Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod

Abstract

18 19 Microbial endosymbiosis is widespread in animals, with major ecological and evolutionary 20 implications. Successful symbiosis relies on efficient vertical transmission through host generations. 21 However, when symbionts negatively affect host fitness, hosts are expected to evolve suppression of 22 symbiont effects or transmission. Here we show that sex chromosomes control vertical transmission 23 of feminizing Wolbachia endosymbionts in the isopod Armadillidium nasatum. Theory predicts that 24 the invasion of an XY/XX species by cytoplasmic sex ratio distorters is unlikely because it leads to 25 fixation of the unusual (and often lethal or infertile) YY genotype. We demonstrate that A. nasatum X 26 and Y sex chromosomes are genetically highly similar and YY individuals are viable and fertile, 27 thereby enabling Wolbachia spread in this XY-XX species. Nevertheless, we show that Wolbachia 28 cannot drive fixation of YY individuals because infected YY females do not transmit Wolbachia to 29 their offspring, unlike XX and XY females. The genetic basis fits the model of a Y-linked recessive 30 allele (associated with an X-linked dominant allele), in which the homozygous state suppresses 31 Wolbachia transmission. Moreover, production of all-male progenies by infected YY females restores 32 a balanced sex ratio at the host population level. This suggests that blocking of Wolbachia 33 transmission by YY females may have evolved to suppress feminization, thereby offering a whole 34 new perspective on the evolutionary interplay between microbial symbionts and host sex 35 chromosomes. 36 37 Keywords 38 39 Male heterogamety, sex chromosomes, endosymbiont, sex ratio distorter, Wolbachia, genetic 40 conflicts, feminization, genome sequencing 41 65degeneration process also causes the formation of pseudogenes and gene loss, resulting in increasing 66 differentiation of sex chromosomes over time. This is well illustrated by the human X and Y sex 67 chromosomes, which dramatically differ in size and gene content [19]. 68 Arthropods host a diverse array of intracellular symbionts, including bacteria (such as 69Wolbachia, Cardinium, Rickettsia, Spiroplasma and others) and unicellular eukaryotes 70 (microsporidia), that are able to distort host sex ratios towards females [9,10]. The evolutionary 71 impact of cytoplasmic sex ratio distorters on host sex determination systems has been particularly 72 investigated in terrestrial isopods (crustaceans). This is because both female and male heterogametic 73 systems of sex chromosomes are found in this speciose taxonomic group [20] and many species are 74 females are both viable and fertile. Nevertheless, Wolbachia cannot drive the loss of the X 109 chromosome because infected YY females do not transmit Wolbachia to their offspring, unlike XX 110 and XY females. As infected YY females produce all-male progenies, a balanced sex ratio is 111 maintained at the host population level despite the presence of feminizing Wolbachia, suggesting 112 that blocking of Wolbachia transmission b...