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What Makes Mealybugs Such Effective Agricultural Pests?

Science The Wire

Mealybugs are insects covered with a mealy or cottony wax secretion. Known also as scale insects, mealybugs are serious agricultural pests. They attach to the host plant’s surface and suck its sap.  Moreover, the infested produce looks unappetising. All of this exacts a heavy economic toll on farmers and horticulturists. In 2018, the papaya mealybug reduced papaya yield in Kenya by about 57%. Bacteria act “hand in glove” in diverting plant resources to the insect.

Most mealybug cells are descended from the zygote formed when the mother’s egg is fertilised by the father’s sperm. Both eggs and sperm contain a single copy of the mealybug genome.  That is, they are haploid. The egg is a large cell. It is one of four haploid cells made in the female when a cell called the oocyte undergoes the division called meiosis. The other three post-meiotic cells are much smaller, and are called polar bodies. In males, meiosis acts on the spermatocyte and produces four equal-sized haploid spermatids. The spermatids then differentiate into spermatozoa. The zygote, and cells descended from it, contain two sets of the genome (one apiece from egg and sperm), and hence are diploid. We do not know what determines how a zygote develops into either a male or a female.

In humans and most other animals the polar bodies are lost. In the mealybug, however, they make cells called bacteriocytes. Bacteriocytes are genetically different from the insect’s diploid cells. In the citrus mealybug, Planococcus citri (hereafter referred to as PCIT) the bacteriocytes are pentaploid. They are produced by fusion of a zygote-derived diploid cell with a triploid cell made by fusion of the three polar bodies. Several bacteriocytes together constitute the bacteriome which sits in the body cavity.

Sibling mealybugs have genetically identical bacteriocytes, while their diploid cells share only 75% genetic identity. This is because the paternally-derived chromosomes are inactive in males and not passed on to the sperm. Therefore, all of a male’s sperm inherit the same genome whereas a female’s eggs share only 50% of the maternal genome.

Symbiotic bacteria

The bacteriocyte provides a congenial residence for symbiotic betaproteobacterium bacteria. The betaproteobacteria, in turn, are a residence for gammaproteobacterium bacteria. In PCIT, the betaproteobacterium is Tremblaya princeps and the gammaproteobacterium, Moranella endobia. During embryonic development, bacteria from the mother’s bacteriome migrate to populate the embryo’s bacteriome. The bacteria enable the host to synthesise amino acids and vitamins missing from the nutritionally poor plant sap. This enables the insect to thrive in an otherwise unpromising ecological niche.

Variations exist on this theme. In the whitefly Bemisia tabaci, the bacteriocytes are immortal polyploid insect cells passed down the maternal lineage along with their bacterial passengers.  These cells are only remotely related to the other cells of the insect body.

Why are bacteriocytes genetically different from the other cells? Since sperm do not transmit bacteria, the bacteria see a male as a dead end. In many mealybug species the bacteria induce male-killing or parthenogenesis to increase their representation in the next generation via the female germline.  Parthenogenetic embryos develop from unfertilised egg cells. Haploid nuclei produced following the first post-meiotic division fuse to restore the diploid female “zygote”. The genetic constitution of PCIT and Bemisia tabaci bacteriocytes might make it difficult for bacteria to infer their host’s sex, and thus preserve males from bacterially-induced elimination.

The rabbit hole

Unlike free-living bacteria, symbiotic bacteria are unable to exchange genes with other lineages of their species. Consequently, they accumulate mutations with time and their genome degenerates. Tremblaya princeps has one of the smallest known bacterial genomes. Functions missing from it are provided for by genes in the Moranella endobia and PCIT genomes. On the other hand, any bacterial genes lucky enough to be transferred from the bacterial to the host genome become exposed to the insect sexual cycle, and thus are saved from degeneration. The PCIT genome contains many genes acquired by transfer from long-lost bacteria, presumably, ancestral symbionts.

Tremblaya bacteria in the mealybug Pseudococcus longispinus contained two gammaproteobacterial endosymbionts mixed together. Both gammaproteobacterial genomes contained thousands of mutationally inactivated genes, consistent with the shift from a free-living to endosymbiotic lifestyle. Pathways for biosynthesis of key metabolites were partitioned among the two gammaproteobacterial genomes, the Tremblaya genome, and the ancestrally-acquired bacterial genes in the nuclear genome.

Comparing the two gammaproteobacterial genomes with genomes of their free-living relatives suggested that the gammaproteobacteria were acquired less than a million years ago. This is relatively recent, considering that humans and chimpanzees diverged from each other more than 4 million years ago. Thus, it is apparently not too challenging to replace the innermost bacteria. The change might even allow the host to access a novel and previously inaccessible food source. Mealybugs have become such effective agricultural pests thanks to their nested ‘bug (gammaproteobacteria) in a bug (betaproteobacteria) in a bug (bacteriocyte) in a bug (diploid insect)’ organisation.

D.P. Kasbekar is a retired scientist.


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