William F. Hutchinson

Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua)

Despite increasing evidence that current exploitation rates can contribute to shifts in life–history traits and the collapse of marine fish stocks, few empirical studies have investigated the likely evolutionary impacts. Here, we used DNA recovered from a temporal series of archived North Sea cod (Gadus morhua) otoliths, to investigate genetic diversity within the Flamborough Head population between 1954 and 1998, during which time the population underwent two successive declines. Microsatellite data indicated a significant reduction in genetic diversity between 1954 and 1970 (total number of alleles: 1954, 46; 1960, 42; 1970, 37), and a subsequent recovery between 1970 and 1998 (total number of alleles: 1970, 37; 1981, 42; 1998, 45). Furthermore, estimates of genetic differentiation (F and R) showed a significant divergence between 1998 and earlier samples. Data are consistent with a period of prolonged genetic drift, accompanied by a replacement of the Flamborough Head population through an increased effective migration rate that occurred during a period of high exploitation and appreciable demographic and phenotypic change. Other studies indicate that diversity at neutral microsatellite loci may be correlated with variability at selected genes, thus compromising a populations subsequent recovery and adaptive potential. Such effects are especially pertinent to North Sea cod, which are threatened by continuing exploitation and rising sea temperatures.

Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring

The existence of biologically differentiated populations has been credited with a major role in conferring sustainability and in buffering overall productivity of anadromous fish population complexes where evidence for spatial structure is uncontroversial. Here, we describe evidence of correlated genetic and life history (spawning season linked to spawning location) differentiation in an abundant and highly migratory pelagic fish, Atlantic herring, Clupea harengus, in the North Sea (NS) and adjacent areas. The existence of genetically and phenotypically diverse stocks in this region despite intense seasonal mixing strongly implicates natal homing in this species. Based on information from genetic markers and otolith morphology, we estimate the proportional contribution by NS, Skagerrak (SKG) and Kattegat and western Baltic (WBS) fish to mixed aggregations targeted by the NS fishery. We use these estimates to identify spatial and temporal differences in life history (migratory behaviour) and habitat use among genetically differentiated migratory populations that mix seasonally. Our study suggests the existence of more complex patterns of intraspecific diversity than was previously recognized. Sustainability may be compromised if such complex patterns are reduced through generalized management (e.g. area closures) that overlooks population differences in spatial use throughout the life cycle.

Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci.

In many marine fish species, genetic population structure is typically weak because populations are large, evolutionarily young and have a high potential for gene flow. We tested whether genetic markers influenced by natural selection are more efficient than the presumed neutral genetic markers to detect population structure in Atlantic herring (Clupea harengus), a migratory pelagic species with large effective population sizes. We compared the spatial and temporal patterns of divergence and statistical power of three traditional genetic marker types, microsatellites, allozymes and mitochondrial DNA, with one microsatellite locus, Cpa112, previously shown to be influenced by divergent selection associated with salinity, and one locus located in the major histocompatibility complex class IIA (MHC-IIA) gene, using the same individuals across analyses. Samples were collected in 2002 and 2003 at two locations in the North Sea, one location in the Skagerrak and one location in the low-saline Baltic Sea. Levels of divergence for putatively neutral markers were generally low, with the exception of single outlier locus/sample combinations; microsatellites were the most statistically powerful markers under neutral expectations. We found no evidence of selection acting on the MHC locus. Cpa112, however, was highly divergent in the Baltic samples. Simulations addressing the statistical power for detecting population divergence showed that when using Cpa112 alone, compared with using eight presumed neutral microsatellite loci, sample sizes could be reduced by up to a tenth while still retaining high statistical power. Our results show that the loci influenced by selection can serve as powerful markers for detecting population structure in high gene-flow marine fish species.

