The Costs and Benefits of Two Secondary Symbionts in a Whitefly Host Shape Their Differential Prevalence in the Field

Abstract

Insects commonly harbor maternally inherited intracellular symbionts in nature, and the microbial partners often exert influence on host reproduction and fitness to promote their prevalence. Here, we investigated composition of symbionts and their biological effects in the invasive Bemisia tabaci MED species of a whitefly complex. Our field surveys revealed that populations of the MED whitefly, in addition to the primary symbiont Portiera, mainly contain two secondary symbionts Hamiltonella, which is nearly fixed in the host populations, and Cardinium with infection frequencies ranging from 0 to 86%. We isolated and established Cardinium-positive and Cardinium-free whitefly lines with a similar nuclear genetic background from a field population, and compared performance of the two whitefly lines. The infection of Cardinium incurred significant fitness costs on the MED whitefly, including reduction of fecundity and egg viability as well as delay in development. We then selectively removed Hamiltonella from the Cardinium-free whitefly line and compared performance of two whitefly lines, one harboring both Portiera and Hamiltonella and the other harboring only Portiera. While depletion of Hamiltonella had little or only marginal effects on the fecundity, developmental rate, and offspring survival, the Hamiltonella-free whitefly line produced very few female offspring, often reducing the progeny female ratio from about 50% to less than 1%. Our findings indicate that the varying costs and benefits of the association between these two symbionts and the MED whitefly may play an important role in shaping their differential prevalence in the field.

Ecological Factors Associated with the Distribution of Bemisia tabaci Cryptic Species and Their Facultative Endosymbionts

“…was 92.3% in MED, 71.6% in MEAM1, 0.13% in Asia I, and 3.57% in China 1. The results regarding the infection frequency of endosymbionts among cryptic species were consistent with previous reports [ 17 , 61 , 62 ].…”

Heterogeneous distribution of Cardinium in whitefly populations is associated with host nuclear genetic background

“…Our data show that Cardinium infection frequency was not uniform in B. tabaci MED populations across China according to 2 field investigations completed during 2012 and 2021, with a higher prevalence observed in South China and a lower prevalence recorded in North China. These findings were consistent with previous field surveys (Pan et al, 2012;Shan & Liu, 2021). A similar phenomenon was found in another cryptic species (B. tabaci Middle East Asia Minor 1) with its facultative symbiont Rickettsia.…”

“…However, previous work has demonstrated that Cardinium infection confers significant fitness costs to B. tabaci MED, including weaker competitive ability, reductions in fecundity and egg survival rate, and delay in development (Fang et al. , 2014; Shan & Liu, 2021). It suggests a complex nature of the close symbiotic associations between Cardinium and the host whitefly.…”

“…The large-scale field investigation showed that the frequency of Cardinium infection is heterogeneous across China (e.g., almost 100% in Hainan Province and <20% in Shandong Province) (Chu et al, 2011;Pan et al, 2012). Similarly, a recent study reported that Cardinium occurred extensively in B. tabaci MED, but that infection frequencies were comparatively low and varied widely across field populations, possibly in association with Cardinium-mediated host fitness (Shan & Liu, 2021). Although heterogeneous Cardinium frequency in spatiotemporal field surveys was evident in B. tabaci MED across China, the reason for this remains poorly understood.…”

The gut bacterium Serratia marcescens mediates detoxification of organophosphate pesticide in Riptortus pedestris by microbial degradation

“…S. marcescens presence in insect midguts was detected using specific PCR primers targeting the bacterium's 16S rRNA gene with the forward primer Ser16S-F (5'-CCTTC GGG TTG TA A AGCACT-3′) and the reverse primer Ser16S-R (5'-TA AGG TTC TTC GCG TTGCAT-3′) after 5 days. The insect midgut was dissected, and total DNA was extracted from individual midguts with Lysis buffer containing Tris-HCl, EDTA Nonidet P-40 and proteinase K as described previously (Shan & Liu, 2021). The resulting PCR product's size and quality were confirmed using 1% agarose gel electrophoresis.…”