Genetic sex determination (GSD) evolved independently and repeatedly in diverse taxa, including animals, plants, and fungi (Tree of Sex Consortium et al., 2014; Beukeboom and Perrin, 2014), but the stability of such systems varies drastically among groups. In mammals and birds, conserved male or female heterogametic sex determination (SD) systems have been maintained over a long evolutionary time with conserved master sex-determining (MSD) genes (Marshall Graves, 2008). In contrast, teleost fishes display both genetic and environmental sex determination (ESD), and a remarkable evolutionary lability driven by rapid turnovers of sex chromosomes and MSD genes (Kikuchi and Hamaguchi, 2013; Pan et al., 2017). These characteristics make teleosts an attractive group in which to study the evolution of SD systems.

In the past two decades, the identity of a variety of MSD genes has been revealed in teleosts thanks to advances in sequencing technologies. These findings generated new hypotheses on how the birth of MSD genes through allelic diversification or duplication with or without translocation may drive sex chromosome turnover in vertebrates (Kikuchi and Hamaguchi, 2013; Pan et al., 2017). These teleost MSD genes also provided empirical support for the ‘limited option’ idea that states that certain genes known to be implicated in sex differentiation pathways are more likely to be recruited as new MSD genes (Marshall Graves and Peichel, 2010). The majority of these recently discovered MSD genes, however, were phylogenetically scattered, making it challenging to infer evolutionary patterns and conserved themes of sex chromosomes and/or MSD gene turnovers. Although comparative studies have been accomplished in medakas, poeciliids, tilapiine cichlids, salmonids, and sticklebacks (Kikuchi and Hamaguchi, 2013), transitions of SD systems in relation to the fate of known MSD genes within closely related species have only been explored in medakas (Myosho et al., 2015) and salmonids (Guiguen et al., 2018).

Esociformes is a small order of teleost fishes (Figure 1) that diverged from their sister group Salmoniformes about 110 million years ago (Mya) and diversified from a common ancestor around 90 Mya (Campbell et al., 2013; Campbell and Lopéz, 2014). With two families (Esocidae, including Esox, Novumbra, and Dallia, and Umbridae, including Umbra) and 13 well-recognized species (Warren et al., 2020), Esociformes is an ecologically important group of freshwater species from the northern hemisphere (Campbell et al., 2013; Campbell and Lopéz, 2014). We demonstrated that a male-specific duplication of the anti-Müllerian hormone gene (amhby) is the MSD gene in Esociformes and that this gene is located in a small male-specific insertion on the Y chromosome of northern pike (Esox lucius) (Pan et al., 2019).

Figure 1

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Here, we took advantage of the small number of Esociformes species and their relatively long evolutionary history to explore the evolution of SD in relation to the fate of this amhby MSD gene. Generating novel draft genome assemblies and population genomic data in multiple species of Esociformes (Figure 1), we traced the evolutionary trajectory of amhby from its origin in a gene duplication event 65–90 Mya to its demise during species- or population-specific SD transitions. Our results highlight the diverse evolutionary fates experienced by an MSD gene. Among SD transitions, we uncovered a recent loss of the entire Y chromosome in some populations of northern pike. We hypothesize that drift, exacerbated by the bottleneck effect, may have facilitated the loss of the sex chromosome along with its MSD gene in these populations, a new mechanism for entire sex chromosome loss in vertebrates.

The northern pike MSD gene amhby substantially diverges from its autosomal copy amha, suggesting an ancient origin (Pan et al., 2019), unlike other cases of amh duplication in fishes, that appears to be comparatively young (Hattori et al., 2013; Li et al., 2015). Here, we show that the amhby duplicate emerged before the split of Esocidae and Umbridae between 65 and 90 Mya (Campbell et al., 2013) and was subsequently secondarily lost in the Dallia lineage. We also demonstrate that amhby presence is significantly associated with male phenotype in most species of Esox and in Novumbra. Although we cannot rule out the possibility that amhby was recruited independently as the MSD gene in Esox and Novumbra, our results suggest the more parsimonious hypothesis that amhby likely acquired an MSD function before the diversification of Esocidae at least 56 Mya.

