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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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Genealogical inferences from complete versus partial mitochondrial genomes, and the impact on haplotype identification. Maximum likelihood trees constructed using a GTR+Γ model of nucleotide evolution: (A) complete mitochondrial genome versus (B) the D-loop region. Haplotypes are colored by geographic source. Black terminal taxa labelled "Hap 1-12" in panel 3B are D-loop haplotypes from Drew et al. [26]. Numbers above edges indicate boot strap support values > 85% derived from 1,000 replicates.
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Figure 3: Genealogical inferences from complete versus partial mitochondrial genomes, and the impact on haplotype identification. Maximum likelihood trees constructed using a GTR+Γ model of nucleotide evolution: (A) complete mitochondrial genome versus (B) the D-loop region. Haplotypes are colored by geographic source. Black terminal taxa labelled "Hap 1-12" in panel 3B are D-loop haplotypes from Drew et al. [26]. Numbers above edges indicate boot strap support values > 85% derived from 1,000 replicates.

Mentions: Previous mtDNA genotyping based on D-loop [26] and combined D-loop and cytochrome b [32] sequences of fishers revealed 12 haplotypes range wide. Partitioning of these haplotypes among subspecies groupings was inconclusive. For example, some observed haplotypes were unique to geographic and taxonomic partitions. However, these authors also observed haplotypes that were shared among these partitions. One haplotype ("haplotype 1", Figure 3B; [26]) was shared among subspecies pennanti, columbiana and pacifica, and showed a geographic distribution that spanned Minnesota, Wisconsin, Montana, Idaho, British Columbia and California. In Montana and Idaho, previous mitochondrial DNA data demonstrated haplotypes present as a result of reintroductions of fishers to the Rocky Mountains from eastern and northern populations [30], and identification of a native haplotype that is hypothesized to have escaped trapping pressure and population extinction during the 20th century [30]. In another case, the sharing of a haplotype among the rarest populations in the Sierra Nevada range of Southern California with a Northern California population has been used to suggest that California fisher populations were historically connected, despite a gap of 430 km in their current geographic distribution [31,32]. In both Californian and Rocky Mountain populations, management and conservation decisions have relied on matrilineal inferences estimated from partial mitochondrial genome sequences, and these data play a role in ongoing decisions regarding the status of fishers in these areas [32].


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)

Genealogical inferences from complete versus partial mitochondrial genomes, and the impact on haplotype identification. Maximum likelihood trees constructed using a GTR+Γ model of nucleotide evolution: (A) complete mitochondrial genome versus (B) the D-loop region. Haplotypes are colored by geographic source. Black terminal taxa labelled "Hap 1-12" in panel 3B are D-loop haplotypes from Drew et al. [26]. Numbers above edges indicate boot strap support values > 85% derived from 1,000 replicates.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Genealogical inferences from complete versus partial mitochondrial genomes, and the impact on haplotype identification. Maximum likelihood trees constructed using a GTR+Γ model of nucleotide evolution: (A) complete mitochondrial genome versus (B) the D-loop region. Haplotypes are colored by geographic source. Black terminal taxa labelled "Hap 1-12" in panel 3B are D-loop haplotypes from Drew et al. [26]. Numbers above edges indicate boot strap support values > 85% derived from 1,000 replicates.
Mentions: Previous mtDNA genotyping based on D-loop [26] and combined D-loop and cytochrome b [32] sequences of fishers revealed 12 haplotypes range wide. Partitioning of these haplotypes among subspecies groupings was inconclusive. For example, some observed haplotypes were unique to geographic and taxonomic partitions. However, these authors also observed haplotypes that were shared among these partitions. One haplotype ("haplotype 1", Figure 3B; [26]) was shared among subspecies pennanti, columbiana and pacifica, and showed a geographic distribution that spanned Minnesota, Wisconsin, Montana, Idaho, British Columbia and California. In Montana and Idaho, previous mitochondrial DNA data demonstrated haplotypes present as a result of reintroductions of fishers to the Rocky Mountains from eastern and northern populations [30], and identification of a native haplotype that is hypothesized to have escaped trapping pressure and population extinction during the 20th century [30]. In another case, the sharing of a haplotype among the rarest populations in the Sierra Nevada range of Southern California with a Northern California population has been used to suggest that California fisher populations were historically connected, despite a gap of 430 km in their current geographic distribution [31,32]. In both Californian and Rocky Mountain populations, management and conservation decisions have relied on matrilineal inferences estimated from partial mitochondrial genome sequences, and these data play a role in ongoing decisions regarding the status of fishers in these areas [32].

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