Characterization of a Y‐specific duplication/insertion of the anti‐Mullerian hormone type II receptor gene based on a chromosome‐scale genome assembly of yellow perch, Perca flavescens

Abstract

Yellow perch, Perca flavescens, is an ecologically and economically important species native to a large portion of the northern United States and southern Canada and is also a promising candidate species for aquaculture. However, no yellow perch reference genome has been available to facilitate improvements in both fisheries and aquaculture management practices. By combining Oxford Nanopore Technologies long‐reads, 10X Genomics Illumina short linked reads and a chromosome contact map produced with Hi‐C, we generated a high‐continuity chromosome‐scale yellow perch genome assembly of 877.4 Mb. It contains, in agreement with the known diploid chromosome yellow perch count, 24 chromosome‐size scaffolds covering 98.8% of the complete assembly (N50 = 37.4 Mb, L50 = 11). We also provide a first characterization of the yellow perch sex determination locus that contains a male‐specific duplicate of the anti‐Mullerian hormone type II receptor gene (amhr2by) inserted at the proximal end of the Y chromosome (chromosome 9). Using this sex‐specific information, we developed a simple PCR genotyping assay which accurately differentiates XY genetic males (amhr2by+) from XX genetic females (amhr2by−). Our high‐quality genome assembly is an important genomic resource for future studies on yellow perch ecology, toxicology, fisheries and aquaculture research. In addition, characterization of the amhr2by gene as a candidate sex‐determining gene in yellow perch provides a new example of the recurrent implication of the transforming growth factor beta pathway in fish sex determination, and highlights gene duplication as an important genomic mechanism for the emergence of new master sex determination genes.

The rise and fall of the ancient northern pike master sex determining gene

“…A similar duplication and truncation of an amh MSD gene has already been reported in the cobaltcap silverside (Hypoatherina tsurugae), another teleost 22 . In addition, other cases of MSD genes having evolved through duplication / truncation of their ancestral copy have also been described, such as the sdY MSD gene in Salmonids and the putative amhr2by MSD gene in yellow perch, Perca flavescens, demonstrating that preservation of all ancestral domains is not always necessary for a duplicated protein to assume an MSD role 13,23,24 . Because domain gains and losses can both contribute to new protein functions 25,26 , the evolution of a new MSD protein structure can even be seen as a strong evolutionary driver required for the emergence and fixation of some new MSD genes.…”

“…), poeciliids, tilapiine cichlids, salmonids, and sticklebacks, in which different SD systems, sex chromosomes and MSD genes were found even in closely related species [14][15][16][17][18] . Apart from the Oryzias family [19][20][21][22][23][24][25][26][27][28][29] and the salmonids 18,[30][31][32] , however, relatively few studies have explored the evolution of SD systems and the fate of MSD genes within an entire group of closely related species.…”

Sex chromosome and sex locus characterization in goldfish, Carassius auratus (Linnaeus, 1758)

“…Unlike birds and mammals, sex determination in teleost is highly dynamic, with frequent turnovers of both sex determination (SD) systems [8] and master sex determining genes (MSD) [9,10]. Currently about half a dozen different master sex determining genes have been identified in teleosts, including dmrt1 (doublesex and mab-3 related transcription factor 1) in the Japanese medaka, Oryzias latipes (Temminck and Schlegel 1846) [11], sdY (sexually dimorphic on the Y-chromosome) in rainbow trout [12], amh (anti-Mullerian hormone) in Northern pike, Nile tilapia and pejerrey [13][14][15], amhr2 (anti-Mullerian Hormone Receptor Type 2) in yellow perch and the Takifugu pufferfish [16,17], gsdf (gonadal somatic cell derived factor) in sablefish and Luzon medaka, O. luzonensis, (Herre & Ablan, 1934) [18,19], gdf6a (growth differentiation factor 6a) in the turquoise killifish [20] and sox3 (SRY-box transcription factor 3) in the Indian ricefish O. dancena, (Hamilton, 1822) [21]. MSD turnover can be evolutionarily frequent as this has been shown for instance in various ricefish species, in which many MSD switches have been described within different species of the genus Oryzias [22].…”

Sex chromosome and sex locus characterization in the goldfish, Carassius auratus

“…In this study, we 191 explored goldfish sex determination using two complementary whole-genome approaches and 192 found that this species has a XX/XY sex determination system as previously described [24] and 193 a large, non-recombining sex determination region on LG22. Although RAD-sequencing or 194 pool-sequencing have been often used separately to explore sex determination in vertebrates 195 [16,30,31], we choose to combine these two approaches in goldfish because of the significant 196 female-to-male sex reversal induced by temperature [25] that would have prevented a clear 197 identification of the sex determining region using only a pooled strategy, which mixes genetic 198 XY males and XX males resulting from the sex reversal of genetic females. Because sequencing keeps track of each individual, we were able to identify sex-reversed individuals in 200 goldfish that might have masked sex-linked markers in Pool-seq.…”

“…74 Unlike birds and mammals, sex determination in teleost is highly dynamic, with frequent 75 turnovers of both sex determination (SD) systems [8] and master sex determining genes (MSD) 76 [9,10]. Currently about half a dozen different master sex determining genes have been 77 identified in teleosts, including dmrt1 in the Japanese medaka, Oryzias latipes [11], sdY in 78 rainbow trout [12], amh in Northern pike, Nile tilapia and pejerrey [13][14][15], amhr2 in yellow 79 perch and the Takifugu pufferfish [16,17], gsdf in sablefish and Luzon medaka, O. luzonensis 80 [18,19], gsdf6a in the turquoise killifish [20] and sox3 in the Indian ricefish O. dancena [21]. 81 MSD turnover can be evolutionarily rapid as has been shown for instance in various ricefish 82 species [22].…”