Independent Origin of XY and ZW Sex Determination Mechanisms in Mosquitofish Sister Species

Kottler, Verena A.; Féron, Romain; Nanda, Indrajit; Klopp, Christophe; Du, Kang; Kneitz, Susanne; Helmprobst, Frederik; Lamatsch, Dunja K.; Roques, Céline; Lluch, Jérôme; Journot, Laurent; Parrinello, Hugues; Guiguen, Yann; Schartl, Manfred

doi:10.1534/genetics.119.302698

Cited by 35 publications

(41 citation statements)

References 104 publications

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“…Genetic-controlled sex determination systems in fish are variable, ranging from XX/XY to ZZ/ZW [ 68 ]. Fish generally do not have highly morphologically differentiated sex chromosomes, making it difficult to distinguish between autosomes and sex chromosomes.…”

Section: Resultsmentioning

confidence: 99%

“…Gambusia holbrooki and G. affinis are so closely related that for a long time, biologists thought they were the same species. Phylogenetic analyses estimated that their divergence time was ∼2–7 Mya [ 69 , 73 , 74 ], and other researchers showed that the XY and ZW sex determination mechanisms had independent origins in G. holbrooki and G. affinis , respectively [ 68 ]. Therefore, we speculate that the differentiation of Z and W sex chromosomes is a very recent event.…”

Section: Resultsmentioning

confidence: 99%

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Chromosome-level genome assembly of the female western mosquitofish (Gambusia affinis)

et al. 2020

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Background The western mosquitofish (Gambusia affinis) is a sexually dimorphic poeciliid fish known for its worldwide biological invasion and therefore an important research model for studying invasion biology. This organism may also be used as a suitable model to explore sex chromosome evolution and reproductive development in terms of differentiation of ZW sex chromosomes, ovoviviparity, and specialization of reproductive organs. However, there is a lack of high-quality genomic data for the female G. affinis; hence, this study aimed to generate a chromosome-level genome assembly for it. Results The chromosome-level genome assembly was constructed using Oxford nanopore sequencing, BioNano, and Hi-C technology. G. affinis genomic DNA sequences containing 217 contigs with an N50 length of 12.9 Mb and 125 scaffolds with an N50 length of 26.5 Mb were obtained by Oxford nanopore and BioNano, respectively, and the 113 scaffolds (90.4% of scaffolds containing 97.9% nucleotide bases) were assembled into 24 chromosomes (pseudo-chromosomes) by Hi-C. The Z and W chromosomes of G. affinis were identified by comparative genomic analysis of female and male G. affinis, and the mechanism of differentiation of the Z and W chromosomes was explored. Combined with transcriptome data from 6 tissues, a total of 23,997 protein-coding genes were predicted and 23,737 (98.9%) genes were functionally annotated. Conclusions The high-quality female G. affinis reference genome provides a valuable omics resource for future studies of comparative genomics and functional genomics to explore the evolution of Z and W chromosomes and the reproductive developmental biology of G. affinis.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Chromosome-level genome assembly of the female western mosquitofish (Gambusia affinis)

et al. 2020

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“…Recent findings indicated that these transitions among heterogametic systems can be favored by haploid selection ( Scott et al, 2018 ). Shifts between different sex chromosome systems (XY ↔ ZW) are also well documented across several clades of animal species and appear to be a common phenomenon, especially in reptiles, frogs, and fishes ( Vicoso et al, 2013 ; Bachtrog et al, 2014 ; Zhou et al, 2014 ; Jeffries et al, 2018 ; Pennell et al, 2018 ; Kottler et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

The Diversity and Dynamics of Sex Determination in Dioecious Plants

Montalvão¹,

Kersten²,

Fladung³

et al. 2021

Front. Plant Sci.

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The diversity of inflorescences among flowering plants is captivating. Such charm is not only due to the variety of sizes, shapes, colors, and flowers displayed, but also to the range of reproductive systems. For instance, hermaphrodites occur abundantly throughout the plant kingdom with both stamens and carpels within the same flower. Nevertheless, 10% of flowering plants have separate unisexual flowers, either in different locations of the same individual (monoecy) or on different individuals (dioecy). Despite their rarity, dioecious plants provide an excellent opportunity to investigate the mechanisms involved in sex expression and the evolution of sex-determining regions (SDRs) and sex chromosomes. The SDRs and the evolution of dioecy have been studied in many species ranging from Ginkgo to important fruit crops. Some of these studies, for example in asparagus or kiwifruit, identified two sex-determining genes within the non-recombining SDR and may thus be consistent with the classical model for the evolution of dioecy from hermaphroditism via gynodioecy, that predicts two successive mutations, the first one affecting male and the second one female function, becoming linked in a region of suppressed recombination. On the other hand, aided by genome sequencing and gene editing, single factor sex determination has emerged in other species, such as persimmon or poplar. Despite the diversity of sex-determining mechanisms, a tentative comparative analysis of the known sex-determining genes and candidates in different species suggests that similar genes and pathways may be employed repeatedly for the evolution of dioecy. The cytokinin signaling pathway appears important for sex determination in several species regardless of the underlying genetic system. Additionally, tapetum-related genes often seem to act as male-promoting factors when sex is determined via two genes. We present a unified model that synthesizes the genetic networks of sex determination in monoecious and dioecious plants and will support the generation of hypothesis regarding candidate sex determinants in future studies.

