A migration-associated supergene reveals loss of biocomplexity in Atlantic cod

Chromosome structural variation may underpin ecologically important intraspecific diversity by reducing recombination within supergenes containing linked, coadapted alleles. Here, we confirm that an ancient chromosomal rearrangement is strongly associated with migratory phenotype and individual genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. We reconstruct trends in effective population size over the last century and reveal declines in effective population size matching onset of industrialized harvest (after 1950). We find different demographic trajectories between individuals homozygous for the chromosomal rearrangement relative to heterozygous or homozygous individuals for the noninverted haplotype, suggesting different selective histories across the past 150 years. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic, phenotypic, and demographic variation in a highly connected marine species and show how overfishing may have led to loss of biocomplexity within Northern cod stock.

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A migration-associated supergene reveals loss of biocomplexity in Atlantic cod

10.1101/361691 ◽

2018 ◽

Author(s):

Tony Kess ◽

Paul Bentzen ◽

Sarah J. Lehnert ◽

Emma V.A. Sylvester ◽

Sigbjørn Lien ◽

...

Keyword(s):

Population Size ◽

Effective Population Size ◽

Phenotypic Variation ◽

Chromosomal Rearrangement ◽

Atlantic Cod ◽

Marine Species ◽

Genomic Variation ◽

Fine Scale ◽

Effective Population ◽

Northern Cod

AbstractIntraspecific phenotypic diversity is integral to ecological resilience and the provision of ecosystem services1. Chromosome structural variation may underpin intraspecific diversity and complex phenotypes2 by reducing recombination within supergenes containing linked, co-adapted alleles. Connecting ecologically-relevant phenotypes to genomic variation can enable more precise conservation of exploited marine species by protecting important genetic diversity3,4. Here, using genome-wide association analysis of a 12K single nucleotide polymorphism (SNP) array we confirm that an ancient, derived chromosomal rearrangement consisting of two adjacent inversions is strongly associated with migratory phenotype and individual-level genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. The presence of all identified migration-associated loci within this rearrangement indicates that pervasive variation in migration phenotype is in part controlled by a recombination-resistant supergene, facilitating fine-scale individual phenotypic variation within Northern cod. Furthermore, we reconstruct trends in effective population size over the last century, and find genomic signatures of population collapse, and different patterns of population expansion and decline among individuals based on supergene alleles. We demonstrate declines in effective population size consistent with the onset of industrialized harvest (post 1950) and substantially reduced effective size of individuals homozygous for the derived chromosomal rearrangement relative to heterozygous individuals or those homozygous for the ancestral version of this chromosomal region. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic and phenotypic variation in a highly connected marine species, and suggest a loss of biocomplexity from a migration-associated supergene within Northern cod by overfishing.

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Large effective population size and temporal genetic stability in Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f10-084 ◽

2010 ◽

Vol 67 (10) ◽

pp. 1585-1595 ◽

Cited By ~ 50

Author(s):

Nina Overgaard Therkildsen ◽

Einar Eg Nielsen ◽

Douglas P. Swain ◽

Jes Søe Pedersen

Keyword(s):

Genetic Variability ◽

Population Size ◽

Effective Population Size ◽

Gadus Morhua ◽

Atlantic Cod ◽

Population Decline ◽

Allelic Diversity ◽

Estimation Methods ◽

Effective Population ◽

Commercial Fish

Worldwide, many commercial fish stocks have experienced dramatic declines due to overfishing. Such fisheries-induced population reductions could potentially erode the genetic diversity of marine fish populations. Based on analyses of DNA extracted from archived and contemporary samples, this paper compares the genetic variability at nine microsatellite loci in a Canadian population of Atlantic cod ( Gadus morhua ) over 80 years, spanning from before the fishery intensified to now when the population is at historically low abundance. Extensively validated genetic data from the temporally spaced samples were used to estimate the effective population size. Over the period, we observed no loss of either heterozygosity or allelic diversity. Several of the estimation methods applied could not distinguish the effective population size from infinity, and the lower 95% confidence limit on estimates was generally >500, suggesting that the effective population size is probably considerably larger than this. Hence, it appears that the southern Gulf of St. Lawrence cod stock has maintained genetic variability to sustain future evolution despite a dramatic population decline.

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Family relationships and effective population size in a natural cohort of Atlantic cod (Gadus morhua) larvae

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f96-161 ◽

1997 ◽

Vol 54 (S1) ◽

pp. 11-18 ◽

Cited By ~ 38

Author(s):

C M Herbinger ◽

R W Doyle ◽

C T Taggart ◽

S E Lochmann ◽

A L Brooker ◽

...

