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

Abstract

Microbial endosymbiosis is widespread in animals, with major ecological and evolutionary implications. Successful symbiosis relies on efficient vertical transmission through host generations. However, when symbionts negatively affect host fitness, hosts are expected to evolve suppression of symbiont effects or transmission. Here, we show that sex chromosomes control vertical transmission of feminizing Wolbachia endosymbionts in the isopod Armadillidium nasatum. Theory predicts that the invasion of an XY/XX species by cytoplasmic sex ratio distorters is unlikely because it leads to fixation of the unusual (and often lethal or infertile) YY genotype. We demonstrate that A. nasatum X and Y sex chromosomes are genetically highly similar and that YY individuals are viable and fertile, thereby enabling Wolbachia spread in this XY-XX species. Nevertheless, we show that Wolbachia cannot drive fixation of YY individuals, because infected YY females do not transmit Wolbachia to their offspring, unlike XX and XY females. The genetic basis fits the model of a Y-linked recessive allele (associated with an X-linked dominant allele), in which the homozygous state suppresses Wolbachia transmission. Moreover, production of all-male progenies by infected YY females restores a balanced sex ratio at the host population level. This suggests that blocking of Wolbachia transmission by YY females may have evolved to suppress feminization, thereby offering a whole new perspective on the evolutionary interplay between microbial symbionts and host sex chromosomes.

Fig 1. Identification of sex-specific contigs in the A. nasatum genome assembly.

Frequency distribution of CQ (a) and YGS (b) scores calculated for each contig and scaffold of the assembly. (c) Comparison of CQ and YGS scores. Each dot corresponds to one contig or scaffold (those with CQ > 2 are not represented). The red box contains 78 contigs with CQ ≤ 0.35 and YGS ≥ 35%. CQ, Chromosome Quotient; YGS, Y chromosome Genome Scan.

Fig 2. A. nasatum pedigree used to track inheritance of the Y chromosome and Wolbachia.

The pedigree spans three generations (F0–F2) and comprises 62 individuals (35 males and 27 females) for which sex chromosome genotype (XX, XY, or YY) was identified and 15 F1 females (not included in the molecular analyses; dotted circle). Males are shown as squares, and females are shown as circles. Individuals carrying Wolbachia are shown in purple. Progeny identifiers are shown in gray. Sex chromosome genotype of individuals marked with an orange star (34 males and two females) was also assessed with a quantitative PCR assay.

Fig 3. Boxplot of Wolbachia transmission rate from mother to offspring (measured as the frequency of Wolbachia-carrying individuals in each progeny) according to mother’s sex chromosome genotype.

The analysis is based on 16 progenies (n), in which Wolbachia presence was tested in ≥10 individuals (the underlying data for this figure can be found in Table 2). Thick lines and boxes depict median and interquartile range, respectively. Whiskers are bounded to the most extreme data point within the 1.5 interquartile range. Plots marked with the same letter (a, b) are not statistically different from each other (Kruskal-Wallis test followed by pairwise comparison Dunn test).

Fig 4. Evolutionary consequences of a cytoplasmic sex ratio distorter at the population level.

(a) Equilibrium frequencies of X chromosome (pink line), Y chromosome (blue line), and distorter (dashed line), according to distorter transmission rate in XX and XY females (YY females do not transmit the distorter). (b) Evolution of the frequencies of females (solid lines) and individuals carrying the distorter (dashed lines) through time, with a distorter transmission rate of 0.9. Green: YY females do not transmit the distorter (only XX and XY females do); orange: all females transmit the distorter.