Intraspecific Phylogeographic Genomics From Multiple Complete mtDNA Genomes in Atlantic Cod (Gadus morhua): Origins of the “Codmother,” Transatlantic Vicariance and Midglacial Population Expansion

Abstract

On the basis of multiple complete mitochondrial DNA genome sequences, we describe the temporal phylogeography of Atlantic cod (Gadus morhua), a lineage that has undergone a complex pattern of vicariant evolution, postglacial demographic shifts, and historic sharp population declines due to fishing and/or environmental shifts. Each of 32 fish from four spawning aggregations from the northwest Atlantic and Norway has a unique mtDNA sequence, which differs by 6-60 substitutions. Phylogenetic analysis identifies six major haplogroups that range in age from 37 to 75 KYA. The widespread haplotype identified by previous single-locus analyses at the center of a ''star phylogeny'' is shown to be a paraphyletic assemblage of genome lineages. The coalescent that includes all cod occurs 162 KYA. The most basal clade comprises two fish from the western Atlantic. The most recent superclade that includes all fish examined from Norway, and which includes 84% of all fish examined, dates to 128 KYA at the Sangamon/Wü rm interglacial, when ocean depths on continental shelves would have favored transcontinental movement. The pairwise mismatch distribution dates population expansion of this superclade to the middle of the Wisconsinan/Weichsel glaciation 59 KYA, rather than to a postglacial emergence from a marine refugium 12 KYA, or to more recent historic events. We discuss alternative scenarios for the expansion and distribution of the descendants of the ''codmother'' in the North Atlantic. Mitochondrial phylogenomic analyses generate highly resolved trees that enable fine-scale tests of temporal hypotheses with an accuracy not possible with single-locus methods.

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

“…The observed mean genetic distance of 0.039 substitutions per site then gives an estimated divergence rate of 1.03 × 10 −8 substitutions/site/year, and a temporal interval of 5,844 years between substitutions. These values are similar to those calculated by Carr and Marshall (2008a) for the 15,655‐bp cod genome without the control region, and only slightly higher than that calculated for the Alaska pollock (Carr & Marshall, 2008b) and Homo (Achilli et al., 2004). Similar results are obtained with Alaska pollock ( Gadus chalcogrammus ) as the outgroup (Lait, 2016).…”

“…The Labrador and Baffin Island samples were collected by local fishermen between September 2013 and November 2014 (Table 1; see Acknowledgments). The 32 partial mtDNA genomes from Carr and Marshall (2008a; GenBank Accession Numbers EU877710‐EU877741; NOR, HAW, NGB, and FLM) are included here, with the addition of the complete control region sequence (see below).…”

“…Primers were originally designed for use with Atlantic cod (Coulson et al., 2006) or as part of this study. The control regions for the 32 partial mitogenomes from Carr and Marshall (2008a) were amplified using the primers g20F with g20‐2R1 and g20‐2F1 with g20R. PCRs were carried out using Qiagen PCR kits following the manufacturer's protocol with the following modifications: 2.0 mM MgCl 2 , 0.4 μM forward and reverse primer, and 40 extension cycles.…”

“…Carr and Marshall (2008a) identified a much older time scale of population divergence than previously suspected, based on 32 mitogenomes from four populations from north and south of the Laurentian Channel, the offshore seamount Flemish Cap, and off Norway, as well as paraphyly among short (0.3–0.4 kbp) cytochrome b genotypes within six major mitogenomic lineages. We expand the data to a total of 153 mitogenomes by inclusion of 10 new populations from north and south of the Laurentian Channel in the Northwest Atlantic, the Baltic Sea, and a landlocked Arctic fjord at Lake Qasigialiminiq, Baffin Island (see Table S1).…”

“…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). …”