Chromosome level reference of Atlantic halibut Hippoglossushippoglossus provides insight into the evolution of sexual determination systems

Abstract

Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes.To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system.We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes. K E Y W O R D Sevolution of sex, fish, genome-wide association analyses, pleuronectiformes, sex chromosome turnover | 1687 EINFELDT ET aL.

A compendium of novel genomics technologies provides a chromosome-scale assembly and insights into the sex determining system of the Greenland Halibut

“…We generated a final genome assembly of 598.5 Mb, with overall high contiguity (N50=25MB, N90=20MB), of which 96.35% was comprised into 24 chromosome-length scaffolds (GenBank accession: GCA_006182925.3). These 24 scaffolds are consistent with the number of diploid chromosomes (2n=48) for Atlantic Halibut (Einfeldt et al 2021) and Pacific Halibut (GCA_013339905.1). The Hi-C data supported a high degree of accuracy in the overall assembly into these 24 scaffolds, as indicated by the strong concentration of data points along the diagonal rather than elsewhere in the contact maps (Figure S1).…”

“…Chr10 and Chr21 neither correspond to locations where sexdetermining regions have been defined in other species (Figure 1, Table1). Overall, the resolved sex-determining system in Greenland Halibut is highly consistent with the rapid turnover of sex chromosomes in fish, particularly in flatfish, given that the Atlantic Halibut has also undergone a recent evolution of an XY sex-determination mechanism (Einfeldt et al 2021).…”

“…Since juvenile growth potential and size are sexually dimorphic in this species (Ghinter et al 2019), it is valuable to better understand the sex-determining mechanisms to control sex imbalance in catches. Moreover, the recent genome assemblies of flatfish species (Figure 1, Table1, Chen et al 2014, Figueras et al 2016, Shao et al 2017, Einfeldt et al 2021 together with studies on sex-determining loci in this group (Chen et al 2014, Liang et al 2018, Drinan et al 2018, Einfeldt et al 2021 provides an opportunity to investigate the evolutionary turnover of sex chromosomes and sex-determination systems. Flatfishes studied so far are characterized by a variable heterogametic system and different sex-determining genes.…”

“…Within the righteye flounder family (Pleuronectidae), the Hippoglossinae subfamiliy harbors variable genetic SD systems. The Pacific Halibut (Hippoglossus stenolepis) has a ZZ/ZW system and several sex-linked loci aligned in three different linkage groups (Drinan, Loher, & Hauser 2018) while its sister-species, the Atlantic Halibut (H. hippoglossus), has a XX/XY system and a putative SD factor called gsdf on chromosome 12 (Palaiokostas et al 2013;Einfeldt et al 2021).…”

Differential use of multiple genetic sex determination systems in divergent ecomorphs of an African crater lake cichlid

“…(2017) found that the major chr7 XY locus previously identified in Malawi Mbuna cichlids determined sex in a population of A. calliptera from Lake Malawi. Despite only mapping the effect to megabase-scale resolution, they postulated that a variant in the gonadal soma-derived factor ( gsdf ) gene on chromosome 7 was responsible for dictating sex given its repeated role in sex determination in other fish species (Einfeldt et al ., 2021; Jiang et al ., 2016; Kaneko et al ., 2015; Myosho et al ., 2012).…”