Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies

Abstract

Ligula intestinalis (Linnaeus, 1758) is a tapeworm parasite with a worldwide distribution that uses a wide variety of fish species as its second intermediate host. In the present study, we investigated the prevalence and population genetic structure of plerocercoids of L. intestinalis in five common cyprinoid species, roach Rutilus rutilus (Linnaeus), freshwater bream Abramis brama (Linnaeus), white bream Blicca bjoerkna (Linnaeus), bleak Alburnus alburnus (Linnaeus), and rudd Scardinius erythrophthalmus (Linnaeus), collected in six water bodies of the Czech Republic (Milada, Most, Medard, Jordán, Římov and Lipno). Of the six study sites, the highest frequency of parasitism was recorded in Lake Medard (15%). The overall prevalence rate among the species was as follows: roach > rudd ≥ freshwater bream > bleak > white bream. Two mitochondrial genes (cytb and COI) were used to compare the population genetic structure of parasite populations using selected samples from the five fish species. The results of the phylogenetic analysis indicated that all populations of L. intestinalis were placed in Clade A, previously identified as the most common in Europe. At a finer scale, haplotype network and PCoA analyses indicated the possible emergence of host specificity of several mtDNA haplotypes to the freshwater bream. Moreover, pairwise Fixation indices (F ST ) revealed a significant genetic structure between the parasite population in freshwater bream and other host species. Parasite populations in roach not only showed the highest rate of prevalence but also depicted a maximum number of shared haplotypes with populations from bleak and rudd. Our results suggest that recent ecological differentiation might have influenced tapeworm populations at a fine evolutionary scale. Thus, the differences in prevalence between fish host species in different lakes might be influenced not only by the parasite's ecology, but also by its genetic diversity.

Host-associated genetic differentiation in the face of ongoing gene flow: ecological speciation in a pathogenic parasite of freshwater fish

“…These ecological data might be indicative of emerging host-specific races of the parasite; however, a subsequent microsatellite study using 15 polymorphic loci revealed only low genetic structuring within Lineage A, with almost no variation attributable to different fish hosts across the European continent (Štefka et al, 2009). In contrast, a recent study focusing on sympatric populations from four different fish species found nonrandom distribution of mitochondrial haplotypes between the hosts, suggesting possible evolution of host specificity (Nazarizadeh et al, 2022). Considering its unique ecological character, Lineage A presents an ideal model to explore the interactions between divergent selection pressures and ecological isolation mechanisms.…”

“…We collected 84 plerocercoid samples from five prevalent host species in Czechia: R. rutilus , A. alburnus , B. bjoerkna , S. erythrophthalmus , and A. brama (Nazarizadeh et al, 2022). These specimens were sourced from 10 different freshwater ecosystems throughout Czechia (see Table S1 and Figure 1) using gillnets, in the frame of hydrobiological research (see Nazarizadeh et al, 2022 for sampling details). The samples were fixed in 96% ethanol and subsequently stored at a refrigerated temperature prior to DNA extraction.…”

“…Ligula intestinalis (Cestoda) is a widespread pseudophyllidean tapeworm that serves as a valuable model organism for exploring the intricate dynamics of ecological speciation (Bouzid et al, 2008; Hoole et al, 2010; Nazarizadeh et al, 2023, 2022; Štefka et al, 2009). It possesses a complex life cycle that begins with eggs hatching in freshwater environments into coracidia larvae, which are then ingested by a copepod, the initial intermediate host.…”

Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm Ligula intestinalis

“…A total of 16 plerocercoids were collected from 15 roach ( Rutilus rutilus ), caught from water bodies Želivka, Most and Klíčava in the Czech Republic according to previously described methods [23] (electronic supplementary material, table S1). To maintain uniform conditions and minimize variability in transcriptome expression, only 1-year old fish infected with a single tapeworm were selected from the Most and Klíčava water bodies (electronic supplementary material, figure S1).…”

“…Larval worms can be induced to develop sexually in vitro [18]. The tapeworm has been extensively used in endocrinological, ecological, population genetic, phylogeographic and immunological studies [20][21][22][23].…”