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“…While micromelanophores differentiate in waves during embryonic stages to create the base pigmentation pattern, macromelanophores begin differentiation simultaneously and do so later in the fish's life to create spotting patterns (Humm and Young, 1956;Vielkind et al, 1976. Macromelanophores are 150-300 µm in diameter, approximately three times the size of micromelanophores measured in G. holbrooki (Regan, 1961;Kottler et al, 2020). Unlike micromelanophores, macromelanophores do not appear to have distance-dependent regulation, so they can overlap each other to form larger spots or blotches Anders et al, 1984).…”

Section: Pigment Cellsmentioning

confidence: 99%

“…Unlike micromelanophores, macromelanophores do not appear to have distance-dependent regulation, so they can overlap each other to form larger spots or blotches Anders et al, 1984). Both melanophore types have dendritic or stellate shapes, but macromelanophores have Myers, 1925;Regan, 1961;Angus, 1989;Horth, 2006;Kottler et al, 2020 Limia Haskins et al, 1960;Schultz and Kallman, 1968;Turner et al, 1980;Schartl et al, 1997;Lampert et al, 2007;Nanda et al, 2007;Lamatsch et al, 2010 Atz, 1962;Zander, 1965Zander, , 1967Kallman, 1971;Rauchenberger et al, 1990 Carbomaculatus, spotted Atz, 1962;Kallman and Atz, 1966;Kallman, 1975;Franck et al, 1998;Weis and Schartl, 1998;Walter et al, 2006 X. maculatus Pulchra, spotted X. maculatus (Up-2) with spotted pattern-4 2…”

Section: Pigment Cellsmentioning

confidence: 99%

The Biology of Polymorphic Melanic Side-Spotting Patterns in Poeciliid Fishes

Zerulla

Stoddard

2021

Front. Ecol. Evol.

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Melanin-based color patterns are an emerging model for studying molecular and evolutionary mechanisms driving phenotypic correlations. Extensive literature exists on color patterns and their correlated traits in the family Poeciliidae, indicating that these fishes are tractable models. We review the biology of polymorphic melanic side-spotting patterns characterized by macromelanophores forming irregular spotted patterns across fishes’ flanks. These patterns are present in the genera Gambusia, Limia, Phalloceros, Poecilia, and Xiphophorus. Their presence is controlled by dominant genes on autosomes or sex chromosomes. Variation in expression is under polygenic control; however, these genes’ identities are still largely unknown. In some Gambusia holbrooki and Poecilia latipinna, expression is dependent on low temperature exposure, but underlying molecular mechanisms are unknown. Spotted fish develop melanoma in rare cases and are a well-developed model for melanoma research. Little is known about other physiological correlates except that spotted G. holbrooki males exhibit higher basal cortisol levels than unspotted males and that metabolic rate does not differ between morphs in some Xiphophorus species. Behavioral differences between morphs are widespread, but specific to population, species, and social context. Spotted G. holbrooki males appear to be more social and more dominant. Juvenile spotted G. holbrooki have lower behavioral flexibility, and spotted X. variatus exhibit greater stress resistance. Findings conflict on whether morphs differ in sexual behavior and in sexual selection by females. Melanic side-spotting patterns are uncommon (<30%) in populations, although extreme high-frequency populations exist. This low frequency is surprising for dominant genes, indicating that a variety of selective pressures influence both these patterns and their correlated traits. Little is known about reproductive life history traits. Spotted G. holbrooki are larger and have higher survival when uncommon, but underlying mechanisms remain unknown. Spotted morphs appear to have a strong selective advantage during predation. Predators prefer to attack and consume unspotted morphs; however, this preference disappears when spotted G. holbrooki males are common, indicating negative frequency-dependent selection. Spotted morphs are preferred socially under turbid conditions, but other environmental factors that shape phenotypic correlations and morph fitness have not been studied. Finally, we present questions for future studies on melanic side-spotting patterns.

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Independent Origin of XY and ZW Sex Determination Mechanisms in Mosquitofish Sister Species

Cited by 35 publications

References 104 publications

Chromosome-level genome assembly of the female western mosquitofish (Gambusia affinis)

Chromosome-level genome assembly of the female western mosquitofish (Gambusia affinis)

The Diversity and Dynamics of Sex Determination in Dioecious Plants

The Biology of Polymorphic Melanic Side-Spotting Patterns in Poeciliid Fishes

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