ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp

Abstract

Eurasian brine shrimp (genus Artemia) have closely related sexual and asexual lineages of parthenogenetic females, which produce rare males at low frequencies. Although they are known to have ZW chromosomes, these are not well characterized, and it is unclear whether they are shared across the clade. Furthermore, the underlying genetic architecture of the transmission of asexuality, which can occur when rare males mate with closely related sexual females, is not well understood. We produced a chromosome-level assembly for the sexual Eurasian species A. sinica and characterized in detail the pair of sex chromosomes of this species. We combined this new assembly with short-read genomic data for the sexual species A. sp. Kazakhstan and several asexual lineages of A. parthenogenetica, allowing us to perform an in-depth characterization of sex-chromosome evolution across the genus. We identified a small differentiated region of the ZW pair that is shared by all sexual and asexual lineages, supporting the shared ancestry of the sex chromosomes. We also inferred that recombination suppression has spread to larger sections of the chromosome independently in the American and Eurasian lineages. Finally, we took advantage of a rare male, which we backcrossed to sexual females, to explore the genetic basis of asexuality. Our results suggest that parthenogenesis is likely partly controlled by a locus on the Z chromosome, highlighting the interplay between sex determination and asexuality.

Slower-X: reduced efficiency of selection in the early stages of X chromosome evolution

“…Nonrecombining regions with intermediate or low levels of Y/W degeneration have been described in various taxa ( Charlesworth, 2021 ), e.g. : schistosomes ( Elkrewi et al, 2021 ), frogs ( Furman & Evans, 2018 ), crustaceans ( Elkrewi et al, 2022 ), birds ( Liu et al, 2021 ), fish ( Sardell et al, 2021 ), and plants ( Veltsos et al, 2019 ). It is therefore clear that many young X-linked genes can remain diploid for substantial periods of time.…”

Chromosome-Level Assembly of Artemia franciscana Sheds Light on Sex Chromosome Differentiation

“…While they have yielded important insights into the adaptation to extreme environments, several aspects of their reproductive biology, including the molecular basis of sex determination and the extent of sex chromosome differentiation, are difficult to elucidate without a chromosome-level assembly ( Huylmans et al 2019 ). Currently, the closest relative with a published chromosome-level assembly is the Asian Artemia sinica ( Elkrewi et al 2022 ), from which A. franciscana diverged 30 million years ago ( Baxevanis et al 2006 ; Maniatsi et al 2009 ).…”

“…Artemia are also a great model for sex chromosome evolution, as they have ZW sex chromosomes ( Bowen 1963 ; De Vos et al 2013 ; Elkrewi et al 2022 ; Boyer et al 2023 ). Sex chromosomes are known to evolve from autosomes, when one of them acquires a sex determination gene.…”

“…Recombination is then thought to be lost in a stepwise manner, creating strata of different ages ( Lahn and Page 1999 ; Handley et al 2004 ), but this process is difficult to study in well-differentiated sex chromosomes. An earlier comparison between A. franciscana and A. sinica suggested that younger strata were acquired independently in the 2 lineages, which would make Artemia an ideal model for studying this stepwise process, but the fragmented assembly of A. franciscana limited this analysis ( Elkrewi et al 2022 ). Furthermore, the Artemia genus includes multiple obligate parthenogenetic populations ( Abatzopoulos 2018 ), and the Z chromosome has been implicated in their origin ( Elkrewi et al 2022 ).…”

Genetic drift drives faster-Z evolution in the salmon louseLepeophtheirus salmonis

“…Crustacea are an ancient (∼500mya, Zhang et al 2007), polyphyletic clade (Regier and Shultz 1997) with diverse sex determination systems (Ye et al 2023). Most known categories of sex determination system are represented among the Crustacea, including male (Becking et al 2017) and female (Jiang and Qiu 2013) heterogamety, sequential (Chiba 2007) and simultaneous hermaphroditism (Hessler et al 1995), environmental sex determination (Kato et al 2011), polygenic sex determination (Voordouw et al 2005; Richardson et al 2023), asexual reproduction (Boyer et al 2023), parthenogenesis (Elkrewi et al 2022), as well as control by non-Mendelian genetic elements like Wolbachia (cytoplasmic sex determination, (Cordaux et al 2011). ZW sex determination occurs in three major crustacean clades: Malacostraca (e.g.…”