scholarly journals Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome

2016 ◽  
Vol 113 (52) ◽  
pp. 15036-15041 ◽  
Author(s):  
Sébastien Leclercq ◽  
Julien Thézé ◽  
Mohamed Amine Chebbi ◽  
Isabelle Giraud ◽  
Bouziane Moumen ◽  
...  

Sex determination is a fundamental developmental pathway governing male and female differentiation, with profound implications for morphology, reproductive strategies, and behavior. In animals, sex differences between males and females are generally determined by genetic factors carried by sex chromosomes. Sex chromosomes are remarkably variable in origin and can differ even between closely related species, indicating that transitions occur frequently and independently in different groups of organisms. The evolutionary causes underlying sex chromosome turnover are poorly understood, however. Here we provide evidence indicating that Wolbachia bacterial endosymbionts triggered the evolution of new sex chromosomes in the common pillbug Armadillidium vulgare. We identified a 3-Mb insert of a feminizing Wolbachia genome that was recently transferred into the pillbug nuclear genome. The Wolbachia insert shows perfect linkage to the female sex, occurs in a male genetic background (i.e., lacking the ancestral W female sex chromosome), and is hemizygous. Our results support the conclusion that the Wolbachia insert is now acting as a female sex-determining region in pillbugs, and that the chromosome carrying the insert is a new W sex chromosome. Thus, bacteria-to-animal horizontal genome transfer represents a remarkable mechanism underpinning the birth of sex chromosomes. We conclude that sex ratio distorters, such as Wolbachia endosymbionts, can be powerful agents of evolutionary transitions in sex determination systems in animals.

Cells ◽  
2021 ◽  
Vol 10 (2) ◽  
pp. 291
Author(s):  
Peta Hill ◽  
Foyez Shams ◽  
Christopher P. Burridge ◽  
Erik Wapstra ◽  
Tariq Ezaz

Sex determination directs development as male or female in sexually reproducing organisms. Evolutionary transitions in sex determination have occurred frequently, suggesting simple mechanisms behind the transitions, yet their detail remains elusive. Here we explore the links between mechanisms of transitions in sex determination and sex chromosome evolution at both recent and deeper temporal scales (<1 Myr; ~79 Myr). We studied a rare example of a species with intraspecific variation in sex determination, Carinascincus ocellatus, and a relative, Liopholis whitii, using c-banding and mapping of repeat motifs and a custom Y chromosome probe set to identify the sex chromosomes. We identified both unique and conserved regions of the Y chromosome among C. ocellatus populations differing in sex determination. There was no evidence for homology of sex chromosomes between C. ocellatus and L. whitii, suggesting independent evolutionary origins. We discuss sex chromosome homology between members of the subfamily Lygosominae and propose links between sex chromosome evolution, sex determination transitions, and karyotype evolution.


2016 ◽  
Author(s):  
Céline M.O. Reisser ◽  
Dominique Fasel ◽  
Evelin Hürlimann ◽  
Marinela Dukič ◽  
Cathy Haag-Liautard ◽  
...  

AbstractSex chromosomes can evolve during the evolution of genetic sex determination (GSD) from environmental sex determination (ESD). Despite theoretical attention, early mechanisms involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-GSD animal species have been reported, except for some species of Daphnia, small freshwater crustaceans in which sex is usually determined solely by the environment, but in which a dominant female sex-determining locus is present in some populations. This locus follows Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We now show that the sex-determining genomic region maps to the same low-recombining peri-centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of historical recombination, suggesting a role for selection acting on several genes thereby maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken together, the region determining the NMP phenotype shows characteristics of a sex-related supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of significant additional restriction of recombination between Z and W. The occurrence of the female-determining locus in a pre-existing low recombining region illustrates one possible form of recombination suppression in sex chromosomes. D. magna is a promising model for studying the evolutionary transitions from ESD to GSD and early sex chromosome evolution.


Genes ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 483
Author(s):  
Wen-Juan Ma ◽  
Paris Veltsos

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.


2011 ◽  
Vol 7 (3) ◽  
pp. 443-448 ◽  
Author(s):  
Alexander E. Quinn ◽  
Stephen D. Sarre ◽  
Tariq Ezaz ◽  
Jennifer A. Marshall Graves ◽  
Arthur Georges

Sex in many organisms is a dichotomous phenotype—individuals are either male or female. The molecular pathways underlying sex determination are governed by the genetic contribution of parents to the zygote, the environment in which the zygote develops or interaction of the two, depending on the species. Systems in which multiple interacting influences or a continuously varying influence (such as temperature) determines a dichotomous outcome have at least one threshold. We show that when sex is viewed as a threshold trait, evolution in that threshold can permit novel transitions between genotypic and temperature-dependent sex determination (TSD) and remarkably, between male (XX/XY) and female (ZZ/ZW) heterogamety. Transitions are possible without substantive genotypic innovation of novel sex-determining mutations or transpositions, so that the master sex gene and sex chromosome pair can be retained in ZW–XY transitions. We also show that evolution in the threshold can explain all observed patterns in vertebrate TSD, when coupled with evolution in embryonic survivorship limits.


2021 ◽  
Vol 376 (1832) ◽  
pp. 20200089
Author(s):  
Heiner Kuhl ◽  
Yann Guiguen ◽  
Christin Höhne ◽  
Eva Kreuz ◽  
Kang Du ◽  
...  

Several hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet ( Acipenser ruthenus ). Using chromosome-scale assemblies and pool-sequencing, we first identified an approximately 16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages ( A. sturio, A. oxyrinchus versus A. ruthenus, Huso huso ), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species ( A. gueldenstaedtii, A. baerii ). Conservation of a female-specific sequence for a long period, representing 180 Myr of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.


