With some 1 million species and counting, insects may be the most abundant class of animals living today. Their protective exoskeleton, prolific reproductive rate, and wings help their cause, as do the symbiotic bacteria that inhabit their cells, gut, or body cavity. Endocellular symbionts live inside specialized insect cells and provide essential nutrients for their hosts, and this exclusive relationship often means that the evolutionary history of one matches the other. Gut or body cavity symbionts, however, are vulnerable to displacement or attack by other microbes and are thought to have less-exclusive relationships with their hosts. But a new study published in the open access journal PLoS Biology suggests that not all gut symbionts opt for the more promiscuous lifestyle. Takahiro Hosokawa, Takema Fukatsu, and colleagues provide the first evidence of cospeciation between a group of gut symbionts and their insect hosts, plataspid stinkbugs. Not only do their evolutionary histories mirror each other, but the gut symbionts share many of the unique genetic traits typical of endocellular symbionts.
Plataspid stinkbug symbionts live in the bugs' posterior midgut and are vertically transmitted by the mother in symbiont "capsules." When the female lays eggs, small, brown symbiont-filled capsules always appear under the egg mass. Nymph hatchlings ingest symbionts from the capsule. Hosokawa et al. collected 12 populations of stinkbugs, representing three genera and seven species, from several locations in Japan. The researchers analyzed the DNA of the resident bacteria from four of the species and found that each bacterial species was associated with a different stinkbug species and fell into their own class of Proteobacteria, but were closely related to the well-characterized obligate endosymbiont (Buchnera aphidocola) of aphids. The authors also showed that adult stinkcbugs lacking symbionts showed developmental delays, grew smaller, failed to copulate or reproduce, and died prematurely. Just as aphids depend on their endosymbionts, plataspid stinkbugs depend on their gut symbionts to survive. And, like Buchnera, the gut endosymbionts also appear to have co-evolved with their host. The phylogenetic tree of the stinkbugs, the researchers found, "perfectly agreed" with the phylogenetic relationships of the gut symbionts. Moreover, the symbiotic lifestyle that has shaped the genome evolution of endocellular symbionts like Buchnera also applies to these gut symbionts. The authors found the same intriguing pattern of a small genome, a high percentage of A and T nucleotides in their DNA, and accelerated molecular evolution, thought to possibly result from population genetic forces--for example, small population size and bottlenecks.
Hosokawa et al. have named these gut symbionts "Candidatus Ishikawaella capsulata," in honor of Hajime Ishikawa, a pioneer in the molecular study of symbiosis, who recently passed away. With some 530 species and 56 genera in the Plataspidae family, researchers have their work cut out for them as they survey the lineages for a stinkbug without a capsule. But with this unique plataspid stinkbug system, they will be well equipped to study insect symbiosis and its influence on genome evolution.
Citation: Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4(10): e337. DOI: 10.1371/journal.pbio.0040337.
National Institute of Advanced Industrial Science and Technology, Tsukuba
Institute for Biological Resources and Functions
Tsukuba, 305-8566, Japan
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