The dangers of ignoring stock complexity in fishery management: the case of the North Sea cod

The plight of the marine fisheries is attracting increasing attention as unsustainably high exploitation levels, exacerbated by more extreme climatic conditions, are driving stocks to the point of collapse. The North Atlantic cod (Gadus morhua), a species which until recently formed a major component of the demersal fisheries, has undergone significant declines across its range. The North Sea stock is typical of many, with a spawning stock biomass that has remained below the safe biological limit since 2000 and recruitment levels near the lowest on record. Cod within the North Sea are currently managed as a single stock, and yet mounting empirical evidence supports the existence of a metapopulation of regionally variable, genetically distinct, sub-stocks. Applying the same management strategies to multiple stocks that differ in their resilience to exploitation inevitably results in the overfishing and likely collapse of the weaker components. Indeed, recent studies have identified two North Sea spawning stocks that have undergone disproportionally large collapses with very substantial reductions in egg production. Similarly affected cod stocks in the northwest Atlantic have shown little evidence of recovery, despite fishery closures. The possible implications of ignoring sub-structuring within management units for biocomplexity, local adaptation and ecosystem stability are considered.

Phylogeography of the rare Balkan endemic Martino's vole, Dinaromys bogdanovi, reveals strong differentiation within the western Balkan Peninsula

The spatial genetic structure of Martinos vole, a rare palaeoendemic species of the western Balkans, was investigated using DNA isolated from archived museum samples. The study was based on partial sequencing (555 bp) of the mitochondrial cytochrome b gene for 63 specimens from 20 different localities throughout the species’ range. Three highly divergent allopatric phylogenetic lineages (Northwestern, Central and Southeastern) were recognized among 47 haplotypes, suggesting three independent glacial differentiation centres within the western Balkans. The Northwestern lineage, which showed the highest divergence from all other samples (mean sequence divergence of 6.64% ± 1.10), comprised samples collected from northwest of the Neretva River in Croatia, western Bosnia and Herzegovina. The Central and Southeastern lineages were separated by an average sequence divergence of 2.95% ± 0.66 and were geographically divided by the Drim River (the Kosovo Basin in Serbia). Overall, haplotype diversity decreased from the Northwestern lineage to the Central and subsequently the Southeastern lineage, in a geographical pattern consistent with a stepping stone colonization. The observed distribution indicates a gradual southerly expansion with subsequent allopatry across the Neretva River and Drim River approximately 1 and 0.3 million years ago, respectively. Such a scenario is concordant with palaeontological evidence. Several highly divergent sublineages within the Northwestern and Central lineages showed no significant geographical structuring, suggesting secondary contact of allopatrically evolved lineages. We hypothesize that the topographical complexity of the Balkans promoted allopatry and isolation on a small geographical scale during interglacial periods, with secondary contact during glacial maxima. Furthermore, the three main lineages should be regarded as evolutionary significant units with important implications for conservation. Ecological data show that the Northwestern lineage in particular fulfils all criteria for a highly endangered, evolutionarily significant unit.

DNA barcodes of fish of the Scotia Sea, Antarctica indicate priority groups for taxonomic and systematics focus

Abstract We analysed cytochrome oxidase I (COI) barcodes for 35 putative fish species collected in the Scotia Sea, and compared the resultant molecular data with field-based morphological identifications, and additional sequence data obtained from GenBank and the Barcode of Life Data System (BOLD). There was high congruence between morphological and molecular classification, and COI provided effective species-level discrimination for nearly all putative species. No effect of geographic sampling was observed for COI sequence variation. For two families, including the Liparidae and Zoarcidae, for which morphological field identification was unable to resolve taxonomy, DNA barcoding revealed significant species-level divergence. However, the dataset lacked sufficient sensitivity for resolving species within the Bathydraco and Artedidraco genera. Analysis of cytochrome b for these two genera also failed to resolve taxonomic identity. The data are discussed in relation to emergent priorities for additional taxonomic studies. We emphasize the utility of DNA barcoding in providing a valuable taxonomic framework for fundamental population studies through assigning life history stages or other morphologically ambiguous samples to parental species.

