DNA barcoding reveals different cestode helminth species in northern European marine and freshwater ringed seals

Abstract

Three subspecies of the ringed seal (Pusa hispida) are found in northeastern Europe: P. h. botnica in the Baltic Sea, P. h saimensis in Lake Saimaa in Finland, and P. h. ladogensis in Lake Ladoga in Russia. We investigated the poorly-known cestode helminth communities of these closely related but ecologically divergent subspecies using COI barcode data. Our results show that, while cestodes from the Baltic Sea represent Schistocephalus solidus, all worms from the two lakes are identified as Ligula intestinalis, a species that has previously not been reported from seals. The observed shift in cestode communities appears to be driven by differential availability of intermediate fish host species in marine vs. freshwater environments. Both observed cestode species normally infect fish-eating birds, so further work is required to elucidate the health and conservation implications of cestode infections in European ringed seals, whether L. intestinalis occurs also in marine ringed seals, and whether the species is able to reproduce in seal hosts. In addition, a deep barcode divergence found within S. solidus suggests the presence of cryptic diversity under this species name.

Keywords: COI barcoding; Cestoda; Freshwater seals; Ligula intestinalis; Pusa hispida; Schistocephalus solidus.

Graphical abstract

Fig. 1

(A) Geographic distributions of the three northern European ringed seal subspecies from which cestodes were collected for COI barcoding: Baltic ringed seal (green), Saimaa ringed seal (blue), and Ladoga ringed seal (red). (B) Midpoint-rooted neighbor-joining tree based on K2P distances among COI barcode sequences of 35 cestode individuals collected from the three focal ringed seal subspecies. Individuals are colored according to host subspecies, numbers above or next to branches are bootstrap support values based on 500 resamplings of the data matrix (only values > 70% shown). Cestode species names indicated under the main branches are based on barcode similarity to reference sequences in GenBank. (C) Maximum-likelihood tree based on a 562-bp alignment of the barcode sequences of the focal cestodes and 34 diphyllobothriidean reference taxa obtained from GenBank. Numbers above branches are bootstrap support values based on 100 resamplings of the data (only values > 70% shown). In both trees, individual names include the voucher code or GenBank accession number, seal subspecies abbreviation with seal individual code, barcode-based cestode species name, and name of the host (sub)species from which the cestode specimen was collected. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)