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Journal ArticleDOI

Facultative Symbionts in Aphids and the Horizontal Transfer of Ecologically Important Traits

01 Jan 2010-Annual Review of Entomology (Annual Reviews)-Vol. 55, Iss: 1, pp 247-266
TL;DR: Experiments on pea aphids have demonstrated that facultative symbionts protect against entomopathogenic fungi and parasitoid wasps, ameliorate the detrimental effects of heat, and influence host plant suitability.
Abstract: Aphids engage in symbiotic associations with a diverse assemblage of heritable bacteria. In addition to their obligate nutrient-provisioning symbiont, Buchnera aphidicola, aphids may also carry one or more facultative symbionts. Unlike obligate symbionts, facultative symbionts are not generally required for survival or reproduction and can invade novel hosts, based on both phylogenetic analyses and transfection experiments. Facultative symbionts are mutualistic in the context of various ecological interactions. Experiments on pea aphids (Acyrthosiphon pisum) have demonstrated that facultative symbionts protect against entomopathogenic fungi and parasitoid wasps, ameliorate the detrimental effects of heat, and influence host plant suitability. The protective symbiont, Hamiltonella defensa, has a dynamic genome, exhibiting evidence of recombination, phage-mediated gene uptake, and horizontal gene transfer and containing virulence and toxin-encoding genes. Although transmitted maternally with high fidelity, facultative symbionts occasionally move horizontally within and between species, resulting in the instantaneous acquisition of ecologically important traits, such as parasitoid defense.
Citations
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Journal ArticleDOI
TL;DR: Gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication, and the extent of these roles is still unclear and awaits further studies.
Abstract: Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.

1,633 citations


Cites background from "Facultative Symbionts in Aphids and..."

  • ...These effects are commonly beneficial to the host, as in the case of H. defensa, which uses a bacteriophage-encoded mechanism to protect its host against parasitoid wasp larvae, thereby enabling its own survival and transmission (Oliver et al., 2010)....

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  • ..., 2009) and possess mechanisms for actively invading host tissues and for affecting host biology in a way that promotes the increased frequency of infected hosts in the host population (Werren et al., 2008; Oliver et al., 2010)....

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  • ...defensa, which uses a bacteriophage-encoded mechanism to protect its host against parasitoid wasp larvae, thereby enabling its own survival and transmission (Oliver et al., 2010)....

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  • ...…larger and more dynamic genomes (Werren et al., 2008; Degnan et al., 2009) and possess mechanisms for actively invading host tissues and for affecting host biology in a way that promotes the increased frequency of infected hosts in the host population (Werren et al., 2008; Oliver et al., 2010)....

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Journal ArticleDOI
Stephen Richards1, Richard A. Gibbs1, Nicole M. Gerardo2, Nancy A. Moran3  +220 moreInstitutions (58)
TL;DR: The genome of the pea aphid shows remarkable levels of gene duplication and equally remarkable gene absences that shed light on aspects of aphid biology, most especially its symbiosis with Buchnera.
Abstract: Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.

1,271 citations

Journal ArticleDOI
TL;DR: An evolutionary perspective on mutualism breakdown is developed to complement the ecological perspective, by focusing on three processes: shifts from mutualism to antagonism, switches to novel partners and mutualism abandonment.
Abstract: Ecology Letters (2010) 13: 1459–1474 Abstract There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.

461 citations

Journal ArticleDOI
TL;DR: Bacterial symbionts play a prominent role in insect nutritional ecology by aiding in digestion of food or providing nutrients that are limited or lacking in the diet.
Abstract: 1. Bacterial symbionts play a prominent role in insect nutritional ecology by aiding in digestion of food or providing nutrients that are limited or lacking in the diet. Thereby, endosymbionts open niches to their insect host that would otherwise be unavailable. 2. Currently, several other ecologically relevant traits mediated by endosymbionts are being investigated, including enhanced parasite resistance, enhanced heat tolerance, and influences on insect–plant interactions such as manipulation of plant physiology to the benefit of the insect. 3. Traits mediated by endosymbionts are often identified by correlative studies where traits are found to be altered in the presence of a particular symbiont. Recent developments in genomic tools offer the opportunity for studying the impact of bacteria–insect symbioses under natural conditions in a population and community ecology context. In vivo experiments specifically testing putative functions of endosymbionts in parallel to population-level studies on the prevalence of endosymbionts allow disentangling host versus symbiont contribution to phenotypic variability observed in individuals. Effects of symbionts on host phenotype are often large and relevant to host fitness, e.g. by significantly enhancing survival or fecundity in a context-dependent manner. 4. Predominantly vertically transmitted endosymbionts contribute to the heritable genetic variation present in a host species. Phenotypic variation on which selection can act may be due to differences either among host genomes, symbiont genomes, or genotype × genotype interactions. Therefore the holobiont, i.e. the host including all symbionts, should be regarded as the unit of selection as the association between host and symbionts may affect the fitness of the holobiont depending on the environment.

459 citations


Cites background from "Facultative Symbionts in Aphids and..."

  • ...Interestingly, Rickettsiella is often found in concert with Hamiltonella or Serratia, those aphids that confer protection against parasitoid wasps (Oliver et al., 2010; Tsuchida et al., 2010)....

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  • ...…have been shown to be major players in defence of the insects themselves by enhancing pathogen and parasitoid resistance (Currie et al., 2003a,b; Oliver et al., 2003, 2009, 2010; Kaltenpoth et al., 2005; Hedges et al., 2008; Teixeira et al., 2008; Brownlie & Johnson, 2009; Kaltenpoth, 2009) or…...

