Limits...
Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore.

Knaus BJ, Cronn R, Liston A, Pilgrim K, Schwartz MK - BMC Ecol. (2011)

Bottom Line: Whole-genome analysis identifies Californian haplotypes from the northern-most populations as highly distinctive, with a significant excess of amino acid changes that may be indicative of molecular adaptation; D-loop sequences fail to identify this unique mitochondrial lineage.Second, the impact of recurrent mutation appears most acute in closely related haplotypes, due to the low level of evolutionary signal (unique mutations that mark lineages) relative to evolutionary noise (recurrent, shared mutation in unrelated haplotypes).This message is timely because it highlights the new opportunities for basing conservation decisions on more accurate genetic information.

View Article: PubMed Central - HTML - PubMed

Affiliation: USDA Forest Service, Pacific Northwest Research Station, Corvallis, OR 97331, USA.

ABSTRACT

Background: Science-based wildlife management relies on genetic information to infer population connectivity and identify conservation units. The most commonly used genetic marker for characterizing animal biodiversity and identifying maternal lineages is the mitochondrial genome. Mitochondrial genotyping figures prominently in conservation and management plans, with much of the attention focused on the non-coding displacement ("D") loop. We used massively parallel multiplexed sequencing to sequence complete mitochondrial genomes from 40 fishers, a threatened carnivore that possesses low mitogenomic diversity. This allowed us to test a key assumption of conservation genetics, specifically, that the D-loop accurately reflects genealogical relationships and variation of the larger mitochondrial genome.

Results: Overall mitogenomic divergence in fishers is exceedingly low, with 66 segregating sites and an average pairwise distance between genomes of 0.00088 across their aligned length (16,290 bp). Estimates of variation and genealogical relationships from the displacement (D) loop region (299 bp) are contradicted by the complete mitochondrial genome, as well as the protein coding fraction of the mitochondrial genome. The sources of this contradiction trace primarily to the near-absence of mutations marking the D-loop region of one of the most divergent lineages, and secondarily to independent (recurrent) mutations at two nucleotide position in the D-loop amplicon.

Conclusions: Our study has two important implications. First, inferred genealogical reconstructions based on the fisher D-loop region contradict inferences based on the entire mitogenome to the point that the populations of greatest conservation concern cannot be accurately resolved. Whole-genome analysis identifies Californian haplotypes from the northern-most populations as highly distinctive, with a significant excess of amino acid changes that may be indicative of molecular adaptation; D-loop sequences fail to identify this unique mitochondrial lineage. Second, the impact of recurrent mutation appears most acute in closely related haplotypes, due to the low level of evolutionary signal (unique mutations that mark lineages) relative to evolutionary noise (recurrent, shared mutation in unrelated haplotypes). For wildlife managers, this means that the populations of greatest conservation concern may be at the highest risk of being misidentified by D-loop haplotyping. This message is timely because it highlights the new opportunities for basing conservation decisions on more accurate genetic information.

Show MeSH

Related in: MedlinePlus

Maximum likelihood tree for all coding nucleotides of the fisher mitochondrial genome. The GTR+Γ model of sequence evolution was used; numbers above nodes represent bootstrap support ≥ 85. The branch colored in red indicates a significant departure from neutral evolution.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3108907&req=5

Figure 4: Maximum likelihood tree for all coding nucleotides of the fisher mitochondrial genome. The GTR+Γ model of sequence evolution was used; numbers above nodes represent bootstrap support ≥ 85. The branch colored in red indicates a significant departure from neutral evolution.

Mentions: To test whether amino acid replacement rates showed evidence of non-neutral evolution, we used a codon-based genetic algorithm [33] to test whether the ratio of non-synonymous (dN) to synonymous (dS) substitutions was greater than 1. This method partitions branches of a tree (in this case, the maximum likelihood topology of the protein coding portion of the genome, with a GTR + Γ substitution model; Figure 4) into groups according to dN/dS. This analysis identified that a three rate class model had a significantly better fit than other models (see Methods). Using this model, the MP7/MP25 haplotype from Northern California was the only terminal that showed a probability greater than 99% of dN exceeding dS (Prob{dN > dS} = 0.999; red branch, Figure 4). Since all four substitutions on this terminal branch result in amino acid replacements, the dN/dS ratio falls in the highest rate class (0.195, 10,000) but the dN/dS ratio cannot be defined due to the absence of synonymous substitutions. This unusual substitution pattern, reflected in two independent samples (MP7, MP25), shows a clear departure from neutral evolution.


Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore.

Knaus BJ, Cronn R, Liston A, Pilgrim K, Schwartz MK - BMC Ecol. (2011)

Maximum likelihood tree for all coding nucleotides of the fisher mitochondrial genome. The GTR+Γ model of sequence evolution was used; numbers above nodes represent bootstrap support ≥ 85. The branch colored in red indicates a significant departure from neutral evolution.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3108907&req=5

Figure 4: Maximum likelihood tree for all coding nucleotides of the fisher mitochondrial genome. The GTR+Γ model of sequence evolution was used; numbers above nodes represent bootstrap support ≥ 85. The branch colored in red indicates a significant departure from neutral evolution.
Mentions: To test whether amino acid replacement rates showed evidence of non-neutral evolution, we used a codon-based genetic algorithm [33] to test whether the ratio of non-synonymous (dN) to synonymous (dS) substitutions was greater than 1. This method partitions branches of a tree (in this case, the maximum likelihood topology of the protein coding portion of the genome, with a GTR + Γ substitution model; Figure 4) into groups according to dN/dS. This analysis identified that a three rate class model had a significantly better fit than other models (see Methods). Using this model, the MP7/MP25 haplotype from Northern California was the only terminal that showed a probability greater than 99% of dN exceeding dS (Prob{dN > dS} = 0.999; red branch, Figure 4). Since all four substitutions on this terminal branch result in amino acid replacements, the dN/dS ratio falls in the highest rate class (0.195, 10,000) but the dN/dS ratio cannot be defined due to the absence of synonymous substitutions. This unusual substitution pattern, reflected in two independent samples (MP7, MP25), shows a clear departure from neutral evolution.

Bottom Line: Whole-genome analysis identifies Californian haplotypes from the northern-most populations as highly distinctive, with a significant excess of amino acid changes that may be indicative of molecular adaptation; D-loop sequences fail to identify this unique mitochondrial lineage.Second, the impact of recurrent mutation appears most acute in closely related haplotypes, due to the low level of evolutionary signal (unique mutations that mark lineages) relative to evolutionary noise (recurrent, shared mutation in unrelated haplotypes).This message is timely because it highlights the new opportunities for basing conservation decisions on more accurate genetic information.

View Article: PubMed Central - HTML - PubMed

Affiliation: USDA Forest Service, Pacific Northwest Research Station, Corvallis, OR 97331, USA.

ABSTRACT

Background: Science-based wildlife management relies on genetic information to infer population connectivity and identify conservation units. The most commonly used genetic marker for characterizing animal biodiversity and identifying maternal lineages is the mitochondrial genome. Mitochondrial genotyping figures prominently in conservation and management plans, with much of the attention focused on the non-coding displacement ("D") loop. We used massively parallel multiplexed sequencing to sequence complete mitochondrial genomes from 40 fishers, a threatened carnivore that possesses low mitogenomic diversity. This allowed us to test a key assumption of conservation genetics, specifically, that the D-loop accurately reflects genealogical relationships and variation of the larger mitochondrial genome.

Results: Overall mitogenomic divergence in fishers is exceedingly low, with 66 segregating sites and an average pairwise distance between genomes of 0.00088 across their aligned length (16,290 bp). Estimates of variation and genealogical relationships from the displacement (D) loop region (299 bp) are contradicted by the complete mitochondrial genome, as well as the protein coding fraction of the mitochondrial genome. The sources of this contradiction trace primarily to the near-absence of mutations marking the D-loop region of one of the most divergent lineages, and secondarily to independent (recurrent) mutations at two nucleotide position in the D-loop amplicon.

Conclusions: Our study has two important implications. First, inferred genealogical reconstructions based on the fisher D-loop region contradict inferences based on the entire mitogenome to the point that the populations of greatest conservation concern cannot be accurately resolved. Whole-genome analysis identifies Californian haplotypes from the northern-most populations as highly distinctive, with a significant excess of amino acid changes that may be indicative of molecular adaptation; D-loop sequences fail to identify this unique mitochondrial lineage. Second, the impact of recurrent mutation appears most acute in closely related haplotypes, due to the low level of evolutionary signal (unique mutations that mark lineages) relative to evolutionary noise (recurrent, shared mutation in unrelated haplotypes). For wildlife managers, this means that the populations of greatest conservation concern may be at the highest risk of being misidentified by D-loop haplotyping. This message is timely because it highlights the new opportunities for basing conservation decisions on more accurate genetic information.

Show MeSH
Related in: MedlinePlus