short adult lifespan in turquoise killifish populations. 31 3 Main 32Killifish are a highly successful teleost group, dwelling in a range of diverse habitats and, 33 uniquely among teleosts, evolved an annual life cycle to survive in arid climates characterized by 34 cycles of rainfalls and drought 1 . While on the one hand intermittent precipitation and periodic 35 drought pose strong selective pressures leading to the evolution of embryonic diapause, an 36 adaptation that enables killifish to survive in absence of water 2,3 , on the other hand they cause 37 habitat and population fragmentation, promoting genetic drift. The co-occurrence of strong 38 selective pressure for early-life and extensive drift characterizes life history evolution in African 39 annual killifishes 4 . 40The turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate with a thoroughly 41 documented a post-embryonic life, which, in the shortest-lived strains, amounts to four 42 months 2,3,5,6 . Turquoise killifish has recently emerged as a powerful new laboratory model to 43 study experimental biology of aging due to its short lifespan and to its wide range of aging-44 related changes, which include neoplasias 7 , decreased regenerative capacity 8 , cel...

Deleterious mutations show increasing negative effects with age in Drosophila melanogaster

“…Developments of the MA theory of aging [19,52] predict that the genetic variance in fitness and inbreeding depression should increase with age and that "hybrid" vigor of individuals from crosses between different populations with small effective population sizes should be primarily confined to late ages. These predictions have been supported by a suite of studies (e.g., [19][20][21][22][23][24][25][52][53][54]). However, provided that deleterious mutations with increasing negative effects show increasing variance in effect size with age, and that they in general are at least partly recessive, the above findings are also compatible with aging through deleterious mutations with increasing negative effects.…”

Ancestral transoceanic colonization and recent population reduction in a nonannual killifish from the Seychelles archipelago

“…Despite having some portion of the genome under relaxed purifying selection, fish of the genus Pachypanchax live for several years, significantly longer than the corresponding annual species from continental Africa, whose lifespan can be as short as 4–6 months (Valenzano et al, 2015; Willemsen et al, 2020). Since relaxation of purifying selection largely affects genes involved in late‐life maintenance in annual African killifishes (Cui et al, 2019), we investigated what genes and gene functions were affected by relaxed selection in a clade with long‐term island isolation yet maintaining a normal lifespan.…”

“…The amount of fixed and segregating deleterious mutations in Nothobranchius has been shown to correlate negatively with effective population size (Cui et al, 2019;Willemsen et al, 2019). Hence, we asked whether a similar trend occurred in nonannual species, such as the golden panchax (P. playfairii).…”

“…Previous studies conducted in continental African killifishes have shown that relaxation of selection dominates genome evolution in short-lived annual species, preferentially targeting ageing-related pathways, probably resulting from population fragmentation and population size reduction, combined with a strong selection for early-life phenotypes, such as embryonic diapause and explosive sexual maturation (Cui et al, 2019;Willemsen et al, 2019). Here, we investigate the impact of island isolation on genome evolution and relaxation of selective constraints in a longlived killifish.…”

Extreme genomic volatility characterizes the evolution of the immunoglobulin heavy chain locus in cyprinodontiform fishes

“…Following assembly, any E. coli scaffolds resulting from residual contaminating reads were identified by aligning scaffolds to the E. coli genome using BLASTN [39], and scaffolds containing significant matches were discarded. The remaining scaffolds were then scaffolded using SSPACE [45] using jumping libraries from the killifish genome project [16,17,38].…”