Heterogeneous distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

Abstract

In the isopod Armadillidium vulgare , many females produce progenies with female-biased sex ratios, owing to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and the f element. We investigated the distribution and population dynamics of these SRD and mitochondrial DNA variation in 16 populations from Europe and Japan. Confirming and extending results from the 1990s, we found that the SRD are present at variable frequencies in populations and that the f element is overall more frequent than Wolbachia . The two SRD never co-occur at high frequency in any population, suggesting an apparent mutual exclusion. We also detected Wolbachia or the f element in some males, which probably reflects insufficient titer to induce feminization or presence of masculinizing alleles. Our results are consistent with a single integration event of a Wolbachia genome in the A. vulgare genome at the origin of the f element, which contradicts an earlier hypothesis of frequent losses and gains. We identified strong linkage between Wolbachia strains and mitochondrial haplotypes, but no association between the f element and mitochondrial background. Our results open new perspectives on SRD evolutionary dynamics in A. vulgare , the evolution of genetic conflicts and their impact on the variability of sex determination systems.

Temporal stability of sex ratio distorter prevalence in natural populations of the isopodArmadillidium vulgare

“…We found that 29.9% of individuals carried only the f element, 15.2% carried only Wolbachia , 0.6% carried both SRD and 54.3% carried none. While both SRD were mostly found in females, they were also sometimes present in males, as previously reported (Durand et al ., 2023). Wolbachia -infected individuals carried one of the three previously known Wolbachia strains of A. vulgare : w VulC (n=22), w VulM (n=25) or w VulP (n=83).…”

“…Yet, the f element was the dominant SRD in 4 out of 6 populations we studied and was rising in frequency in Niort (Juchault et al ., 1992). Overall, the f element is more widespread than Wolbachia in A. vulgare populations (Juchault et al ., 1993; Durand et al ., 2023). Previously proposed explanations include a higher fitness cost entailed by Wolbachia relative to the f element and occasional paternal transmission of the f element (which some males carry, Figure 1) enabled by masculinizing epistatic alleles (Juchault et al ., 1992; Rigaud and Juchault, 1993; Rigaud, 1997; Rigaud and Moreau, 2004; Cordaux and Gilbert, 2017).…”

“…To elucidate the potential impact of SRD on the evolution of sex determination in terrestrial isopods, it is essential to clarify the intraspecific evolutionary dynamics of SRD such as Wolbachia and the f element. Previous studies have shown that: (i) Wolbachia and the f element are present at variable frequencies in A. vulgare populations, (ii) the f element is overall more frequent than Wolbachia , (iii) the two SRD usually do not co-occur at high frequency in populations, and (iv) mitochondrial haplotypes (mitotypes) are tightly linked to Wolbachia strains (suggesting stable maternal transmission), but not to the f element (Juchault et al ., 1993; Durand et al ., 2023). These results have provided insights into the spatial distribution of Wolbachia and the f element in A. vulgare ; in the present study, we investigate their temporal dynamics.…”

Widespread infection, diversification and old host associations of Nosema Microsporidia in European freshwater gammarids (Amphipoda)

“…duebeni and G . roeselii or Wolbachia pipientis in the isopod Armadillidium vulgare —are always more frequent in females than in males (which makes sense given that the parasites convert infected males into females) [ 20 , 23 , 89 ]. The high prevalence and above all the homogeneity of Nosema haplogroups across the geographic range of G .…”

“…However, the analysis of infection patterns relative to sexes showed that there were no significant differences in prevalence between sexes in most populations. Yet, parasites that have been shown to be sex ratio distorters-such as N. granulosis in G. duebeni and G. roeselii or Wolbachia pipientis in the isopod Armadillidium vulgare-are always more frequent in females than in males (which makes sense given that the parasites convert infected males into females) [20,23,89]. The high prevalence and above all the homogeneity of Nosema haplogroups across the geographic range of G. balcanicus is therefore puzzling.…”