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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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A reconstruction of the phylogenetic relationship of the 35 concatenated COX1 and NADH1 haplotype sequences from Schistocephalus collected from two different stickleback hosts and across three geographic regions.The tree is rooted using Spirometra erinaceieuropaei sequence as an outgroup, which is the closest cestode relative for which there was sufficient mtDNA sequence. The tree was reconstructed using Parsimony, Maximum Likelihood, and Bayesian approaches, and all gave qualitatively similar results (Maximum Likelihood topology is shown). In particular, the deepest division is between sequences from P. pungitius hosts (top) and G. aculeatus host (bottom), with these sequences being different, on average, at nearly 20% of the sites in the sequence (substitution rate above branch). This division is highly supported regardless of being measured by Bayesian Posterior Probability, Bootstrap, or Likelihood Ratio (support below branch). The next supported division is between Schistocephalus from Wales as compared to Oregon and Alaska, but with a sequence divergence less than 5%. The final strongly supported division are Schistocephalus from Oregon as compared to Alaska, but with a sequence divergence of less than 1%. Black dots represented Schistocephalus samples collected from either threespine or ninespine hosts from within Mud Lake, Alaska.
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pone-0022505-g001: A reconstruction of the phylogenetic relationship of the 35 concatenated COX1 and NADH1 haplotype sequences from Schistocephalus collected from two different stickleback hosts and across three geographic regions.The tree is rooted using Spirometra erinaceieuropaei sequence as an outgroup, which is the closest cestode relative for which there was sufficient mtDNA sequence. The tree was reconstructed using Parsimony, Maximum Likelihood, and Bayesian approaches, and all gave qualitatively similar results (Maximum Likelihood topology is shown). In particular, the deepest division is between sequences from P. pungitius hosts (top) and G. aculeatus host (bottom), with these sequences being different, on average, at nearly 20% of the sites in the sequence (substitution rate above branch). This division is highly supported regardless of being measured by Bayesian Posterior Probability, Bootstrap, or Likelihood Ratio (support below branch). The next supported division is between Schistocephalus from Wales as compared to Oregon and Alaska, but with a sequence divergence less than 5%. The final strongly supported division are Schistocephalus from Oregon as compared to Alaska, but with a sequence divergence of less than 1%. Black dots represented Schistocephalus samples collected from either threespine or ninespine hosts from within Mud Lake, Alaska.

Mentions: Both the Maximum Likelihood and Bayesian methodologies provided the same topology for the unique DNA sequences. Two major clades exist that are separated by approximately 20% of the sequence variation. These two clades are highly supported, and correspond precisely with the two different stickleback hosts from which the schistocephalus were drawn (Figure 1). Importantly, even Schistocephalus sequences from the same lake were partitioned between the two clades if the parasites came from different stickleback hosts (Figure 1) such that Schistocephalus from globally distributed threespine stickleback are all more closely related to one another than parasites collected from threespine and ninespine hosts in the same Alaskan lake.


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)

A reconstruction of the phylogenetic relationship of the 35 concatenated COX1 and NADH1 haplotype sequences from Schistocephalus collected from two different stickleback hosts and across three geographic regions.The tree is rooted using Spirometra erinaceieuropaei sequence as an outgroup, which is the closest cestode relative for which there was sufficient mtDNA sequence. The tree was reconstructed using Parsimony, Maximum Likelihood, and Bayesian approaches, and all gave qualitatively similar results (Maximum Likelihood topology is shown). In particular, the deepest division is between sequences from P. pungitius hosts (top) and G. aculeatus host (bottom), with these sequences being different, on average, at nearly 20% of the sites in the sequence (substitution rate above branch). This division is highly supported regardless of being measured by Bayesian Posterior Probability, Bootstrap, or Likelihood Ratio (support below branch). The next supported division is between Schistocephalus from Wales as compared to Oregon and Alaska, but with a sequence divergence less than 5%. The final strongly supported division are Schistocephalus from Oregon as compared to Alaska, but with a sequence divergence of less than 1%. Black dots represented Schistocephalus samples collected from either threespine or ninespine hosts from within Mud Lake, Alaska.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0022505-g001: A reconstruction of the phylogenetic relationship of the 35 concatenated COX1 and NADH1 haplotype sequences from Schistocephalus collected from two different stickleback hosts and across three geographic regions.The tree is rooted using Spirometra erinaceieuropaei sequence as an outgroup, which is the closest cestode relative for which there was sufficient mtDNA sequence. The tree was reconstructed using Parsimony, Maximum Likelihood, and Bayesian approaches, and all gave qualitatively similar results (Maximum Likelihood topology is shown). In particular, the deepest division is between sequences from P. pungitius hosts (top) and G. aculeatus host (bottom), with these sequences being different, on average, at nearly 20% of the sites in the sequence (substitution rate above branch). This division is highly supported regardless of being measured by Bayesian Posterior Probability, Bootstrap, or Likelihood Ratio (support below branch). The next supported division is between Schistocephalus from Wales as compared to Oregon and Alaska, but with a sequence divergence less than 5%. The final strongly supported division are Schistocephalus from Oregon as compared to Alaska, but with a sequence divergence of less than 1%. Black dots represented Schistocephalus samples collected from either threespine or ninespine hosts from within Mud Lake, Alaska.
Mentions: Both the Maximum Likelihood and Bayesian methodologies provided the same topology for the unique DNA sequences. Two major clades exist that are separated by approximately 20% of the sequence variation. These two clades are highly supported, and correspond precisely with the two different stickleback hosts from which the schistocephalus were drawn (Figure 1). Importantly, even Schistocephalus sequences from the same lake were partitioned between the two clades if the parasites came from different stickleback hosts (Figure 1) such that Schistocephalus from globally distributed threespine stickleback are all more closely related to one another than parasites collected from threespine and ninespine hosts in the same Alaskan lake.

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