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  • ...More and more traits can now be correlated with the presence of the often less well characterised secondary symbionts (Teixeira et al., 2008; Brownlie & Johnson, 2009; Oliver et al., 2010)....

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  • ...The endosymbiont community was largely transmitted maternally as expected, however, hybrids carrying Arsenophonus were found significantly less often than expected, pointing either towards loss of this endosymbiont in viable hybrids or lower viability of hybrids carrying it....

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  • ...Likewise, aphids cannot tolerate high temperatures well (Dean, 1974; Oliver et al., 2010)....

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Journal ArticleDOI
19 Nov 2010-Science
TL;DR: It is discovered that infection with a facultative endosymbiont of the genus Rickettsiella changes the insects’ body color from red to green in natural populations of the pea aphid.
Abstract: Color variation within populations of the pea aphid influences relative susceptibility to predators and parasites. We have discovered that infection with a facultative endosymbiont of the genus Rickettsiella changes the insects' body color from red to green in natural populations. Approximately 8% of pea aphids collected in Western Europe carried the Rickettsiella infection. The infection increased amounts of blue-green polycyclic quinones, whereas it had less of an effect on yellow-red carotenoid pigments. The effect of the endosymbiont on body color is expected to influence prey-predator interactions, as well as interactions with other endosymbionts.

364 citations

References
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Book
01 Jan 1993
TL;DR: This book synthesizes the work of both schools of parasitoid biology and asks how a consideration of evolutionary biology can help to understand the behavior, ecology, and diversity of the approximately one to two million species of Parasitoids found on earth.
Abstract: Parasitoids lay their eggs on or in the bodies of other species of insects, and the parasitoid larvae develop by feeding on the host, causing its eventual death. Known for a long time to applied biologists for their importance in regulating the population densities of economic pests, parasitoids have recently proven to be valuable tools in testing many aspects of evolutionary theory. This book synthesizes the work of both schools of parasitoid biology and asks how a consideration of evolutionary biology can help us understand the behavior, ecology, and diversity of the approximately one to two million species of parasitoids found on earth. After a general introduction to parasitoid natural history and taxonomy, the first part of the book treats the different components of the reproductive strategy of parasitoids: searching for a host, host selection, clutch size, and the sex ratio. Subsequent chapters discuss pathogens and non-Mendelian genetic elements that affect sexual reproduction; evolutionary aspects of the physiological interactions between parasitoid and host; mating strategies; and life history theory and community ecology. A special effort is made to discuss the theoretical background to the subject, but without the use of mathematics.

2,875 citations


"Facultative Symbionts in Aphids and..." refers background in this paper

  • ...After locating an aphid nymph, a female wasp deposits an egg into the aphid hemocoel, which subsequently develops within a living aphid before pupating and eventually killing the host (39)....

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Journal ArticleDOI
TL;DR: Insect heritable symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
Abstract: Insect heritable symbionts have proven to be ubiquitous, based on molecular screening of various insect lineages. Recently, molecular and experimental approaches have yielded an immensely richer understanding of their diverse biological roles, resulting in a burgeoning research literature. Increasingly, commonalities and intermediates are being discovered between categories of symbionts once considered distinct: obligate mutualists that provision nutrients, facultative mutualists that provide protection against enemies or stress, and symbionts such as Wolbachia that manipulate reproductive systems. Among the most farreaching impacts of widespread heritable symbiosis is that it may promote speciation by increasing reproductive and ecological isolation of host populations, and it effectively provides a means for transfer of genetic information among host lineages. In addition, insect symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.

1,438 citations


"Facultative Symbionts in Aphids and..." refers background in this paper

  • ...The genomes of examined primary symbionts are extremely reduced and evolutionarily static, exhibiting little evidence of foreign gene uptake via mobile genetic elements as is typical of their free-living and pathogenic relatives (69)....

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Book
01 Jan 1983
TL;DR: Books, as a source that may involve the facts, opinion, literature, religion, and many others are the great friends to join with.
Abstract: New updated! The latest book from a very famous author finally comes out. Book of evolution of sex determining mechanisms, as an amazing reference becomes what you need to get. What's for is this book? Are you still thinking for what the book is? Well, this is what you probably will get. You should have made proper choices for your better life. Book, as a source that may involve the facts, opinion, literature, religion, and many others are the great friends to join with.

1,421 citations

Journal ArticleDOI
21 May 1999-Science
TL;DR: Several Gram-negative pathogenic bacteria have evolved a complex protein secretion system termed type III to deliver bacterial effector proteins into host cells that then modulate host cellular functions.
Abstract: Several Gram-negative pathogenic bacteria have evolved a complex protein secretion system termed type III to deliver bacterial effector proteins into host cells that then modulate host cellular functions. These bacterial devices are present in both plant and animal pathogenic bacteria and are evolutionarily related to the flagellar apparatus. Although type III secretion systems are substantially conserved, the effector molecules they deliver are unique for each bacterial species. Understanding the biology of these devices may allow the development of novel prevention and therapeutic approaches for several infectious diseases.

1,295 citations


"Facultative Symbionts in Aphids and..." refers background in this paper

  • ...In pathogenic Enterobacteriaceae, including Salmonella and Yersinia species, type III secretion systems function in the invasion of eukaryotic cells (37), and the presence of these genes is evidence of invasive potential of H....

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Book
15 Jan 1965

1,255 citations