Studies on SD systems of cichlid fishes and true frogs suggested that frequent turnovers can keep sex chromosomes undifferentiated (Gammerdinger et al., 2018; Jeffries et al., 2018). It was proposed that in these organisms, the turnover of sex chromosomes was facilitated by autosomes that host genes involved in sex differentiation pathways that could be readily recruited as new MSD genes, facilitating turnovers of sex chromosomes (Vicoso, 2019). Alternative evolutionary pathways could also involve conserved MSD genes that translocate onto different autosomes, as demonstrated for the salmonid sdY gene (Guiguen et al., 2018). Interestingly, this scenario does not seem to be the case with Esocidae. No highly differentiated sex chromosomes were observed in the surveyed population of E. masquinongy and N. hubbsi (this study), or in E. lucius, despite Esocidae having retained the same ancestral XX/XY system (likely controlled by amhby) for at least 56 million years. In addition, whole-genome analyses in E. masquinongy suggest that its male-specific locus on the Y chromosome is conserved in terms of size and location with that of E. lucius despite 45 million years of divergence. Such conservation is unusual in teleosts, where frequent turnover of SD systems is considered the norm (Kikuchi and Hamaguchi, 2013; Pan et al., 2017). In line with our present results, substantially undifferentiated sex chromosomes have also been maintained over relatively long evolutionary periods in some Takifugu fish species (Kamiya et al., 2012), supporting the idea that theoretical models of sex chromosome evolution cannot be generalized across taxa and that additional, as-yet unknown evolutionary forces can prevent sex chromosome decay.

Even though this MSD gene has been maintained for a long evolutionary period, our results revealed that it has been subjected to several independent SD transitions, potentially driven by different mechanisms in the Esocidae lineage. In D. pectoralis, we observed a transition from the ancestral XX/XY male heterogametic system shared by Esocidae and U. pygmaea to a ZZ/ZW female heterogametic system. This transition also coincided with the loss of amhby. This shift from male to female heterogamety could have been driven by the rise of a new dominant female determinant, leading to the obsolescence and the subsequent loss of the ancestral male MSD gene, similar to the transition of SD documented among the Oryzias and also in the housefly (Kozielska et al., 2008, Myosho et al., 2012).

The other SD transitions that we characterized, those in E. lucius and E. masquinongy, are probably more recent because these transitions are found within populations of the same species. In E. masquinongy, we observed population-specific variation in SD systems, supporting the conservation of an XX/XY system with amhby as the MSD gene in two US populations belonging to the northern lineage, but not in a Quebec population belonging to the Great Lakes lineage (Turnquist et al., 2017). This result suggests that although amhby is still present in the genome of the Great Lakes lineage, it is no longer the MSD gene and that a new population-specific SD mechanism emerged after the split of the lineages. Previously, female heterogamety was inferred for the Great Lakes lineage based on the presence of males in the offspring of gynogenetic females (Dabrowski et al., 2000). With RAD-Seq, we did not find evidence for female-specific genomic regions in the Great Lakes lineage of E. masquinongy. Higher resolution approaches are needed to identify differentiation between male and female genomes to reveal the new SD locus and its interaction with amhby in the Great Lakes lineage.

In E. lucius, we found that amhby is present and completely sex linked in European, Asian, and Alaskan regions, but is not present elsewhere in North America (Figure 5). This finding suggests that amhby functions as an MSD gene in Eurasian and Alaskan populations, but that populations from elsewhere in North America lost amhby together with the entire sex locus. The current geographic distribution of E. lucius results from a post-glacial expansion from three glacial refugia ~0.18 to 0.26 Mya. The North American populations lacking amhby belong to a monophyletic lineage with a circumpolar distribution originating from the same refugia as the other population we surveyed that carry amhby (Skog et al., 2014). Fossil records from Alaska support the idea of an ‘out of Alaska’ North American expansion of E. lucius within the last 100,000 years (Wooller et al., 2015), suggesting that the Y-specific sequences containing amhby were lost during this dispersal period (Figure 5, Appendix 1—figure 7).

