Genetical and Biochemical Interactions between the Host and Its Endocytobiotes in the Weevils Sitophilus (Coleoptere, Curculionidae) and Other Related Species

Nardon, P.; Grenier, Anne-Marie

doi:10.1007/978-3-642-73154-9_18

Cited by 30 publications

(19 citation statements)

References 28 publications

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“…The bottleneck experienced by 'Ca. S. philanthi' during vertical transmission is significantly more severe than in most other symbiotic systems investigated so far: The symbiont populations of aphids (Acyrthosiphon pisum), weevils (Sitophilus oryzae), and stinkbugs (Megacopta punctatissima) suffer reductions of 1.6 9 10 -2 -4.6 9 10 -3 during transmission events (Nardon and Grenier 1988;Mira and Moran 2002;Hosokawa et al 2007). To our knowledge, only symbiotic Spiroplasma spp.…”

Section: Discussionmentioning

confidence: 97%

“…Theoretical considerations as well as empirical evidence suggest that narrow bottlenecks in combination with the effective lack of recombination in strictly vertically transmitted symbionts lead to increased genetic drift, an accumulation of mildly deleterious mutations, faster sequence evolution, and a shift in base composition due to mutational bias in symbiont lineages (Lynch and Gabriel 1990;Moran 1996;Rispe and Moran 2000;Degnan et al 2004;Gil et al 2004). Earlier studies revealed substantial differences in the severity of bottlenecks experienced by symbiont populations, with factors of the reduction in cell numbers ranging from 0.3 to about 5 9 10 -5 (Nardon and Grenier 1988;Mira and Moran 2002;Anbutsu and Fukatsu 2003;Hosokawa et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission

et al. 2009

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Insects engage in mutualistic relationships with a wide variety of microorganisms that are usually transmitted vertically to the next generation. During transmission, the symbiont populations often suffer significant bottlenecks that may entail major genetic and genomic consequences. Here we investigated the life-cycle and the severity of transmission bottlenecks in a symbiotic system with an unusual way of post-hatch vertical transmission by using quantitative PCRs and morphological 3D-reconstructions. European beewolves (Philanthus triangulum, Hymenoptera: Crabronidae) harbor symbiotic bacteria ('Candidatus Streptomyces philanthi') in specialized antennal gland reservoirs and secrete them into their subterranean brood cells. The symbionts are later taken up by the beewolf larva and incorporated into the cocoon material to provide protection against pathogenic microorganisms. Even after months of hibernation, the symbiont population on the cocoon is estimated to encompass around 1.4 9 10 5 cells. However, our results indicate that only few of these bacterial cells (about 9.7 9 10 2 ) are taken up from the cocoon by the emerging female. The symbiont population subsequently undergoes logistic growth within the antennal gland reservoirs and reaches a maximum of about 1.5 9 10 7 cells 3-4 days after emergence. The maximum specific growth rate is estimated to be 0.084-0.105 h -1 . With a total reduction in cell numbers of about 6.7 9 10 -5 during vertical transmission, the symbiont population experiences one of the most severe bottlenecks known for any symbiotic system to date. This extreme bottleneck may have significantly affected the evolution of the beewolf-Streptomyces symbiosis by increased genetic drift, an accumulation of mildly deleterious mutations and genome erosion.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission

et al. 2009

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“…However, one important prerequisite for this transition was the possession of endosymbiotic bacteria, socalled SOPE (Sitophilus oryzae primary endosymbionts), which were first characterised for S. oryzae, later for S. granarius and S. zeamais, and more recently also for S. rugicollis (Mansour, 1930;Nardon, 1971;Nardon & Grenier, 1988;Heddi et al, 2001;Nardon et al, 2002). These gram-negative bacteria of the gamma 3-proteobacteria group exist freely in the cytoplasms of adult beetles, are passed onto future generations via the oocyte by a complex transmission during oogenesis (Nardon, 2006), and are found in the larva in the bacteriomes (mycetomes) at the junction between the stomodeum and the midgut.…”

Section: Predisposition For Utilising Stored Grainsmentioning

confidence: 99%

An attempt to reconstruct the natural and cultural history of the granary weevil, Sitophilus granarius (Coleoptera: Curculionidae)

Plarre¹

2010

Eur. J. Entomol.

