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Distinct lineages of Schistocephalus parasites in threespine and ninespine stickleback hosts revealed by DNA sequence analysis.

Nishimura N, Heins DC, Andersen RO, Barber I, Cresko WA - PLoS ONE (2011)

Bottom Line: These clades most likely represent different species that diverged soon after the speciation of their stickleback hosts.In addition, genetic structuring exists among Schistocephalus taken from threespine stickleback hosts from Alaska, Oregon and Wales, although it is much less than the divergence between hosts.Our findings emphasize that biological communities may be even more complex than they first appear, and beg the question of what are the ecological, physiological, and genetic factors that maintain the specificity of the Schistocephalus parasites and their stickleback hosts.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, United States of America.

ABSTRACT
Parasitic interactions are often part of complex networks of interspecific relationships that have evolved in biological communities. Despite many years of work on the evolution of parasitism, the likelihood that sister taxa of parasites can co-evolve with their hosts to specifically infect two related lineages, even when those hosts occur sympatrically, is still unclear. Furthermore, when these specific interactions occur, the molecular and physiological basis of this specificity is still largely unknown. The presence of these specific parasitic relationships can now be tested using molecular markers such as DNA sequence variation. Here we test for specific parasitic relationships in an emerging host-parasite model, the stickleback-Schistocephalus system. Threespine and ninespine stickleback fish are intermediate hosts for Schistocephalus cestode parasites that are phenotypically very similar and have nearly identical life cycles through plankton, stickleback, and avian hosts. We analyzed over 2000 base pairs of COX1 and NADH1 mitochondrial DNA sequences in 48 Schistocephalus individuals collected from threespine and ninespine stickleback hosts from disparate geographic regions distributed across the Northern Hemisphere. Our data strongly support the presence of two distinct clades of Schistocephalus, each of which exclusively infects either threespine or ninespine stickleback. These clades most likely represent different species that diverged soon after the speciation of their stickleback hosts. In addition, genetic structuring exists among Schistocephalus taken from threespine stickleback hosts from Alaska, Oregon and Wales, although it is much less than the divergence between hosts. Our findings emphasize that biological communities may be even more complex than they first appear, and beg the question of what are the ecological, physiological, and genetic factors that maintain the specificity of the Schistocephalus parasites and their stickleback hosts.

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An alignment of the translated protein sequences Schistocephalus from Alaskan, Oregon and Wales threespine hosts, as well as Schistocephalus from ninespine hosts.Only positions that are variable in at least one comparison are represented in this alignment. Using the Alaskan threespine host sequence as a reference, only a single AA difference (red highlighting) occurs at position 152 of NADH1 from a Valine to Isoleucine in the Oregon threespine hosts. Nine differences occur between Schistocephalus collected from threespine hosts in the Pacific vs. Atlantic basins. In comparisons between Schistocephalus collected from threespine and ninespine hosts in Alaska twenty one residue changes exist (position numbers in red), many of which are likely to change the structure of the proteins.
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pone-0022505-g002: An alignment of the translated protein sequences Schistocephalus from Alaskan, Oregon and Wales threespine hosts, as well as Schistocephalus from ninespine hosts.Only positions that are variable in at least one comparison are represented in this alignment. Using the Alaskan threespine host sequence as a reference, only a single AA difference (red highlighting) occurs at position 152 of NADH1 from a Valine to Isoleucine in the Oregon threespine hosts. Nine differences occur between Schistocephalus collected from threespine hosts in the Pacific vs. Atlantic basins. In comparisons between Schistocephalus collected from threespine and ninespine hosts in Alaska twenty one residue changes exist (position numbers in red), many of which are likely to change the structure of the proteins.

Mentions: Based upon the fact that the majority of phylogenetic structuring of the sequences was among host species and large geographic regions, we generated translations from the consensus sequences from both three and ninespine hosts from Alaska, Oregon and Wales. Identifying these protein coding changes provides an indication of how many of the nucleotide changes are potentially functional and subject to natural selection. These translations showed that the majority of SNPs segregating among the threespine populations were in silent sites, leading to very similar protein sequences between worms drawn from threespine hosts from Alaska and Oregon. Over this geographic scale only one nonsynonymous change was observed in residue 152 of NADH1 (Figure 2). In comparison, the differences between worms from threespine hosts from the Pacific vs. Atlantic Ocean basins exhibit greater divergence, with nine residue changing substitutions (Figure 2). In contrast, a very different pattern is observed when comparing the sequences from ninespine hosts to those from threespine hosts. A total of twenty one residues exhibit fixed differences between worms drawn from the two hosts (Figure 2). These 21 amino acid differences between Schistocephalus sequences from different hosts exists even between worms drawn from the two stickleback species living in the same lake in Alaska. These data further support the hypothesis that the nature of the genetic variation among Schistocephalus from the same and different host is qualitatively different, and likely represents two different Schistocephalus species that are specialized to use either threespine or ninespine stickleback.


