Loss of species and genetic diversity during colonization: Insights from acanthocephalan parasites in northern European seals.

Studies on host-parasite systems that have experienced distributional shifts, range fragmentation, and population declines in the past can provide information regarding how parasite community richness and genetic diversity will change as a result of anthropogenic environmental changes in the future. Here, we studied how sequential postglacial colonization, shifts in habitat, and reduced host population sizes have influenced species richness and genetic diversity of Corynosoma (Acanthocephala: Polymorphidae) parasites in northern European marine, brackish, and freshwater seal populations. We collected Corynosoma population samples from Arctic, Baltic, Ladoga, and Saimaa ringed seal subspecies and Baltic gray seals, and then applied COI barcoding and triple-enzyme restriction-site associated DNA (3RAD) sequencing to delimit species, clarify their distributions and community structures, and elucidate patterns of intraspecific gene flow and genetic diversity. Our results showed that Corynosoma species diversity reflected host colonization histories and population sizes, with four species being present in the Arctic, three in the Baltic Sea, two in Lake Ladoga, and only one in Lake Saimaa. We found statistically significant population-genetic differentiation within all three Corynosoma species that occur in more than one seal (sub)species. Genetic diversity tended to be high in Corynosoma populations originating from Arctic ringed seals and low in the landlocked populations. Our results indicate that acanthocephalan communities in landlocked seal populations are impoverished with respect to both species and intraspecific genetic diversity. Interestingly, the loss of genetic diversity within Corynosoma species seems to have been less drastic than in their seal hosts, possibly due to their large local effective population sizes resulting from high infection intensities and effective intra-host population mixing. Our study highlights the utility of genomic methods in investigations of community composition and genetic diversity of understudied parasites.

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

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.

Complementary methods assessing short and long-term prey of a marine top predator ‒ Application to the grey seal-fishery conflict in the Baltic Sea.

The growing grey seal (Halichoerus grypus) population in the Baltic Sea has created conflicts with local fisheries, comparable to similar emerging problems worldwide. Adequate information on the foraging habits is a requirement for responsible management of the seal population. We investigated the applicability of available dietary assessment methods by comparing morphological analysis and DNA metabarcoding of gut contents (short-term diet; n = 129/125 seals, respectively), and tissue chemical markers i.e. fatty acid (FA) profiles of blubber and stable isotopes (SIs) of liver and muscle (mid- or long-term diet; n = 108 seals for the FA and SI markers). The methods provided complementary information. Short-term methods indicated prey species and revealed dietary differences between age groups and areas but for limited time period. In the central Baltic, herring was the main prey, while in the Gulf of Finland percid and cyprinid species together comprised the largest part of the diet. Perch was also an important prey in the western Baltic Proper. The DNA analysis provided firm identification of many prey species, which were neglected or identified only at species group level by morphological analysis. Liver SIs distinguished spatial foraging patterns and identified potentially migrated individuals, whereas blubber FAs distinguished individuals frequently utilizing certain types of prey. Tissue chemical markers of adult males suggested specialized feeding to certain areas and prey, which suggest that these individuals are especially prone to cause economic losses for fisheries. We recommend combined analyses of gut contents and tissue chemical markers as dietary monitoring methodology of aquatic top predators to support an optimal ecosystem-based management.

Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata).

Organisms undergoing latitudinal range expansion face a change in the photoperiod which can lead to a mismatch between the timing of seasonal changes in physiological and life history traits with seasonal environmental changes. This mismatch can lead to lowered survival, for example, due to unsynchronized diapause timing. Successful range expansion even in recent introductions requires that organisms which use the photoperiod for seasonal predictions should show interpopulational differences in photoperiodic responses at different latitudes, as the photoperiod is a function of latitude. We investigated among population differences in photoperiodic responses of life history and physiological traits linked to diapause in the invasive beetle Leptinotarsa decemlineata. Beetles from a northern marginal and a southern European population were reared under short day (12:12L:D) and long day (18:6L:D) photoperiods. Both populations reacted similarly to the short day photoperiod. Their abdominal total lipid content increased and water content decreased which suggests that the beetles prepared for diapause. This was also indicated by low mortality during diapause. In the long day photoperiod large interpopulational differences were found, the southern population ceased lipid accumulation after 5 days, while the northern population continued lipid accumulation as beetles in the short day photoperiod. This indicates that the northern population has a longer critical photoperiod than the southern one. Abdominal total lipid stores in 10 day old beetles were shown to be predominantly composed of neutral lipids (85%), most likely representing storage triacylglycerols. Fatty acid profiles of both the neutral lipids and the phospholipids showed large shifts during the first 10 day of adult life, predominantly in the fractions of 18:0, 18:1ω9, 18:2ω6 and 18:3ω3. Although the degree of unsaturation increased with age, it was not higher in diapausing than non-diapausing beetles. This indicates that this species does not increase diapause related cold tolerance via homeoviscous adaptation, and might have developed other means to cope with suboptimal temperatures, such as behavioral adaptations.

Intestinal helminths of a landlocked ringed seal (Phoca hispida saimensis) population in eastern Finland.

A small, landlocked, endangered ringed seal (Phoca hispida saimensis) population lives as a postglacial relict in Lake Saimaa in eastern Finland. In this study, the intestinal metazoans were examined from a total of 61 Saimaa seals found dead from 1981 to 2001. The helminth fauna was very depauperate. Only one acanthocephalan species, Corynosoma magdaleni, has been able to survive during isolation in the freshwater environment. In addition, only two cestode species were found: Diphyllobothrium ditretum and Schistocephalus sp. However, neither of these larvae developed in the ringed seals. As the newborn pups of Saimaa seals are nursed for about 2 months only one of them was infected by C. magdaleni. At 2-5 months the pups harboured worms; however, the mean intensity did not rise distinctively until the seals were adults. C. magdaleni infection increased with increasing age and the abundances were significantly different between the age groups. There was no correlation between the number of parasites and the adult seal body weight; however, seals weighing 36 kg or more carried the majority of the worms. The distribution of the parasites was aggregated; six seals carried 65% (n=1,182) of all worms (total n=1,809) and 26 seals were uninfected. Variation in the number of worms in individual seals may indicate differences in feeding behaviour and in the diet of seals, and/or variation in the immune status of the seals.