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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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Estimates of mutation rates and divergence dates from complete versus partial genomes. Imposing carnivore-based estimates of mutation rates and a log-normal distribution shows that the modal time to an observed mutation for the complete fisher mitochondrial genomes is 8,428 years (95% C.I. = 5,004 - 17,364), based on all 3,796 third codon positions in the mitochondrial genome (brown). This value is significantly lower than the modal time to an observed mutation for the 379 third codons of cytochrome b (pink; 84,411 years, 95% C.I. = 50,115-173,914).
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Figure 5: Estimates of mutation rates and divergence dates from complete versus partial genomes. Imposing carnivore-based estimates of mutation rates and a log-normal distribution shows that the modal time to an observed mutation for the complete fisher mitochondrial genomes is 8,428 years (95% C.I. = 5,004 - 17,364), based on all 3,796 third codon positions in the mitochondrial genome (brown). This value is significantly lower than the modal time to an observed mutation for the 379 third codons of cytochrome b (pink; 84,411 years, 95% C.I. = 50,115-173,914).

Mentions: Our complete mitogenomes provide an opportunity to examine how whole genome sequencing might impact the accuracy of dating haplotype divergence events in closely related lineages. The use of complete mitogenomes significantly increases the precision of divergence estimates, primarily due to the increase in the number of available synonymous sites. Given the distribution of carnivore mutation rates [35] and calibrations based on cytochrome b (379 third codon positions), one synonymous substitution is expected in ~84 ky (50-174 ky; Figure 5). In contrast, calibrations based on the fisher mitogenome (3,799 third codon positions) instead show an expectation of one synonymous substitution every 8.4 ky (5.0 - 17.4 ky). This suggests that significant improvements in divergence date accuracy (the point estimate) and precision (decreased variance) can be obtained by simply sequencing whole organelle genomes.


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)

Estimates of mutation rates and divergence dates from complete versus partial genomes. Imposing carnivore-based estimates of mutation rates and a log-normal distribution shows that the modal time to an observed mutation for the complete fisher mitochondrial genomes is 8,428 years (95% C.I. = 5,004 - 17,364), based on all 3,796 third codon positions in the mitochondrial genome (brown). This value is significantly lower than the modal time to an observed mutation for the 379 third codons of cytochrome b (pink; 84,411 years, 95% C.I. = 50,115-173,914).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Estimates of mutation rates and divergence dates from complete versus partial genomes. Imposing carnivore-based estimates of mutation rates and a log-normal distribution shows that the modal time to an observed mutation for the complete fisher mitochondrial genomes is 8,428 years (95% C.I. = 5,004 - 17,364), based on all 3,796 third codon positions in the mitochondrial genome (brown). This value is significantly lower than the modal time to an observed mutation for the 379 third codons of cytochrome b (pink; 84,411 years, 95% C.I. = 50,115-173,914).
Mentions: Our complete mitogenomes provide an opportunity to examine how whole genome sequencing might impact the accuracy of dating haplotype divergence events in closely related lineages. The use of complete mitogenomes significantly increases the precision of divergence estimates, primarily due to the increase in the number of available synonymous sites. Given the distribution of carnivore mutation rates [35] and calibrations based on cytochrome b (379 third codon positions), one synonymous substitution is expected in ~84 ky (50-174 ky; Figure 5). In contrast, calibrations based on the fisher mitogenome (3,799 third codon positions) instead show an expectation of one synonymous substitution every 8.4 ky (5.0 - 17.4 ky). This suggests that significant improvements in divergence date accuracy (the point estimate) and precision (decreased variance) can be obtained by simply sequencing whole organelle genomes.

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