Museomics reveals genetic swamping over 200 years of a marginal native population of the northern forest tree Acer campestre by non-native genotypes introduced as ornamentals

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Abstract

Using historical DNA (hDNA) from herbarium material, we reconstructed two centuries of population‐genetic change in the critically endangered Swedish field maple (Acer campestre). We genotyped 148 herbarium specimens collected from 1820 to 2020 with 12 nuclear microsatellite loci and plastid haplotypes, and compared them with contemporary Swedish and continental reference data. Expected heterozygosity remained high and stable (mean ≈ 0.67), but allelic composition shifted markedly: 66 % of ancestral alleles declined in frequency, 13 % disappeared, and alleles with a continental origin increased. Structure analysis revealed a major turnover from two native gene pools to a present-day population dominated (≈ 74 %) by non-native genotypes. Mantel tests demonstrated a strong isolation-by-time signal (r² = 0.57, p = 0.0001), and plastid data confirmed loss of historical haplotypes and inflow of continental genotypes. Effective population size of the original population was small (Ne ≈ 72; census ≈ 700 trees), yet genetic diversity persisted, probably buffered by long lifespan and repeated introductions. Our results document a cryptic genetic invasion that threatens the evolutionary distinctiveness of the native Swedish lineage. Integrating historical genomics with contemporary data provides a powerful framework for detecting such hidden genetic replacements and for informing targeted conservation of marginal tree populations.

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