Limits...
Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus).

Karvonen A, Lucek K, Marques DA, Seehausen O - PLoS ONE (2015)

Bottom Line: Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited.We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates.The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats.

View Article: PubMed Central - PubMed

Affiliation: University of Jyväskylä, Department of Biological and Environmental Science, FI-40014 University of Jyväskylä, Jyväskylä, Finland.

ABSTRACT
Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in population-pairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide an example of divergent parasitism in freshwater fish ecotypes by examining macroparasite infections in threespine stickleback (Gasterosteus aculeatus) of four Swiss lake systems each harbouring parapatric lake-stream ecotype pairs. We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates. The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats. This suggests that genetic differentiation is unrelated to the magnitude of parasite infection contrasts when gene flow is constrained by geographical barriers while in the absence of physical barriers, genetic differentiation and the magnitude of differences in infections tend to be positively correlated.

No MeSH data available.


Related in: MedlinePlus

Map of the four study lake systems in Switzerland.Lake populations of stickleback are indicated in blue and stream populations (all streams are inlets flowing into the lakes) in green. The Constance and Geneva systems harbour distinct stickleback lineages while the Biel and Wohlen (Bern) systems lie in the stickleback hybrid zone. Note that the distribution ranges of lake and stream populations overlap in the Constance system as lake fish migrate upstream to spawn in spring. Map copyright: Wikimedia (CC BY-SA); Inlets copyright: OpenStreetMap contributors (CC BY-SA).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4472517&req=5

pone.0130579.g001: Map of the four study lake systems in Switzerland.Lake populations of stickleback are indicated in blue and stream populations (all streams are inlets flowing into the lakes) in green. The Constance and Geneva systems harbour distinct stickleback lineages while the Biel and Wohlen (Bern) systems lie in the stickleback hybrid zone. Note that the distribution ranges of lake and stream populations overlap in the Constance system as lake fish migrate upstream to spawn in spring. Map copyright: Wikimedia (CC BY-SA); Inlets copyright: OpenStreetMap contributors (CC BY-SA).

Mentions: Sticklebacks of both lake and stream ecotypes were sampled from each of the four lake systems (Wohlen, Biel, Constance and Geneva, Fig 1) during the stickleback breeding season in April-May 2012 using dip nets from shallow water or un-baited minnow traps set overnight. In the Geneva system, the sampling protocol included samples from two pairs of lake and stream sticklebacks (Fig 1, S1 Table). Waterway distance between the stream sampling location and the lake shore was short in all lake systems (0.18–2.3 km), except for the locations in the Geneva system where they were longer (S1 Table). Fish were euthanized in MS-222 or clove oil solution and put on ice immediately after catching. In the laboratory, the fish were measured for standard length and dissected for macroparasite infections on gills, eyes and internal organs. Since bringing the fish alive to the laboratory was logistically not possible, but fresh material was needed for examination of eye cataracts (see below), protozoan and monogenean infections were not examined. In most cases, parasites were identified to the genus level. For example, eye flukes of the genus Diplostomum commonly include several co-infecting species or cryptic species that are morphologically indistinguishable [56–58]. However, Diplostomum species found in the eye lenses are different from those in the eye humour [57, 59] and they are referred here to as two groups of Diplostomum spp. according to their site of infection, lens or humour of the fish eye. The lens-infecting species of Diplostomum cause cataracts in eyes of fish [60]. To estimate their impact on the sticklebacks, the coverage of cataracts in the eye lenses of the fish (% of lens area) was scored from 0% to 100% in steps of 10% using slit-lamp microscopy [60].


Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus).

Karvonen A, Lucek K, Marques DA, Seehausen O - PLoS ONE (2015)

Map of the four study lake systems in Switzerland.Lake populations of stickleback are indicated in blue and stream populations (all streams are inlets flowing into the lakes) in green. The Constance and Geneva systems harbour distinct stickleback lineages while the Biel and Wohlen (Bern) systems lie in the stickleback hybrid zone. Note that the distribution ranges of lake and stream populations overlap in the Constance system as lake fish migrate upstream to spawn in spring. Map copyright: Wikimedia (CC BY-SA); Inlets copyright: OpenStreetMap contributors (CC BY-SA).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4472517&req=5

pone.0130579.g001: Map of the four study lake systems in Switzerland.Lake populations of stickleback are indicated in blue and stream populations (all streams are inlets flowing into the lakes) in green. The Constance and Geneva systems harbour distinct stickleback lineages while the Biel and Wohlen (Bern) systems lie in the stickleback hybrid zone. Note that the distribution ranges of lake and stream populations overlap in the Constance system as lake fish migrate upstream to spawn in spring. Map copyright: Wikimedia (CC BY-SA); Inlets copyright: OpenStreetMap contributors (CC BY-SA).
Mentions: Sticklebacks of both lake and stream ecotypes were sampled from each of the four lake systems (Wohlen, Biel, Constance and Geneva, Fig 1) during the stickleback breeding season in April-May 2012 using dip nets from shallow water or un-baited minnow traps set overnight. In the Geneva system, the sampling protocol included samples from two pairs of lake and stream sticklebacks (Fig 1, S1 Table). Waterway distance between the stream sampling location and the lake shore was short in all lake systems (0.18–2.3 km), except for the locations in the Geneva system where they were longer (S1 Table). Fish were euthanized in MS-222 or clove oil solution and put on ice immediately after catching. In the laboratory, the fish were measured for standard length and dissected for macroparasite infections on gills, eyes and internal organs. Since bringing the fish alive to the laboratory was logistically not possible, but fresh material was needed for examination of eye cataracts (see below), protozoan and monogenean infections were not examined. In most cases, parasites were identified to the genus level. For example, eye flukes of the genus Diplostomum commonly include several co-infecting species or cryptic species that are morphologically indistinguishable [56–58]. However, Diplostomum species found in the eye lenses are different from those in the eye humour [57, 59] and they are referred here to as two groups of Diplostomum spp. according to their site of infection, lens or humour of the fish eye. The lens-infecting species of Diplostomum cause cataracts in eyes of fish [60]. To estimate their impact on the sticklebacks, the coverage of cataracts in the eye lenses of the fish (% of lens area) was scored from 0% to 100% in steps of 10% using slit-lamp microscopy [60].

Bottom Line: Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited.We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates.The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats.

View Article: PubMed Central - PubMed

Affiliation: University of Jyväskylä, Department of Biological and Environmental Science, FI-40014 University of Jyväskylä, Jyväskylä, Finland.

ABSTRACT
Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in population-pairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide an example of divergent parasitism in freshwater fish ecotypes by examining macroparasite infections in threespine stickleback (Gasterosteus aculeatus) of four Swiss lake systems each harbouring parapatric lake-stream ecotype pairs. We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates. The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats. This suggests that genetic differentiation is unrelated to the magnitude of parasite infection contrasts when gene flow is constrained by geographical barriers while in the absence of physical barriers, genetic differentiation and the magnitude of differences in infections tend to be positively correlated.

No MeSH data available.


Related in: MedlinePlus