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Inherited bacterial symbionts are very common in arthropods, but infection frequency can vary widely among populations. Experiments and interpopulation comparisons suggest that host genetic background might be important in explaining this variation. Our extensive field investigation showed that the infection pattern of the facultative symbiont Cardinium was heterogeneous across geographical populations of the invasive whitefly Bemisia tabaci Mediterranean (MED) in China, with genetic nuclear differences evident in 2 of the populations: 1 with a low infection rate (SD line) and 1 with a high infection rate (HaN line). However, whether the heterogeneous frequency of Cardinium is associated with the host genetic background remains poorly understood. Here, we compared the fitness of the Cardinium‐infected and uninfected sublines with similar nuclear genetic backgrounds from SD and HaN lines, respectively, and further determine whether host extranuclear or nuclear genotype influenced the Cardinium–host phenotype by performing 2 new introgression series of 6 generations between SD and HaN lines (i.e., Cardinium‐infected females of SD were backcrossed with uninfected males of HaN, and vice versa). The results showed that Cardinium provides marginal fitness benefits in the SD line, whereas Cardinium provides strong fitness benefits in the HaN line. Further, both Cardinium and the Cardinium–host nuclear interaction influence the fecundity and pre‐adult survival rate of B. tabaci, whereas the extranuclear genotype does not. In conclusion, our results provide evidence that Cardinium‐mediated fitness effects were closely associated with the host genetic background, which provides a fundamental basis for understanding the mechanism underlying the heterogeneous distribution of Cardinium in B. tabaci MED populations across China. [ABSTRACT FROM AUTHOR]

Aim: The sweet potato whitefly, Bemisia tabaci MED is a globally invasive species that causes serious economic damage to agroecosystems. Despite the significant threat it poses to agricultural and economic crops worldwide, the global perspective of the invasion patterns and genetic mechanisms contributing to the success of this notorious pest is still poorly understood. The objective of this research was to enhance genome and population genetic analyses to better understand the intricate invasion patterns of B. tabaci MED. Location: Samples were collected in native (Spain, Croatia, Bosnia and Herzegovina, Cyprus, and Israel) and invaded regions (China, South Korea and North America). Methods: We first assembled a chromosome‐scale reference genome of B. tabaci MED and then employed the restriction site‐associated 2b‐RAD method to genotype over 20,000 high‐quality single‐nucleotide polymorphisms from 29 geographical populations. Results: A reference genome of B. tabaci MED, with a size of 637.47 Mb, was available. The majority of the assembled sequences (99%) were anchored onto 10 linkage groups, with an N50 size of 58.76 Mb, representing a significant improvement over previous whitefly genome assemblies. We identified rapidly expanded gene families and positively selected genes, probably contributing to successful invasion and rapid adaptation to the new environment. Population genomics analysis showed that three highly differentiated genetic groups were formed, and complex and extensive gene flow occurred across the Mediterranean populations. The genetic admixture patterns in East Asia populations were distinct from those in North America, indicating that they had different source populations. Conclusions: The high‐quality, chromosome‐scale genome of B. tabaci MED offered opportunities for more comprehensive genome‐wide studies and provided solid foundation to the complex introduction events and the differential invasiveness of B. tabaci MED worldwide. [ABSTRACT FROM AUTHOR]

Simple Summary: Bemisia tabaci is a globally notorious agricultural pest due to its highly polyphagous characteristic, its composition as a cryptic species, and its transmission of plant viruses. The whitefly has endosymbiotic bacteria in cells inside their bodies that have strong effects on the host biology. Generally, the geographical distribution of these cryptic species and their endosymbionts' infection patterns are related to ecological factors. In this study, we determined eight cryptic species (MED, MEAM1, Asia I, Asia II 1, Asia II 2, Asia II 6, China 1, and China 6) from 29 geographical localities across China. Native cryptic species were still widespread in the Yangtze River Valley and eastern coastal areas. In addition, we found that the cryptic species distribution and their facultative endosymbionts' infection patterns were closely associated with the geographical and environmental factors, i.e., latitude and annual mean temperature. This work highlights that range expansion of invasive species and host–endosymbiont interactions need to be studied within an environmental and geographic context. The sweetpotato whitefly, Bemisia tabaci species complex, comprises at least 44 morphologically indistinguishable cryptic species, whose endosymbiont infection patterns often varied at the spatial and temporal dimension. However, the effects of ecological factors (e.g., climatic or geographical factors) on the distribution of whitefly and the infection frequencies of their endosymbionts have not been fully elucidated. We, here, analyzed the associations between ecological factors and the distribution of whitefly and their three facultative endosymbionts (Candidatus Cardinium hertigii, Candidatus Hamiltonella defensa, and Rickettsia sp.) by screening 665 individuals collected from 29 geographical localities across China. The study identified eight B. tabaci species via mitochondrial cytochrome oxidase I (mtCOI) gene sequence alignment: two invasive species, MED (66.9%) and MEAM1 (12.2%), and six native cryptic species (20.9%), which differed in distribution patterns, ecological niches, and high suitability areas. The infection frequencies of the three endosymbionts in different cryptic species were distinct and multiple infections were relatively common in B. tabaci MED populations. Furthermore, the annual mean temperature positively affected Cardinium sp. and Rickettsia sp. infection frequencies in B. tabaci MED but negatively affected the quantitative distribution of B. tabaci MED, which indicates that Cardinium sp. and Rickettsia sp. maybe play a crucial role in the thermotolerance of B. tabaci MED, although the host whitefly per se exhibits no resistance to high temperature. Our findings revealed the complex effects of ecological factors on the expansion of the invasive whitefly. [ABSTRACT FROM AUTHOR]