Figure 5 with 1 supplement see all

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The loss of the entire sex locus in such a short evolutionary time is unlikely to have resulted from the pseudogenization of the amhby gene, as is the case for the ancestral MSD gene of the Luzon medaka (Myosho et al., 2012). Rather, it is probably the result of colonization by a small pool of females and sex-reversed XX males. Such a founder-effect hypothesis is supported by the fact that North American populations of E. lucius display a much lower genetic diversity compared to other populations from the same lineage (Skog et al., 2014). This hypothesis is also supported by the fact that environmental influence on GSD systems is a well-documented phenomenon in fishes (Baroiller et al., 2009; Chen et al., 2014; Sato et al., 2005) and that XX sex reversal induced by environmental factors has been observed occasionally in captive E. lucius (Pan et al., 2019). Our whole-genome analyses failed to identify any sex-associated signals in these North American populations, meaning that if such a new sex locus exists, it would lack detectable signatures of sequence differentiation, similar to the one-SNP sex locus of some Takifugu species (Kamiya et al., 2012). Whether ESD, which is common among poikilothermic animals including teleosts (Navara, 2018), could be the SD system in these North American populations or whether these populations already have a new GSD system in place is still unresolved. Notably, this Y chromosome loss in natural populations of E. lucius mirrors the loss of the W chromosome in lab strains of zebrafish after just a few decades of selective breeding (Wilson et al., 2014).

A few evolutionary models have been formulated to capture the dynamics of sex chromosome turnover (Vicoso, 2019). The replacement of the ancestral SD locus by a new one could be driven by drift alone, by positive selection (Bull and Charnov, 1977), by sexual antagonistic selection (van Doorn and Kirkpatrick, 2007), or by the accumulation of deleterious mutations at the sex locus (Blaser et al., 2013). In all of these models, the ancestral sex chromosomes would revert to autosomes only when the new SD locus is fixed in the population. However, in North American populations of E. lucius, the ancestral sex chromosome was likely lost due to drift in bottlenecked populations. Interestingly, this process would not require the simultaneous emergence of a new GSD system, given the flexibility of SD mechanisms in teleosts, where environmental cues generate phenotypic sexes in the absence of a GSD system. ESD, which is easily invaded by a new genetic system (Muralidhar and Veller, 2018; van Doorn, 2014), may serve as a transitional state between sex chromosome turnovers.

We found two cases of altered amhby copies. In N. hubbsi and E. niger, amhby is strongly sex linked, which suggests that it is located in a Y-specific region of the genome. In both species, however, the amhby gene lacks parts of the conserved C- and/or N-terminal Amh regions, which are needed for proper protein secretion and interaction between Amh and its receptor (di Clemente et al., 2010). Although we cannot exclude that these are non-functional amhby copies, this hypothesis seems unlikely because the tight sex linkage of amhby in these species would require the independent emergence of a new MSD gene in close proximity to amhby. It is more likely that these copies still function as MSD genes, but with altered protein sequences. A similar example of a truncated amh duplicate acting as an MSD gene is found in the teleost cobalt silverside Hypoatherina tsurugae (Bej et al., 2017). Additional cases of truncated duplicated genes functioning as MSD genes have been described in Salmonids, yellow perch (Perca flavescens), and Atlantic herring (Clupea harengus), suggesting that the preservation of ancestral domains is not necessary for a duplicated protein to assume a novel role (Feron et al., 2020b; Rafati et al., 2020; Yano et al., 2012). These cases are all consistent with domain gains and losses contributing to new protein functions (Moore and Bornberg-Bauer, 2012).

Collectively, our results depict the evolutionary trajectories of a conserved MSD gene in an entire order of vertebrates, highlighting both the potential stability of MSD genes as well as non-differentiated sex chromosomes in some lineages, and the dynamics of species- or population-specific SD evolution in teleost fishes. Our results highlight the importance of careful consideration of the population demographic history of SD systems, and of the potential buffering role of ESD during transitions between genetic SD systems in sex chromosome evolution.

All gene sequences, genomic, Pool-seq and RAD-Seq reads were deposited under the common project number PRJNA634624.

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Author details

1. Qiaowei Pan

   1. INRAE, LPGP, Rennes, France
   2. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8501-0405

2. Romain Feron

   1. INRAE, LPGP, Rennes, France
   2. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
   3. Swiss Institute of Bioinformatics, Lausanne, Switzerland

