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

Abstract

Sexual reproduction is a ubiquitous basic feature of life and genetic sex determination is thus widespread, at least among eukaryotes. Understanding the remarkable diversity of sex determination mechanisms, however, is limited by the paucity of empirical studies. Here, we traced back the evolution of sex determination in an entire clade of vertebrates and uncovered that the northern pike (Esox lucius) master sex-determining gene initiated from a 65 to 90 million-year-old gene duplication and remained sex-linked on undifferentiated sex chromosomes for at least 56 million years. Contrasting with its ancient origin, we identified several independent species-or population-specific transitions of sex determination mechanisms in this lineage, including an unexpected complete and recent Y-chromosome loss in some North American northern pike populations. These findings highlight the diversity of the evolutionary fates of master sex-determining genes and raise the importance of careful considerations of population demographic history in sex determination studies. Our study also puts forward the hypothesis that occasional sex reversals and genetic bottlenecks provide a nonadaptive explanation for sex determination transitions.

A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific

“…As SD systems and MSD are not well conserved among teleosts, it is a challenge to infer evolutionary patterns and conserved themes from one species to another. However, a recent study investigated the evolution of SD in Esociformes and discovered that the northern pike MSD gene evolved from a gene duplication that occurred before 65 Mya, which has remained sex-linked on undifferentiated sex chromosome for at least 56 Mya (although a few species and populations have undergone an SD transition) [11]. In addition, a duplicated Y-specific amhy was associated with the male phenotype in Odontesthes silversides [20] .…”

A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

“…Similarly, skinks (Scincidae) share homologous, mostly poorly differentiated XX/XY sex chromosomes across a wide phylogenetic spectrum for at least 85 million years [28]. Recent findings in the teleost family Esocidae report undifferentiated sex chromosomes of similar evolutionary age (65–90 Myr) in teleosts [29]. The Salmonidae family, which experienced a whole-genome duplication ca 90 Ma [30], presumably harbours a conserved sex determination gene, perhaps as old as 50 Myr, on different chromosomes in different species [17,18], which encodes a homomorphic XX/XY sex chromosome system.…”

Lessons from an unusual vertebrate sex-determining gene

“…the ability to regulate oestrogen synthesis required for ovarian differentiation [76]. But whether this MSD role has conserved its sex-determining function in all salmonid species remains to be better explored as maintaining the same MSD gene for a long period seems like a difficult endeavour, with complex evolutionary trajectories including gains and losses at the top (sex chromosomes and sex determination), and downstream compromises (sex-differentiation) as have been found in some fish families [78]. Considering the complexity of the mechanisms of sex determination and their plasticity this question still needs more investigation and the discovery of other unusual MSD genes, like sdY , would probably fuel additional models for the tightly linked evolution of sex chromosomes, sex determination and sex-differentiation.…”

“…This process can eventually lead to the degeneration or erosion of the heterogametic sex chromosome in genomic regions surrounding this new MSD and can even cover almost the entire chromosome except for a pseudoautosomal region. However, this evolution towards a highly differentiated sex chromosome does not seem mandatory as there are more and more examples of old but yet still undifferentiated sex chromosomes [18,21,24,78]. Differences between such undifferentiated sex chromosomes can even be restricted to a few single nucleotide polymorphisms, like for instance in some pufferfish species of Takifugu in which recombination suppression did not seem to have spread out from the single Y-defining allele bearing the sex-determining function in the amhr2 gene for at least 5 Myr [24].…”