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Abstract. It is generally accepted that stored grain insects are food opportunists and, when originally made the transition to manmade storage facilities, came from natural reservoirs like bird or rodent nests. This may not be true for Sitophilus granarius. Among all stored-product insects, the granary weevil S. granarius is the only species never recorded outside of storage facilities. Anatomical, physiological, and behavioural aspects of recent and hypothetical ancestral species in the genus Sitophilus are presented and discussed in terms of adaptation to the anthropogenic storage of grain. Full development inside the host kernel, endosymbioses with bacteria, and the reduction in flight activity to prevent water loss in a dry environment can be regarded as pre-adaptations for the evolution of a full synanthropic grain pest of cosmopolitan distribution. Faunistic, archaeological, and historical evidences of the pest's origin and spread in conjunction with early agriculture are reviewed to support a hypothesis of a co-evolutionary event with the dawn of Neolithic agriculture.

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“…Bacteriocytes themselves form the bacteriome tissue and do not differentiate in the absence of the bacteria in the nonsymbiotic strains (Nardon and Grenier 1988). The bacteria have been morphologically described as rodshaped microorganisms 5 to 30 m long (Mansour 1930;Nardon and Wicker 1981).…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, they are permanent in the female germ cell line and are transmitted to the offspring by maternal inheritance (Nardon 1971). The integration process involves the establishment of genetic interactions between the host and the bacteria (Nardon and Grenier 1988) and, probably, DNA rearrangement of the bacterial genome (Charles et al 1997).…”

Section: Introductionmentioning

confidence: 99%

Molecular Characterization of the Principal Symbiotic Bacteria of the Weevil Sitophilus oryzae: A Peculiar G + C Content of an Endocytobiotic DNA

et al. 1998

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The principal intracellular symbiotic bacteria of the cereal weevil Sitophilus oryzae were characterized using the sequence of the 16S rDNA gene (rrs gene) and G + C content analysis. Polymerase chain reaction amplification with universal eubacterial primers of the rrs gene showed a single expected sequence of 1,501 bp. Comparison of this sequence with the available database sequences placed the intracellular bacteria of S. oryzae as members of the Enterobacteriaceae family, closely related to the free-living bacteria, Erwinia herbicola and Escherichia coli, and the endocytobiotic bacteria of the tsetse fly and aphids. Moreover, by high-performance liquid chromatography, we measured the genomic G + C content of the S. oryzae principal endocytobiotes (SOPE) as 54%, while the known genomic G + C content of most intracellular bacteria is about 39.5%. Furthermore, based on the third codon position G + C content and the rrs gene G + C content, we demonstrated that most intracellular bacteria except SOPE are A + T biased irrespective of their phylogenetic position. Finally, using the hsp60 gene sequence, the codon usage of SOPE was compared with that of two phylogenetically closely related bacteria: E. coli, a free-living bacterium, and Buchnera aphidicola, the intracellular symbiotic bacteria of aphids. Taken together, these results show a peculiar and distinctly different DNA composition of SOPE with respect to the other obligate intracellular bacteria, and, combined with biological and biochemical data, they elucidate the evolution of symbiosis in S. oryzae.

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Genetical and Biochemical Interactions between the Host and Its Endocytobiotes in the Weevils Sitophilus (Coleoptere, Curculionidae) and Other Related Species

Cited by 30 publications

References 28 publications

Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission

Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission

An attempt to reconstruct the natural and cultural history of the granary weevil, Sitophilus granarius (Coleoptera: Curculionidae)

Molecular Characterization of the Principal Symbiotic Bacteria of the Weevil Sitophilus oryzae: A Peculiar G + C Content of an Endocytobiotic DNA

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