Postglacial Echoes: Parasite Genomics Uncover Environmental Changes in Postglacial European Lakes

Abstract

Postglacial environmental changes have influenced biodiversity and species evolution, yet the genomic and demographic responses of parasites remain underexplored. This study investigates the population genetics and demographic history of the flatworm Phyllodistomum umblae, a generalist trematode at the definitive host level infecting Coregonus spp. across perialpine and subarctic postglacial lakes. Additionally, we compare its demographic patterns to Proteocephalus fallax, a whitefish specialist tapeworm, to elucidate how ecological strategies shape evolutionary responses to environmental fluctuations. Genomic data from ddRAD sequencing revealed clear genetic differentiation in P. umblae between subarctic and perialpine regions, likely driven by geographic isolation during glacial cycles. Low genetic differentiation suggests hydrological connectivity and the parasite's ability to utilise several host species as definitive hosts. Demographic inference uncovered distinct evolutionary trajectories between P. umblae and Pr. fallax. During the Last Glacial Period (~115-11 kya), P. umblae populations underwent declines, followed by rapid postglacial expansions after the Last Glacial Maximum (~15-10 kya). In contrast, Pr. fallax exhibited older historical fluctuations, including pronounced bottlenecks during the Middle Pleistocene (~300 kya). Its populations remained stable during the LGP, likely due to host persistence in glacial refugia unavailable in earlier glaciation periods. These findings align with the taxon pulse concept within the Stockholm Paradigm, highlighting how glacial cycles triggered episodic population contractions and expansions. By integrating genomic and historical data, this study (1) underscores parasites as models for understanding ecological and evolutionary processes and (2) provides insights into biodiversity resilience and adaptation to past and future environmental changes.

Keywords: Trematoda; ddRAD‐seq; demographic inference; freshwater; population genetics.

FIGURE 1

Sampling locations of Phyllodistomum umblae in the perialpine (four lakes in Switzerland ‐CH‐) and subarctic (two lakes in northern Norway ‐NO‐) regions (insets on the left). Lakes in each region are colour‐coded (enlarged maps: Suohpatjávri, blue; Langfjordvatn, yellow; Bienne, orange; Walen, pink; Thun, dark orange; Brienz, dark green). Illustrations of European whitefish species/ecotypes surveyed are accompanied by black silhouettes of P. umblae parasites, with the number of specimens genotyped from each host species indicated.

FIGURE 2

Haplotype network of Phyllodistomum umblae cox1 gene, sampled from European whitefish (Coregonus spp.) hosts in perialpine (Bienne, Brienz, Thun and Walen) and subarctic (Langfjordvatn and Suohpatjávri) lakes. The network was computed from uncorrected distances among 131 sequences, 504 nucleotides long, with geneHapR (Zhang et al. 2023). Hash marks represent mutational steps and the size of each circle is proportional to the haplotype frequency.

FIGURE 3

Phyllodistomum umblae population genetic structure across all lakes and regions. (A) Principal component analysis showing PC1 and PC2, with each dot representing an individual and colour representing the different lakes. Only the first axis differentiated the populations between the subarctic and perialpine regions. (B) Ancestry proportions from NGSadmix analysis, where the most adequate number of clusters for P. umblae, was K = 4, according to evalAdmix. (C) Heatmap representing the pairwise distances based on the identity by state (IBS) matrix estimated with ANGSD. Colours correspond to similarity between two multilocus genotypes, from yellow (low) to dark red (high). The populations of P. umblae are closely related within each region, but differentiated between regions. (D) Matrix of pairwise FST values between lakes, estimating genetic differentiation among P. umbale populations. Higher FST values (darker shades) indicates stronger genetic differentiation, mainly between the subarctic and perialpine regions, while populations within each region show lower differentaition.

FIGURE 4

Demographic history inference of ancestral metapopulations: (A) perialpine region of P. umblae, (B) subarctic region of P. umblae, (C) perialpine region of Pr. fallax, and (D) subarctic region of Pr. fallax. The X‐axis represents time in thousands of years before present (kya) and the Y‐axis displays the mean effective population size (N _e) in millions of individuals, both axis are on a logarithmic scale. StairWay plots based on site frequency spectrum (SFS). The red line in the plots represents the mean, grey lines indicate 75% (dark) and 95% (light) confidence intervals. (E) Map showing the extent of ice sheets during the Saalian Glaciation (~300–130 kya) (in dark red) and the Last Glacial Maximum (~15–10 kya) (in dark blue) (Ehlers et al. ; Held et al. 2024), with pink dots indicating the locations of the study areas, and red boxes the estimated position of glacial refugia (Østbye et al. 2005).