Abstract

The evolutionary forces shaping life history divergence within species are largely unknown. Turquoise killifish display differences in lifespan among wild populations, representing an ideal natural experiment in evolution and diversification of life history. By combining genome sequencing and population genetics, we investigate the evolutionary forces shaping lifespan among wild turquoise killifish populations. We generate an improved reference genome assembly and identify genes under positive and purifying selection, as well as those evolving neutrally. Short-lived populations from the outer margin of the species range have small population size and accumulate deleterious mutations in genes significantly enriched in the WNT signaling pathway, neurodegeneration, cancer and the mTOR pathway. We propose that limited population size due to habitat fragmentation and repeated population bottlenecks, by increasing the genome-wide mutation load, exacerbates the effects of mutation accumulation and cumulatively contribute to the short adult lifespan.

Highlights

  • IntroductionKillifish (oviparous Cyprinodontiformes) evolved an annual life cycle as an exceptional adaptation to life in arid savannah environments characterized by seasonal water availability

  • Killifish evolved an annual life cycle as an exceptional adaptation to life in arid savannah environments characterized by seasonal water availability

  • Using the new turquoise killifish genome assembly and synteny analysis with medaka and platyfish, we reconstructed the origin of the turquoise killifish sex chromosome, which appears to have evolved through two independent chromosomal events, i.e. a fusion and a translocation event

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Summary

Introduction

Killifish (oviparous Cyprinodontiformes) evolved an annual life cycle as an exceptional adaptation to life in arid savannah environments characterized by seasonal water availability. The turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate known to science and displays differences in lifespan among wild populations, representing an ideal natural experiment in the evolution and diversification of life history. As the populations under stronger genetic drift are the shortest-lived ones, we propose that limited population size due to habitat fragmentation and repeated population bottlenecks, by causing the genome-wide accumulation of deleterious mutations, cumulatively contribute to the short adult lifespan in turquoise killifish populations. While sharing physiological adaptations that enable embryonic diapause and rapid sexual maturation, different wild turquoise killifish populations display differences in lifespan, both in the wild and in captivity[14,15,16], making this species an ideal evolutionary model to study the genetic basis underlying life history trait divergence within species. The evolutionary mechanisms responsible for the lifespan differences among turquoise killifish populations are not yet clearly understood

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