Association between Growth and Pan I* Genotype within Atlantic Cod Full-Sibling Families

Studies of the pantophysin (Pan I*) locus in Atlantic cod Gadus morhua and other marine gadoids indicate that the locus is under positive selection; in Atlantic cod, genotypic variation at this locus has been linked to differences in growth. Here, we present preliminary data comparing the growth and condition of different Atlantic cod Pan I* genotypes within families held under seminatural mesocosm conditions. Larvae from three full-sibling families carrying Pan I*bb or Pan I*ab genotypes were reared for 10 weeks in two mesocosms. Multivariate analysis of variance indicated that larvae carrying the Pan I*ab genotype exhibited significantly higher standard length, dry weight, and RNA: DNA ratio (condition factor) than did larvae that carried the Pan I*bb genotype, potentially indicating selection. The influence of linked loci cannot be excluded; indeed, the absence of a significant correlation between genotype and growth in one family may substantiate this. The lack of differences in survival among genotypes indicates that moderate selective effects are acting primarily through size-specific mortality and fecundity. The proposed putative fitness effects, together with documented marked geographic differentiation in the wild, have implications for Atlantic cod population structure, effective migration rates, recruitment, and local adaptation, which are of particular relevance in a species threatened by continuing exploitation and rising sea temperatures.

Effects of female spawning experience and larval size on feeding and growth of cod larvae Gadus morhua L. reared in mesocosms

Abstract The viability, defined in terms of growth and feeding success, of cod larvae from first-time and repeat spawners of similar sizes was studied in two mesocosms. The growth rate of larvae from first-time and repeat spawners were similar from hatching through to 41 days old, when the experiment was terminated. Larvae from first-time spawners were heavier throughout the experiment than larvae of repeat spawners, a difference that might be explained by a difference (although non-significant) in egg size between the two groups. There was a significant difference in growth rate between the two mesocosms, which may be explained by the difference in temperature between the mesocosms. In both mesocosms larvae fed mainly on copepod nauplii during the first weeks of life and started to actively select copepodites at age 20 days post hatch. There was no significant difference in the energy content of the ingested prey at a given age between offspring of first-time and repeat spawners, although there was a significant difference between the two mesocosms. The dry mass of the ingested prey items compared to larval dry mass increased until age 17–27 days post hatch and decreased thereafter.

Effects of egg size, parental origin and feeding conditions on growth of larval and juvenile cod Gadus morhua

An experimental study was performed to disentangle parental and environmental effects on the growth of Atlantic cod Gadus morhua larvae and juveniles. Eggs were collected during the spawning season from spawning pairs (families) kept separately in specially designed spawning compartments. Newly hatched larvae were released simultaneously into two mesocosms of 2,500 and 4,400 m(3). Larval growth was monitored by sampling over a 10 week period, after which juveniles were transferred to on-growing tanks, where they were tagged and kept for up to 2 years. Maternal origin was determined by individual microsatellite genotyping of the larvae (n = 3949, 24 families) and juveniles (n = 600). The results showed significant positive correlations between egg size and larval size during the whole mesocosm period. Correlations, however, weakened with time and were no longer significant at the first tank-rearing sampling at an age of 9 months. Significant family-specific differences in growth were observed. The coefficient of variation (c.v.) was calculated in order to examine variation in standard length of larvae during the mesocosm period. Inter-family c.v. was on average 69% of intra-family c.v. Differences in zooplankton densities between the two mesocosms were reflected in larval growth, condition factor and c.v. Low food abundance appeared to reduce c.v. and favour growth of larvae that showed relatively slow growth at high food abundance. It is suggested that genetically determined variation in growth potential is maintained by environmental variability.

The globalization of naval provisioning: Ancient DNA and stable isotope analyses of stored cod from the wreck of the Mary Rose, AD 1545

A comparison of ancient DNA (single-nucleotide polymorphisms) and carbon and nitrogen stable isotope evidence suggests that stored cod provisions recovered from the wreck of the Tudor warship Mary Rose, which sank in the Solent, southern England, in 1545, had been caught in northern and transatlantic waters such as the northern North Sea and the fishing grounds of Iceland and Newfoundland. This discovery, underpinned by control data from archaeological samples of cod bones from potential source regions, illuminates the role of naval provisioning in the early development of extensive sea fisheries, with their long-term economic and ecological impacts.