Distinct lineages of Schistocephalus parasites in threespine and ninespine stickleback hosts revealed by DNA sequence analysis.

Nishimura N, Heins DC, Andersen RO, Barber I, Cresko WA - PLoS ONE (2011)

An alignment of the translated protein sequences Schistocephalus from Alaskan, Oregon and Wales threespine hosts, as well as Schistocephalus from ninespine hosts.Only positions that are variable in at least one comparison are represented in this alignment. Using the Alaskan threespine host sequence as a reference, only a single AA difference (red highlighting) occurs at position 152 of NADH1 from a Valine to Isoleucine in the Oregon threespine hosts. Nine differences occur between Schistocephalus collected from threespine hosts in the Pacific vs. Atlantic basins. In comparisons between Schistocephalus collected from threespine and ninespine hosts in Alaska twenty one residue changes exist (position numbers in red), many of which are likely to change the structure of the proteins.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3139657&req=5

pone-0022505-g002: An alignment of the translated protein sequences Schistocephalus from Alaskan, Oregon and Wales threespine hosts, as well as Schistocephalus from ninespine hosts.Only positions that are variable in at least one comparison are represented in this alignment. Using the Alaskan threespine host sequence as a reference, only a single AA difference (red highlighting) occurs at position 152 of NADH1 from a Valine to Isoleucine in the Oregon threespine hosts. Nine differences occur between Schistocephalus collected from threespine hosts in the Pacific vs. Atlantic basins. In comparisons between Schistocephalus collected from threespine and ninespine hosts in Alaska twenty one residue changes exist (position numbers in red), many of which are likely to change the structure of the proteins.
Mentions: Based upon the fact that the majority of phylogenetic structuring of the sequences was among host species and large geographic regions, we generated translations from the consensus sequences from both three and ninespine hosts from Alaska, Oregon and Wales. Identifying these protein coding changes provides an indication of how many of the nucleotide changes are potentially functional and subject to natural selection. These translations showed that the majority of SNPs segregating among the threespine populations were in silent sites, leading to very similar protein sequences between worms drawn from threespine hosts from Alaska and Oregon. Over this geographic scale only one nonsynonymous change was observed in residue 152 of NADH1 (Figure 2). In comparison, the differences between worms from threespine hosts from the Pacific vs. Atlantic Ocean basins exhibit greater divergence, with nine residue changing substitutions (Figure 2). In contrast, a very different pattern is observed when comparing the sequences from ninespine hosts to those from threespine hosts. A total of twenty one residues exhibit fixed differences between worms drawn from the two hosts (Figure 2). These 21 amino acid differences between Schistocephalus sequences from different hosts exists even between worms drawn from the two stickleback species living in the same lake in Alaska. These data further support the hypothesis that the nature of the genetic variation among Schistocephalus from the same and different host is qualitatively different, and likely represents two different Schistocephalus species that are specialized to use either threespine or ninespine stickleback.

Bottom Line: These clades most likely represent different species that diverged soon after the speciation of their stickleback hosts.In addition, genetic structuring exists among Schistocephalus taken from threespine stickleback hosts from Alaska, Oregon and Wales, although it is much less than the divergence between hosts.Our findings emphasize that biological communities may be even more complex than they first appear, and beg the question of what are the ecological, physiological, and genetic factors that maintain the specificity of the Schistocephalus parasites and their stickleback hosts.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, United States of America.

ABSTRACT
Parasitic interactions are often part of complex networks of interspecific relationships that have evolved in biological communities. Despite many years of work on the evolution of parasitism, the likelihood that sister taxa of parasites can co-evolve with their hosts to specifically infect two related lineages, even when those hosts occur sympatrically, is still unclear. Furthermore, when these specific interactions occur, the molecular and physiological basis of this specificity is still largely unknown. The presence of these specific parasitic relationships can now be tested using molecular markers such as DNA sequence variation. Here we test for specific parasitic relationships in an emerging host-parasite model, the stickleback-Schistocephalus system. Threespine and ninespine stickleback fish are intermediate hosts for Schistocephalus cestode parasites that are phenotypically very similar and have nearly identical life cycles through plankton, stickleback, and avian hosts. We analyzed over 2000 base pairs of COX1 and NADH1 mitochondrial DNA sequences in 48 Schistocephalus individuals collected from threespine and ninespine stickleback hosts from disparate geographic regions distributed across the Northern Hemisphere. Our data strongly support the presence of two distinct clades of Schistocephalus, each of which exclusively infects either threespine or ninespine stickleback. These clades most likely represent different species that diverged soon after the speciation of their stickleback hosts. In addition, genetic structuring exists among Schistocephalus taken from threespine stickleback hosts from Alaska, Oregon and Wales, although it is much less than the divergence between hosts. Our findings emphasize that biological communities may be even more complex than they first appear, and beg the question of what are the ecological, physiological, and genetic factors that maintain the specificity of the Schistocephalus parasites and their stickleback hosts.

Show MeSH