Multi-Millennial Genetic Resilience of Baltic Diatom Populations Disturbed in the Past Centuries

Abstract

Little is known about the genetic diversity and stability of natural populations over millennial time scales, although the current biodiversity crisis calls for heightened understanding. Marine phytoplankton, the primary producers forming the basis of food webs in the oceans, play a pivotal role in maintaining marine ecosystems health and serve as indicators of environmental change. This study examines the genetic diversity and shifts in allelic composition in the diatom species Skeletonema marinoi over ~8000 years in the Baltic Sea by analyzing chloroplast and mitochondrial genomes. Sedimentary ancient DNA (sedaDNA) demonstrates the stability and resilience of genetic composition and diversity of this species across millennia in the context of major climate events. Accelerated change in allelic composition is observed from historical periods onwards, coinciding with times of intensifying human activity, like the Roman Empire, the Viking Age, and the Hanseatic Age, suggesting that anthropogenic stressors have profoundly impacted this species for the last two millennia. The data indicate a very high natural stability and resilience of the genomic composition of the species and underscore the importance of uncovering genomic disruptions caused by human impact on organisms, even those not directly exploited, to better predict and manage future biodiversity.

Keywords: Skeletonema marinoi; Baltic Sea; phytoplankton; population genomics; sedaDNA; target capture.

FIGURE 1

(A) Location of the coring sites and corresponding cores in the central Baltic Sea. Gulf of Finland (GOF; core EMB262/12‐3GC) and Eastern Gotland Basin (EGB; core EMB262/6‐30GC). Map lines delineate study areas and do not necessarily depict accepted national boundaries. (B) Sample distribution (in cm) in the sediment cores and corresponding ages. (C) Number of SNPs called per 100 base pairs across the genome for each sample. The mitochondrion and chloroplast genomes of S. marinoi are shown. The gaps indicate the repeat masked regions.

FIGURE 2

Data assessment: (A) sequencing yield and single nucleotide polymorphisms (SNPs): post‐trimming sequencing yield for DNA and RNA baits, and the number of SNPs detected in mitochondrial and chloroplast genomes for each bait set. (B) C‐to‐T substitution: analysis of C‐to‐T substitutions over time for each organelle from all data (GOF and EGB). (C–E) Comparative analysis of normalized nucleotide diversity and diversity indices. (C) Relative nucleotide diversity (PI), (D) Shannon, and (E) Simpson between Eastern Gotland Basin (EGB) and Gulf of Finland (GOF). Each bar graph shows data for both sites with significant p‐values.

FIGURE 3

Principal component analyses of the allelic composition of S. marinoi organelles, demonstrating the genetic diversity and population structure. (A) PC1 and PC2 are categorized by climate events, total organic carbon (TOC) and the age of each sample is given for both sites. (B) PC1 versus time for both sites. The red dashed line marks the transition from the Littorina Sea to the Modern Baltic Sea. Climate events include the Holocene Thermal Maximum (HTM), Late Antique Little Ice Age (LALIA), Medieval Climate Anomaly (MCA), Little Ice Age (LIA), Contemporary Period (CP) and (NA) no event.

FIGURE 4

Temporal analysis of allele turnover in S. marinoi. This figure presents the Generalized Additive Model (GAM) fitted to the allele turnover over time (year cal BP). The data includes both Eastern Gotland Basin (EGB) and Gulf of Finland (GOF) sites. Key environmental events, such as the HTM, LALIA, MCA, LIA, and CP, are noted. Additionally, anthropogenic periods and associated shipping activity estimated from literature sources are shown.