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

Abstract

BackgroundScience-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.ResultsOverall 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.ConclusionsOur 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.

Characterizing habitats associated with fisher den structures in the Southern Sierra Nevada, California using discrete return lidar

“…The fisher had been considered a candidate species under the California Endangered Species Act until 2010, and is currently a furbearer of special concern in this state. Nevertheless, fishers in California now exist as two genetically isolated populations (northwestern California and the southern Sierra Nevada; Davis et al, 2007;Knaus et al, 2011), and a recent estimate noted that there may be fewer than 350 total animals in the southern Sierra Nevada population (Spencer et al, 2011). Because of continued concern over the limited abundance and range extent of this species in western North America, several major studies are underway aimed at identifying population limiting factors, general habitat associations, and specific habitat requirements for resting and reproduction (Purcell et al, 2009;Zielinski et al, 2010).…”

Phylogeographic mitogenomics of Atlantic cod Gadus morhua: Variation in and among trans‐Atlantic, trans‐Laurentian, Northern cod, and landlocked fjord populations

“…Following extensive use in human population and evolutionary genetics (Horai et al., 1995; Ingman, Kaessmann, Pääbo, & Gyllensten, 2000; Mishmar et al., 2003; Pope, Carr, Smith, & Marshall, 2011; Tanaka et al., 2004), increasing use has been made in intraspecific studies of fish (Carr & Marshall, 2008a; Feutry et al., 2014; Teacher, André, Merilä, & Wheat, 2012) and other mammals (Carr et al., 2015; Knaus, Cronn, Liston, Pilgrim, & Schwartz, 2011; Stone et al., 2010). …”

Comparison of the mitochondrial genomes of the Old and New World strains of the legume pod borer, Maruca vitrata (Lepidoptera: Crambidae)

“…Recently, next-generation sequencing (NGS) technologies have led to more straightforward pipelines for the assembly of complete mitogenome sequences (Jex et al, 2010a;Knaus et al, 2011). Mitogenomes have been sequenced from NGS libraries prepared from long-PCR amplified sequences (Maricic et al, 2010;Morin et al, 2010;Horn et al, 2011) or from sequence captured DNA molecules (Vasta et al, 2009).…”

“…Longrange PCR strategies may remain useful for NGSbased sequencing, especially when limited genetic material can be recovered from small invertebrates (Jex et al, 2010b). Ultra-deep sequencing on NGS platforms can acquire data that are sufficient for the subsequent assembly of full mitogenomes at high read depth (Knaus et al, 2011). Also, due to the high copy numbers of mitochondria in most eukaryotic cells, NGS can reduce the impact of rare nuclearintegrated copies of mitochondrial DNAs or other non-target products (Gilbert et al, 2007;Ho and Gilbert, 2010).…”