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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.

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Related in: MedlinePlus

Population variation in the fisher mitochondrial genome. The physical organization of the fisher mitochondrial genome is shown with the position of protein coding (blue), tRNA (red), rRNA (purple) and non-coding (colorless) regions indicated. The middle grey track shows the relative sequencing depth across all 40 genomes; scale runs from 1× to 8,000× and is log transformed. Colored bars on inside track show the location of the D-loop amplicon (yellow), the non-coding portion of the mitochondrion (green), and regions that were excluded from our analysis due to insufficient read depth (red). Orange ticks represent segregating sites with magenta ticks marking amino acid substitutions.
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Figure 2: Population variation in the fisher mitochondrial genome. The physical organization of the fisher mitochondrial genome is shown with the position of protein coding (blue), tRNA (red), rRNA (purple) and non-coding (colorless) regions indicated. The middle grey track shows the relative sequencing depth across all 40 genomes; scale runs from 1× to 8,000× and is log transformed. Colored bars on inside track show the location of the D-loop amplicon (yellow), the non-coding portion of the mitochondrion (green), and regions that were excluded from our analysis due to insufficient read depth (red). Orange ticks represent segregating sites with magenta ticks marking amino acid substitutions.

Mentions: Range-wide analysis of 40 complete fisher mitogenomes yielded an aligned data set of 16,290 bp consisting of 13 protein coding genes (11,397 bp), two ribosomal RNA genes (2,528 bp), 22 transfer RNA genes (1,515 bp), and the non-coding D-loop (299 bp)(Figure 2). Whole genome analysis revealed 15 haplotypes defined by 66 segregating sites, 19 of which are shared between two or more haplotypes, and 47 of which are found in single genomes. These variable sites combine to yield an average pairwise distance of 0.00088 in our sample of 40 genomes; averaged across samples and genomes, this equates to approximately 14.3 differences between any two mitogenomes.


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)

Population variation in the fisher mitochondrial genome. The physical organization of the fisher mitochondrial genome is shown with the position of protein coding (blue), tRNA (red), rRNA (purple) and non-coding (colorless) regions indicated. The middle grey track shows the relative sequencing depth across all 40 genomes; scale runs from 1× to 8,000× and is log transformed. Colored bars on inside track show the location of the D-loop amplicon (yellow), the non-coding portion of the mitochondrion (green), and regions that were excluded from our analysis due to insufficient read depth (red). Orange ticks represent segregating sites with magenta ticks marking amino acid substitutions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Population variation in the fisher mitochondrial genome. The physical organization of the fisher mitochondrial genome is shown with the position of protein coding (blue), tRNA (red), rRNA (purple) and non-coding (colorless) regions indicated. The middle grey track shows the relative sequencing depth across all 40 genomes; scale runs from 1× to 8,000× and is log transformed. Colored bars on inside track show the location of the D-loop amplicon (yellow), the non-coding portion of the mitochondrion (green), and regions that were excluded from our analysis due to insufficient read depth (red). Orange ticks represent segregating sites with magenta ticks marking amino acid substitutions.
Mentions: Range-wide analysis of 40 complete fisher mitogenomes yielded an aligned data set of 16,290 bp consisting of 13 protein coding genes (11,397 bp), two ribosomal RNA genes (2,528 bp), 22 transfer RNA genes (1,515 bp), and the non-coding D-loop (299 bp)(Figure 2). Whole genome analysis revealed 15 haplotypes defined by 66 segregating sites, 19 of which are shared between two or more haplotypes, and 47 of which are found in single genomes. These variable sites combine to yield an average pairwise distance of 0.00088 in our sample of 40 genomes; averaged across samples and genomes, this equates to approximately 14.3 differences between any two mitogenomes.

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