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft

   Competing interests

   No competing interests declared

3. Elodie Jouanno

   INRAE, LPGP, Rennes, France

   Contribution

   Software, Formal analysis, Investigation, Visualization

   Competing interests

   No competing interests declared

4. Hugo Darras

   Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

   Contribution

   Investigation, Visualization, Writing - review and editing

   Competing interests

   No competing interests declared

5. Amaury Herpin

   INRAE, LPGP, Rennes, France

   Contribution

   Supervision, Investigation, Visualization

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0630-4027

6. Ben Koop

   Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada

   Contribution

   Resources, Supervision, Investigation

   Competing interests

   No competing interests declared

7. Eric Rondeau

   Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada

   Contribution

   Resources, Investigation

   Competing interests

   No competing interests declared

8. Frederick W Goetz

   Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, United States

   Contribution

   Resources, Investigation

   Competing interests

   No competing interests declared

9. Wesley A Larson

   Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, Anchorage, United States

   Contribution

   Resources, Investigation

   Competing interests

   No competing interests declared

10. Louis Bernatchez

    Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

11. Mike Tringali

    Fish and Wildlife Conservation Commission, Florida Marine Research Institute, St. Petersburg, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

12. Stephen S Curran

    School of Fisheries and Aquatic Sciences, Auburn University, Auburn, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

13. Eric Saillant

    Gulf Coast Research Laboratory, School of Ocean Science and Technology, The University of Southern Mississippi, Ocean Springs, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

14. Gael PJ Denys

    1. Laboratoire de Biologie des organismes et écosystèmes aquatiques (BOREA), MNHN, CNRS, IRD, SU, UCN, Laboratoire de Biologie des organismes et écosystèmes aquatiques (BOREA), Paris, France
    2. Unité Mixte de Service Patrimoine Naturelle – Centre d’expertise et de données (UMS 2006 AFB, CNRS, MNHN), Muséum national d’Histoire naturelle, Paris, France

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

15. Frank A von Hippel

    Department of Biological Sciences, Northern Arizona University, Flagstaff, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-9247-0231

16. Songlin Chen

    Yellow Sea Fisheries Research Institute, CAFS, Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, China

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

17. J Andrés López

    College of Fisheries and Ocean Sciences Fisheries, Fairbanks, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

18. Hugo Verreycken

    Research Institute for Nature and Forest (INBO), Brussels, Belgium

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-2060-7005

19. Konrad Ocalewicz

    Department of Marine Biology and Ecology, Institute of Oceanography, University of Gdansk, Gdansk, Poland

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

20. Rene Guyomard

    INRAE, GABI, Jouy-en-Josas, France

    Contribution

    Resources, Formal analysis, Investigation

    Competing interests

    No competing interests declared

21. Camille Eche

    GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France

    Contribution

    Resources, Formal analysis, Investigation

    Competing interests

    No competing interests declared

22. Jerome Lluch

    GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France

    Contribution

    Investigation

    Competing interests

    No competing interests declared

23. Celine Roques

    GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

24. Hongxia Hu

    Beijing Fisheries Research Institute & Beijing Key Laboratory of Fishery Biotechnology, Beijing, China

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

25. Roger Tabor

    U.S. Fish and Wildlife Service, Lacey, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

26. Patrick DeHaan

    U.S. Fish and Wildlife Service, Lacey, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

27. Krista M Nichols

    Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, United States

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

28. Laurent Journot

    Institut de Génomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Montpellier, France

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

29. Hugues Parrinello

    Institut de Génomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Montpellier, France

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

30. Christophe Klopp

    INRAE, Sigenae, Genotoul Bioinfo, Toulouse, France

    Contribution

    Resources, Software, Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-7126-5477

31. Elena A Interesova

    Tomsk State University, Tomsk, Russian Federation

    Contribution

    Resources, Software, Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-1148-6283

32. Vladimir Trifonov

    Institute of Molecular and Cellular Biology, Siberian Branch of the Russian Academy of Sciences, Novosibirsk State University, Novosibirsk, Russian Federation

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

33. Manfred Schartl

    University of Wuerzburg, Developmental Biochemistry, Biocenter, 97074 Würzburg, Germany; and The Xiphophorus Genetic Stock Center, Texas State University, San Marcos, United States

    Contribution

    Conceptualization, Resources, Funding acquisition, Investigation, Project administration, Writing - review and editing

    Competing interests

    No competing interests declared

34. John Postlethwait

    Institute of Neuroscience, University of Oregon, Eugene, United States

    Contribution

    Conceptualization, Funding acquisition, Investigation, Project administration, Writing - review and editing

    Competing interests

    No competing interests declared

35. Yann Guiguen

    INRAE, LPGP, Rennes, France

    Contribution

    Conceptualization, Supervision, Funding acquisition, Investigation, Visualization, Project administration, Writing - review and editing

    For correspondence

    yann.guiguen@inrae.fr

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-5464-6219

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