Keyword(s):

Population Size ◽

Effective Population Size ◽

Family Relationships ◽

Gadus Morhua ◽

Atlantic Cod ◽

Effective Population

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Long-term persistence and evolutionary divergence of a marine fish population with a very small effective population size (Kildin cod Gadus morhua kildinensis)

Marine Biology ◽

10.1007/s00227-015-2642-8 ◽

2015 ◽

Vol 162 (5) ◽

pp. 979-992 ◽

Cited By ~ 2

Author(s):

Victor Andreev ◽

Mikhail Fokin ◽

Nikolai Mugue ◽

Petr Strelkov

Keyword(s):

Population Size ◽

Effective Population Size ◽

Marine Fish ◽

Gadus Morhua ◽

Fish Population ◽

Evolutionary Divergence ◽

Effective Population ◽

Kildin Cod ◽

Small Effective Population Size

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Understanding and Estimating Effective Population Size for Practical Application in Marine Species Management

Conservation Biology ◽

10.1111/j.1523-1739.2010.01637.x ◽

2011 ◽

Vol 25 (3) ◽

pp. 438-449 ◽

Cited By ~ 184

Author(s):

MATTHEW P. HARE ◽

LEONARD NUNNEY ◽

MICHAEL K. SCHWARTZ ◽

DANIEL E. RUZZANTE ◽

MARTHA BURFORD ◽

...

Keyword(s):

Population Size ◽

Effective Population Size ◽

Marine Species ◽

Practical Application ◽

Effective Population ◽

Species Management

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Genetic structure and effective population size through time: a tale on two coastal marine species with contrasting life-history patterns

Frontiers in Marine Science ◽

10.3389/conf.fmars.2015.03.00248 ◽

2015 ◽

Vol 2 ◽

Author(s):

Francisco Sara ◽

Robalo Joana

Keyword(s):

Life History ◽

Genetic Structure ◽

Population Size ◽

Effective Population Size ◽

Marine Species ◽

Effective Population ◽

Coastal Marine ◽

Life History Patterns

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Depensation, probability of fertilization, and the mating system of Atlantic cod (Gadus morhua L.)

ICES Journal of Marine Science ◽

10.1016/j.icesjms.2004.07.007 ◽

2004 ◽

Vol 61 (7) ◽

pp. 1144-1150 ◽

Cited By ~ 62

Author(s):

Sherrylynn Rowe ◽

Jeffrey A. Hutchings ◽

Dorte Bekkevold ◽

Ana Rakitin

Keyword(s):

Population Size ◽

Gadus Morhua ◽

Atlantic Cod ◽

Fertilization Rate ◽

Effective Population ◽

Broadcast Spawning ◽

The North ◽

Research Programmes ◽

The North Sea ◽

Census Population Size

Abstract Atlantic cod (Gadus morhua L.) have been severely overexploited and are currently at historic population lows, having declined 90% in the North Sea and 99% off northeast Newfoundland in recent decades. Slow rates of recovery and continuing declines may be attributable to depensation, defined as a reduction in per capita growth rate concomitant with reduced population size. Several potential causes of depensation relate to low mating success and consequent reduced production of offspring. We explore the empirical basis of one of these in Atlantic cod using egg fertilization and male abundance data obtained from 21 experimental populations generated by three independent research programmes. We find support for the hypotheses that (a) fertilization rate declines with abundance and (b) variance in fertilization rate increases as population size declines. The former identifies one potential mechanism underlying depensation in Atlantic cod. The latter has negative genetic consequences for effective population size (Ne), resulting in a decline in the ratio of Ne to census population size (Ne/Nc) with declining abundance. Our results may have general implications for the conservation biology of broadcast-spawning marine fish, particularly those with mating systems similar to that of Atlantic cod.

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Genomic tools for management and conservation of Atlantic cod in a coastal marine protected area

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/cjfas-2017-0254 ◽

2018 ◽

Vol 75 (11) ◽

pp. 1915-1925 ◽

Cited By ~ 2

Author(s):

Marion Sinclair-Waters ◽

Paul Bentzen ◽

Corey J. Morris ◽

Daniel E. Ruzzante ◽

Matthew P. Kent ◽

...

Keyword(s):

Gadus Morhua ◽

Marine Protected Area ◽

Atlantic Cod ◽

Marine Species ◽

Effective Population ◽

Coastal Marine ◽

Genomic Tools ◽

Snp Panel ◽

Surrounding Areas ◽

Management And Conservation

Marine protected areas (MPAs) can serve as effective tools for the management and conservation of exploited marine species. The Gilbert Bay MPA in coastal Labrador was created to protect a genetically distinct population of Atlantic cod (Gadus morhua); however, decreases in abundance continue to occur potentially due to exploitation outside the MPA. We developed a single-nucleotide polymorphism (SNP) panel to identify Gilbert Bay cod in areas outside MPA boundaries where mixing with offshore cod occurs. In total, 361 individuals from Gilbert Bay, surrounding areas, and offshore were genotyped for 10 913 SNPs. Using FST rankings and guided regularized random forest, we selected 23 SNPs that together generate 100% accuracy in individual assignment and accurately estimate the proportion of Gilbert Bay cod in fishery samples from sites outside MPA boundaries: on average, fishery samples included 17.3% Gilbert Bay cod. Estimates of effective population size for the Gilbert Bay population ranged from 655 to 1114. Our findings demonstrate the power of using genomic approaches for management of an exploited marine species and enhancing the design of MPAs.

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