Intracellular symbionts drive sex ratio in the whitefly by facilitating fertilization and provisioning of B vitamins
- 1 December 2020
- journal article
- research article
- Published by Oxford University Press (OUP) in The ISME Journal
- Vol. 14 (12), 2923-2935
- https://doi.org/10.1038/s41396-020-0717-0
Abstract
Symbionts can regulate animal reproduction in multiple ways, but the underlying physiological and biochemical mechanisms remain largely unknown. The presence of multiple lineages of maternally inherited, intracellular symbionts (the primary and secondary symbionts) in terrestrial arthropods is widespread in nature. However, the biological, metabolic, and evolutionary role of co-resident secondary symbionts for hosts is poorly understood. The bacterial symbiontsHamiltonellaandArsenophonushave very high prevalence in two globally important pests, the whitefliesBemisia tabaciandTrialeurodes vaporariorum, respectively. Both symbionts coexist with the primary symbiontPortierain the same host cell (bacteriocyte) and are maternally transmitted. We found that elimination of bothHamiltonellaandArsenophonousby antibiotic treatment reduced the percentage of female offspring in whiteflies. Microsatellite genotyping and cytogenetic analysis revealed that symbiont deficiency inhibited fertilization in whiteflies, leading to more haploid males with one maternal allele, which is consistent with distorted sex ratio in whiteflies. Quantification of essential amino acids and B vitamins in whiteflies indicated that symbiont deficiency reduced B vitamin levels, and dietary B vitamin supplementation rescued fitness of whiteflies. This study, for the first time, conclusively demonstrates that these two intracellular symbionts affect sex ratios in their whitefly hosts by regulating fertilization and supplying B vitamins. Our results reveal that both symbionts have the convergent function of regulating reproduction in phylogenetically-distant whitefly species. The 100% frequency, the inability of whiteflies to develop normally without their symbiont, and rescue with B vitamins suggests that both symbionts may be better considered co-primary symbionts.Funding Information
- National Natural Science Foundation of China (31871967)
- National Natural Science Foundation of China (31871967)
This publication has 68 references indexed in Scilit:
- Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug SymbiosisCell, 2013
- The Evolution of Genomic Instability in the Obligate Endosymbionts of WhitefliesGenome Biology and Evolution, 2013
- Genome Reduction and Co-evolution between the Primary and Secondary Bacterial Symbionts of PsyllidsMolecular Biology and Evolution, 2012
- Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interfaceProceedings of the National Academy of Sciences of the United States of America, 2012
- An Interdependent Metabolic Patchwork in the Nested Symbiosis of MealybugsCurrent Biology, 2011
- Wolbachia as a bacteriocyte-associated nutritional mutualistProceedings of the National Academy of Sciences of the United States of America, 2009
- Convergent evolution of metabolic roles in bacterial co-symbionts of insectsProceedings of the National Academy of Sciences of the United States of America, 2009
- Hamiltonella defensa , genome evolution of protective bacterial endosymbiont from pathogenic ancestorsProceedings of the National Academy of Sciences of the United States of America, 2009
- Analyzing real-time PCR data by the comparative CT methodNature Protocols, 2008
- Parallel genomic evolution and metabolic interdependence in an ancient symbiosisProceedings of the National Academy of Sciences of the United States of America, 2007