Genome ◽  
1989 ◽  
Vol 32 (4) ◽  
pp. 500-509 ◽  
Author(s):  
Klaus Rothfels

In many Simuliidae, patterns of spatial and temporal relationships among the most closely related species are more readily interpreted in terms of sympatric speciation than of allopatric speciation. Specific examples are (i) the allotriploid taxa in Gymnopais and other genera, (ii) the black fly faunas of geologically recent islands (Tahiti), and (iii) species in Prosimulium onychodactylum, a prototype of a continental multisibling species complex. A model of sympatric speciation is presented based on coadaptation of polymorphic sex chromosomes in pairs reinforced by progressive development of assortative mating. This model predicts that (i) populations should frequently exhibit sex-chromosome polymorphism, (ii) these sex-chromosome polymorphisms, and autosomal ones, should in some cases display linkage or association disequilibria, (iii) species pairs or complexes should be incurred that differ only in sex chromosomes and that share extensive ancestral autosomal polymorphisms, and (iv) such species should differ in their biology and perhaps their present-day distribution. Recent publications and observations are in accordance, in general, with predictions from the model. Genetic control, e.g., of diapause, larval developmental timing, and niche preference or ethology, could substitute as a basis of incipient cleavage. The evidence for sympatric speciation is purely inferential, but this is equally true for the allopatric interpretation, and in black flies the circumstantial evidence for prevalence of sympatric speciation appears more compelling. This is not to deny the efficacy of allopatry and founder effect in the origin of some species complexes.Key words: sympatric speciation, black fly, evolution.


2017 ◽  
Vol 284 (1854) ◽  
pp. 20162806 ◽  
Author(s):  
Jessica K. Abbott ◽  
Anna K. Nordén ◽  
Bengt Hansson

Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.


2019 ◽  
Author(s):  
Richard P. Meisel ◽  
Pia U. Olafson ◽  
Kiran Adhikari ◽  
Felix D. Guerrero ◽  
Kranti Konganti ◽  
...  

AbstractSex chromosomes and sex determining genes can evolve fast, with the sex-linked chromosomes often differing between closely related species. A substantial body of population genetics theory has been developed and tested to explain the rapid evolution of sex chromosomes and sex determination. However, we do not know why the sex-linked chromosomes differ between some species pairs yet are relatively conserved in other taxa. Addressing this question will require comparing closely related taxa with conserved and divergent sex chromosomes and sex determination systems to identify biological features that could explain these rate differences. Cytological karyotypes suggest that muscid flies (e.g., house fly) and blow flies are such a taxonomic pair. The sex chromosomes appear to differ across muscid species, whereas they are highly conserved across blow flies. Despite the cytological evidence, we do not know the extent to which muscid sex chromosomes are independently derived along different evolutionary lineages. To address that question, we used genomic data to identify young sex chromosomes in two closely related muscid species, horn fly (Haematobia irritans) and stable fly (Stomoxys calcitrans). We provide evidence that the nascent sex chromosomes of horn fly and stable fly were derived independently from each other and from the young sex chromosomes of the closely related house fly (Musca domestica). We present three different scenarios that could have given rise to the sex chromosomes of horn fly and stable fly, and we describe how the scenarios could be distinguished. Distinguishing between these scenarios in future work could help to identify features of muscid genomes that promote sex chromosome divergence.


2021 ◽  
Author(s):  
Monica M Sheffer ◽  
Mathilde M Cordellier ◽  
Martin Forman ◽  
Malte Grewoldt ◽  
Katharina Hoffmann ◽  
...  

Differences between sexes in growth, ecology and behavior strongly shape species biology. In some animal groups, such as spiders, it is difficult or impossible to identify the sex of juveniles. This information would be useful for field surveys, behavioral experiments, and ecological studies on e.g. sex ratios and dispersal. In species with sex chromosomes, sex can be determined based on the specific sex chromosome complement. Additionally, information on the sequence of sex chromosomes provides the basis for studying sex chromosome evolution. We combined cytogenetic and genomic data to identify the sex chromosomes in the sexually dimorphic spider Argiope bruennichi, and designed RT-qPCR sex markers. We found that genome size and GC content of this spider falls into the range reported for the majority of araneids. The male karyotype is formed by 24 acrocentric chromosomes with an X1X20 sex chromosome system, with little similarity between X chromosomes, suggesting origin of these chromosomes by X chromosome fission or early duplication of an X chromosome and subsequent independent differentiation of the copies. Our data suggest similarly sized X chromosomes in A. bruennichi. They are smaller chromosomes of the complement. Our findings open the door to new directions in spider evolutionary and ecological research.


2021 ◽  
Vol 376 (1832) ◽  
pp. 20200109 ◽  
Author(s):  
Ceri Weber ◽  
Blanche Capel

With or without sex chromosomes, sex determination is a synthesis of many molecular events that drives a community of cells towards a coordinated tissue fate. In this review, we will consider how a sex determination pathway can be engaged and stabilized without an inherited genetic determinant. In many reptilian species, no sex chromosomes have been identified, yet a conserved network of gene expression is initiated. Recent studies propose that epigenetic regulation mediates the effects of temperature on these genes through dynamic post-transcriptional, post-translational and metabolic pathways. It is likely that there is no singular regulator of sex determination, but rather an accumulation of molecular events that shift the scales towards one fate over another until a threshold is reached sufficient to maintain and stabilize one pathway and repress the alternative pathway. Investigations into the mechanism underlying sex determination without sex chromosomes should focus on cellular processes that are frequently activated by multiple stimuli or can synthesize multiple inputs and drive a coordinated response. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.


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