Ancient DNA reveals historical demographic decline and genetic erosion in the Atlantic bluefin tuna

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Abstract Overexploitation has depleted fish stocks during the past century, nonetheless its genomic consequences remain poorly understood. Characterising the spatiotemporal patterns of these consequences may provide baseline estimates of past diversity and productivity to aid management targets, help predict future dynamics, and facilitate the identification of evolutionary factors limiting fish population recovery. Here, we evaluate human impacts on the evolution of the iconic Atlantic bluefin tuna ( Thunnus thynnus ), one of the longest and most intensely exploited marine fishes, with a tremendous cultural and economic importance. We sequenced whole genomes from modern (n=49) and ancient (n=41) specimens dating up to 5000 years ago, uncovering several novel findings. First, we identify temporally stable patterns of population admixture, as bluefin tuna caught off Norway and in the eastern Mediterranean share a greater degree of ancestry with Gulf of Mexico bluefin tuna than western and central Mediterranean bluefin tuna. This suggests that Atlantic spawning areas are important mixing grounds for the genetic diversity of Mediterranean bluefin tuna. We model effective population size to show that Mediterranean bluefin tuna began to undergo a demographic decline by the year 1900 to an extent not observed across the previous millennia. Coinciding with this, we found that heterozygosity and nucleotide diversity was significantly lower in modern (2013-2020), than ancient (pre-1941) Mediterranean bluefin tuna, suggesting bluefin tuna underwent a genetic bottleneck. With this work we show how ancient DNA provides novel perspectives on ecological complexity with the potential to inform the management and conservation of fishes. Significance Achieving the aim of the current UN Ocean Decade to “protect and restore ecosystems and biodiversity” is stymied by a lack of historical knowledge on how human exploitation has impacted and therefore what should be restored. Here, we sequence DNA in ancient fish bones to evaluate the historical diversity of the Atlantic bluefin tuna; which has been of great commercial importance for centuries. We find that bluefin tuna began to undergo demographic decline by 1900, 70 years earlier than currently recognised. Correspondingly, we find modern bluefin tuna had lower levels of genetic diversity than historical ones. This suggests that human impacts on the diversity of marine fishes are likely to have begun earlier and be more complex than previously thought.

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