Endosymbiont diversity in natural populations of Tetranychus mites is rapidly lost under laboratory conditions

Abstract

Although the diversity of bacterial endosymbionts in arthropods is well documented, whether and how such diversity is maintained remains an open question. We investigated the temporal changes occurring in the prevalence and composition of endosymbionts after transferring natural populations of Tetranychus spider-mites from the field to the laboratory. These populations, belonging to three different Tetranychus species (T. urticae, T. ludeni and T. evansi) carried variable infection frequencies of Wolbachia, Cardinium, and Rickettsia. We report a rapid change of the infection status of these populations after only 6 months of laboratory rearing, with an apparent loss of Rickettsia and Cardinium, while Wolbachia apparently either reached fixation or was lost. We show that Wolbachia had variable effects on host longevity and fecundity, and induced variable levels of cytoplasmic incompatibility (CI) in each fully infected population, despite no sequence divergence in the markers used and full CI rescue between all populations. This suggests that such effects are largely dependent upon the host genotype. Subsequently, we used these data to parameterize a theoretical model for the invasion of CI-inducing symbionts in haplodiploids, which shows that symbiont effects are sufficient to explain their dynamics in the laboratory. This further suggests that symbiont diversity and prevalence in the field are likely maintained by environmental heterogeneity, which is reduced in the laboratory. Overall, this study highlights the lability of endosymbiont infections and draws attention to the limitations of laboratory studies to understand host-symbiont interactions in natural populations.

Wolbachiaand host intrinsic reproductive barriers contribute additively to post-mating isolation in spider mites

“…Overall, we found higher levels of female embryonic mortality relative to controls (FM corr index; cf. Methods) in all crosses using Wolbachia-infected red-form males, either crossed with uninfected red-form females (as found by 2020b), or with green-form females independently of their Wolbachia infection status (from 22.2 to 42.7% on average; Main cross effect: χ 2 26 =506.20, p<0.0001; model 1.3; Figure 2b). In addition, there were no significant differences among these crosses (χ 2 7 =8.76, p=0.27; despite a tendency for Ri1 males Note that crosses between infected females and uninfected males (category 5; Figure S1) recapitulate the pattern observed in crosses between uninfected females and uninfected males (categories 1 and 3).…”

“…Breeuwer and Werren 1990; Navajas et al 2000; Vala et al 2000; Vavre et al 2001) or embryonic mortality of fertilized offspring ( i.e. only females in haplodiploids, hence FM-type incompatibility; Vavre et al 2000; Vala et al 2002; Gotoh et al 2007; Suh et al 2015; Zélé et al 2020b), we used indexes adapted from Poinsot et al (1998; see also Cattel et al 2018; Zélé et al 2020). MD-type incompatibility was computed as the proportion of sons produced in each cross relative to the control crosses: where MD obs = number of F1 males/total number of eggs, and CCMD (calculated as MD obs ) is the mean proportion of F1 males observed in control crosses ( i.e.…”

“…Gotoh et al 2003;Perrot-Minnot et al 2002). In most cases, as in diploid species, eggs from uninfected females fail to hatch when fertilized by sperm from Wolbachia-infected males, but wCI affects only the female offspring because males arise from unfertilized eggs (Female mortality -FM-CI type incompatibility; Breeuwer 1997;Vala et al 2002;Gotoh et al 2007;Xie et al 2010;Suh et al 2015;Bing et al 2019;Zélé et al 2020b). In other cases, wCI leads to complete elimination of the paternal set of chromosomes after fertilization of the egg, which successfully develops as a viable haploid male instead of female (Male development -MD-type incompatibility; Vala et al 2000;Perrot-Minnot et al 2002;Gotoh et al 2003).…”

“…In both cases, the penetrance of wCI (i.e. the number of embryos affected) greatly varies among populations (from 0 to more than 90% for FM-type and from 0 to 100% for FMtype wCI; Perrot-Minnot et al 2002;Vala et al 2002;Gotoh et al 2007;Xie et al 2010;Suh et al 2015;Zélé et al 2020b), though the origin (i.e. Wolbachia strain, host genetic background, or both) of such variability in wCI patterns and penetrance is still unknown in spider mites.…”

Consequences of population structure for sex allocation and sexual conflict

“…All populations were treated with antibiotics to ensure that they were free of bacterial endosymbionts, known to be sex ratio distorters (Breeuwer 1997). The sex ratio of each individual population ranges from 0.22 to 0.40 (Zélé et al 2020). In November 2015, more than 50 females from each of the 10 populations were transferred to the University of Montpellier and mixed to form a genetically diverse population to seed the experiment (hereafter called the ‘ancestral population’).…”