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Late Pleistocene stickleback environmental genomes reveal the chronology of freshwater adaptation

Foote, Andrew1

Published Feb 20, 2024 on Dryad. https://doi.org/10.5061/dryad.z8w9ghxkj

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Abstract

Directly observing the chronology and tempo of adaptation in response to ecological change is rarely possible in natural ecosystems. Sedimentary aDNA (sedaDNA) has been shown to be a tractable source of genome-scale data of long-dead organisms, and to thereby potentially provide an understanding of the evolutionary histories of past populations. To date, time series of ecosystem biodiversity have been reconstructed from sedaDNA, typically using DNA metabarcoding or shotgun sequence data generated from less than one gram of sediment. Here we maximise sequence coverage by extracting DNA from ~50x more sediment per sample than the majority of previous studies, to achieve genotype resolution. From a time-series of Late Pleistocene sediments spanning from a marine to freshwater ecosystem, we compare adaptive genotypes reconstructed from the environmental genomes of threespine stickleback at key time points of this transition. We find a staggered temporal dynamic, in which freshwater alleles at known loci of large effect in marine-freshwater divergence of threespine stickleback (e.g. EDA) were already established during the brackish phase of the formation of the isolation basin. Yet marine alleles were still detected across the majority of marine-freshwater divergence associated loci, even after the complete isolation of the lake from marine ingression. Our retrospective approach to studying adaptation from environmental genomes of threespine sticklebacks at the end of the last glacial period complements contemporary experimental approaches and highlights the untapped potential for retrospective ‘evolve-and-resequence’ natural experiments using sedaDNA.