Kent, M. P. | bioRxiv Science

bioRxiv2018

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

Intraspecific 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.

genomics↗

bioRxiv2018

A zinc knuckle gene on the Y chromosome (zkY) determines sex in Atlantic cod (Gadus morhua)

The genetic mechanisms determining sex in teleost fishes are highly variable, ranging from a single gene to complex patterns of polygenic regulation. The master sex determining gene has only been identified in very few species and there is no information about the gene in the superorder Paracanthopterygii that includes the codfishes, toadfishes and anglerfishes. Here we characterize a male-specific region of 9 kb on linkage group 11 in Atlantic cod (Gadus morhua) harboring a single gene named zkY for zinc knuckle on the Y chromosome. A diagnostic PCR test of phenotypically sexed males and females of Atlantic cod confirmed the sex-specific nature of the Y-sequence. We searched for autosomal gene copies of zkY and identified twelve highly similar genes, of which eight (zk1-zk8) code for proteins containing the zinc knuckle motif. 3D structure modelling suggests that the amino acid changes observed in six of the eight copies might influence the putative RNA-binding specificity. Cod zkY and the autosomal proteins zk1 and zk2 possess an identical zinc knuckle structure, but only the Y-specific gene zkY was expressed at high levels in the developing larvae before the onset of sex differentiation. We propose that cod zkY functions as the master masculinization gene by coding for a suppressor of germ cell division in males. PCR amplification of Y-sequences in Arctic cod (Arctogadus glacialis) and Greenland cod (Gadus macrocephalus ogac) suggests that this novel sex determining mechanism emerged in codfishes more than 7.5 million years ago.\n\nAuthor SummaryStudying the diverse sex determining genes in teleost fish may contribute to increase our understanding of sex chromosome evolution in vertebrates. To date, no sex determinant is known for the superorder Paracanthopterygii, comprising about 1340 species, including the commercially important Atlantic cod. In this study we characterize a Y-specific region of 9 kb on linkage group 11 containing a single gene named zkY for zinc knuckle on the Y chromosome. The gene is transcribed at high levels in larvae before commencement of sex differentiation and encodes a novel zinc knuckle protein that putatively binds RNA target sequences. We propose that cod zkY suppresses germ cell proliferation in the developing males by interacting with the germ-cell specific RNA regulatory network.

genetics↗