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

North American fisher and its geographic distribution. Fisher (Martes pennanti), a mid-sized carnivore, is distributed throughout boreal and montane North America. Subspecific classification has followed geographic subdivision of this range: ssp. pennanti occurs in the east (blue), ssp. columbiana occurs in the Northern Rocky Mountains (light and dark green), and ssp. pacifica is found along the Pacific coast (light and dark red).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: North American fisher and its geographic distribution. Fisher (Martes pennanti), a mid-sized carnivore, is distributed throughout boreal and montane North America. Subspecific classification has followed geographic subdivision of this range: ssp. pennanti occurs in the east (blue), ssp. columbiana occurs in the Northern Rocky Mountains (light and dark green), and ssp. pacifica is found along the Pacific coast (light and dark red).

Mentions: The development of new sequencing technologies [19-23] and multiplexing approaches [24,25] now make it practical to sequence population-scale samples of small genomes at a reasonable cost, and these advancements will encourage widespread use of population-level mitogenome screening [8,15-18]. Here, we use multiplexed massively parallel sequencing to sequence and analyze complete mitochondrial genomes from fishers (Martes pennanti; Figure 1A), a rare carnivore in parts of its range, and one that has previously been shown to exhibit low genetic diversity in the mitochondrial [26,27] and nuclear [28,29] genomes. These data are used to evaluate the consistency of evolutionary inferences gained from partial genome genotyping (represented by D-loop sequences). We are particularly interested in evaluating: (1) how much mitochondrial genetic diversity is captured by partial genomic D-loop sequencing relative to whole genome sequencing; (2) the concordance between mitochondrial haplotypes and lineages identified with these different samples; and (3) the potential impact of mitogenome-scale information on the precision of divergence date estimates, with specific focus on differentiating divergence events (e.g., Holocene population and lineage divergence mediated via European settlement of North America) from more distant events (e.g., Pleistocene epoch or older).


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)

North American fisher and its geographic distribution. Fisher (Martes pennanti), a mid-sized carnivore, is distributed throughout boreal and montane North America. Subspecific classification has followed geographic subdivision of this range: ssp. pennanti occurs in the east (blue), ssp. columbiana occurs in the Northern Rocky Mountains (light and dark green), and ssp. pacifica is found along the Pacific coast (light and dark red).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: North American fisher and its geographic distribution. Fisher (Martes pennanti), a mid-sized carnivore, is distributed throughout boreal and montane North America. Subspecific classification has followed geographic subdivision of this range: ssp. pennanti occurs in the east (blue), ssp. columbiana occurs in the Northern Rocky Mountains (light and dark green), and ssp. pacifica is found along the Pacific coast (light and dark red).
Mentions: The development of new sequencing technologies [19-23] and multiplexing approaches [24,25] now make it practical to sequence population-scale samples of small genomes at a reasonable cost, and these advancements will encourage widespread use of population-level mitogenome screening [8,15-18]. Here, we use multiplexed massively parallel sequencing to sequence and analyze complete mitochondrial genomes from fishers (Martes pennanti; Figure 1A), a rare carnivore in parts of its range, and one that has previously been shown to exhibit low genetic diversity in the mitochondrial [26,27] and nuclear [28,29] genomes. These data are used to evaluate the consistency of evolutionary inferences gained from partial genome genotyping (represented by D-loop sequences). We are particularly interested in evaluating: (1) how much mitochondrial genetic diversity is captured by partial genomic D-loop sequencing relative to whole genome sequencing; (2) the concordance between mitochondrial haplotypes and lineages identified with these different samples; and (3) the potential impact of mitogenome-scale information on the precision of divergence date estimates, with specific focus on differentiating divergence events (e.g., Holocene population and lineage divergence mediated via European settlement of North America) from more distant events (e.g., Pleistocene epoch or older).

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