TY - JOUR

T1 - Late Pleistocene stickleback environmental genomes reveal the chronology of freshwater adaptation

AU - Laine, Jan

AU - Mak, Sarah S. T.

AU - Martins, Nuno F. G.

AU - Chen, Xihan

AU - Gilbert, M. Thomas P.

AU - Jones, Felicity C.

AU - Pedersen, Mikkel Winther

AU - Romundset, Anders

AU - Foote, Andrew D.

N1 - Funding Information: We thank three anonymous reviewers whose feedback greatly improved this manuscript. This work was funded by a European Research Council (ERC) consolidator grant ( ERC-COG-101045346 “EXPLOAD”) and a Norwegian Research Council (NFR) ERC application support grant ( 324353 ) awarded to A.D.F. Publisher Copyright: © 2024 The Author(s)

PY - 2024

Y1 - 2024

N2 - Directly observing the chronology and tempo of adaptation in response to ecological change is rarely possible in natural ecosystems. Sedimentary ancient DNA (sedaDNA) has been shown to be a tractable source of genome-scale data of long-dead organisms1,2,3 and to thereby potentially provide an understanding of the evolutionary histories of past populations.4,5 To date, time series of ecosystem biodiversity have been reconstructed from sedaDNA, typically using DNA metabarcoding or shotgun sequence data generated from less than 1 g of sediment.6,7 Here, we maximize sequence coverage by extracting DNA from ∼50× more sediment per sample than the majority of previous studies1,2,3 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 three-spined 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 three-spined stickleback (e.g., EDA)8 were already established during the brackish phase of the formation of the isolation basin. However, 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 three-spined sticklebacks at the end of the last glacial period complements contemporary experimental approaches9,10,11 and highlights the untapped potential for retrospective “evolve and resequence” natural experiments using sedaDNA.

AB - Directly observing the chronology and tempo of adaptation in response to ecological change is rarely possible in natural ecosystems. Sedimentary ancient DNA (sedaDNA) has been shown to be a tractable source of genome-scale data of long-dead organisms1,2,3 and to thereby potentially provide an understanding of the evolutionary histories of past populations.4,5 To date, time series of ecosystem biodiversity have been reconstructed from sedaDNA, typically using DNA metabarcoding or shotgun sequence data generated from less than 1 g of sediment.6,7 Here, we maximize sequence coverage by extracting DNA from ∼50× more sediment per sample than the majority of previous studies1,2,3 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 three-spined 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 three-spined stickleback (e.g., EDA)8 were already established during the brackish phase of the formation of the isolation basin. However, 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 three-spined sticklebacks at the end of the last glacial period complements contemporary experimental approaches9,10,11 and highlights the untapped potential for retrospective “evolve and resequence” natural experiments using sedaDNA.

KW - adaptation

KW - ancient DNA

KW - environmental genomes

KW - evolve and resequence

KW - Gasterosteus aculeatus

KW - sediment core

KW - three-spined sticklebacks

KW - time series

U2 - 10.1016/j.cub.2024.01.056

DO - 10.1016/j.cub.2024.01.056

M3 - Journal article

C2 - 38350445

AN - SCOPUS:85186991757

VL - 34

SP - 1142-1147.e6

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 5

ER -