Evolutionary Genomics of Sex

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Evolution and genomic signature of early-stage sex chromosomes

In sharp contrast to model organisms with degenerated Y/W chromosomes, many reptiles, fish and amphibians have mostly undifferentiated sex chromosomes and exhibit dynamics of birth and death of sex chromosomes. Why and how early-stage sex chromosomes and frequent turnovers are so prevalent across eukaryotes remains mysterious. This also raises pressing questions on alternative mechanisms leading to sex chromosome recombination arrest and sex chromosome stability.
Frogs are ideal systems to study this because they have mostly early-stage sex chromosomes and frequent turnovers. We use frog systems to study the forces and mechanisms driving sex chromosome recombination suppression, the evolutionary origin and frequent turnovers of sex chromosomes, and their genomic signatures.

Early-stage sex chromosome evolution in blue dotted square.
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Evolution and genetic mechanism of sexual dimorphism in recombination

Achiasmy is the lack of meiotic recombination and always occurs in the heterogametic sex. It has evolved at least 29-34 times independently in animals. Extreme heterochiasmy, such as sex-specific telomere-restricted recombination, has been documented in many frog lineages and some fish species, always associates with the heterogametic sex. Sexual dimorphism in recombination may be a by-product of mechanistic differences between meiosis in males and females, or it may be adaptive and selected to promote tight linkage of beneficial alleles on the Y or W.
Neither of these hypotheses can adequately explain sex differences in recombination in all animals. In many species, sex differences in recombination can vary in degree and direction even between closely related species. We aim to understand the pattern and mechanism of extreme heterochiasmy, and the interplay between the extreme heterochiasmy, sex chromosome recombination arrest, and evolutionary dynamics of sex chromosomes.

Figure: Schematic of recombination rate along each chromosome in both sexes.
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The genetic mechanism of sex determination

Sex determination is a fundamental developmental process to determine one individual development as a female or a male. There is a surprising diversity and variability in sex-determining mechanisms among eukaryotes. Unlike stable sex chromosomes in most mammals and birds, sex chromosomes have been found to go through frequent turnovers in certain lineages of reptiles, many amphibians and teleost fishes. The reason that sex determination is so labile in these lineages remains unresolved.

Identifying (master) sex-determining genes within species (with intra-species polymorphism in sex determination), across closely related species, and among various taxa within a phylogenetic framework is the first step towards answering this question. In vertebrates, it is crucial to investigate the degree of evolutionary plasticity of the gonadal differentiation pathway across lineages.
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Figure: Main genes associated with gonadal sex determination in vertebrates (Herpin & Schartl, 2015. EMBO Rep. 16:1260-74).

Genetics of endosymbionts manipulation of host reproduction

Endosymbionts such as Wolbachia, Cardinium, Rickettsia and Spiroplasma can manipulate host reproduction and host sex determination. Infected females produce a highly female-biased offspring sex ratio, which enhance the endosymbiont transmission. 4 major reproductive manipulation types include cytoplasmic incompatibility, parthenogenesis, male killing and feminisation.

The underlying molecular mechanism, i.e. how endosymbionts interfere with host sex determination in terms of host developmental timing, alternation of sex determination and modification of sexual differentiation pathways, is poorly understood.
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Figure: Endosymbionts manipulation of host reproduction throughout development and sex-determining pathway (Ma et al. 2014. Sex. Dev. 8:1-3).