Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid,<i>Acyrthosiphon pisum</i>

Tsuchida, Tsutomu; Koga, Ryuichi; Shibao, Harunobu; Matsumoto, Tadao; Fukatsu, Takema

doi:10.1046/j.1365-294x.2002.01606.x

Cited by 284 publications

(316 citation statements)

References 32 publications

(74 reference statements)

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“…In Japan, pea aphids Acyrthosiphon pisum mainly feed on vetch and clover, and many aphid clones produce more progeny on vetch than on clover. Notably, Regiella infection was detected from aphids on clover at significantly higher frequencies than on vetch [6]. Similar associations between Regiella infection and clover infestation have been identified in pea aphid populations worldwide [7 -9].…”

Section: Introductionsupporting

confidence: 64%

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

et al. 2010

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In Japan, pea aphids Acyrthosiphon pisum mainly feed on vetch and clover, and many aphid clones produce more progeny on vetch than on clover. In this context, particular genotypes of the facultative symbiont Regiella insecticola enhance reproduction of infected pea aphids specifically on clover, thereby broadening the suitable food plant range of the insect. A species that is sympatric to A. pisum, vetch aphids Megoura crassicauda, are commonly found on vetch but not on clover. Laboratory rearing of M. crassicauda strains revealed active reproduction on vetch but substantially no reproduction on clover. Experimental transfection of Regiella from A. pisum to M. crassicauda by haemolymph injection established stable and heritable infection in the recipients, although no Regiella infection has been detected in natural populations of M. crassicauda. Different strains of Regiellatransfected M. crassicauda grew and reproduced on vetch, but exhibited lower fitness in comparison with corresponding uninfected aphid strains. Strikingly, the Regiella-transfected M. crassicauda exhibited improved survival and some reproduction on clover. These results suggest that Regiella has the potential to confer an ecological trait, adaptation to clover, on novel insect hosts, and also account for why Regiella is able to infect M. crassicauda but is scarcely found in these aphid populations.

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Section: Introductionsupporting

confidence: 64%

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

et al. 2010

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“…Our results are the first to suggest probable fitness costs of SS infection of aphids in the absence of parasitism, providing insight into the unanswered question of why uninfected lineages occur at high frequencies in field populations worldwide (Sandström et al 2001;Tsuchida et al 2002;Simon et al 2003;Oliver et al 2006). Given the evidence presented here that Hamiltonella-infected aphids increase rapidly in frequency in the presence of parasitism, one would predict that Hamiltonella would be fixed or much more prevalent in natural populations where A. ervi is a common and important natural enemy (Angalet & Fuester 1977).…”

Section: Discussionmentioning

confidence: 72%

“…Serratia symbiotica was previously called PASS or R-type, H. defensa was called PABS or T-type and Regiella insecticola was called PAUS or U-type (Chen & Purcell 1997;Darby et al 2001;Sandström et al 2001;Tsuchida et al 2002).…”

Section: Methodsmentioning

confidence: 99%

“…Thus, we might predict that, given the documented high fidelity of vertical transmission of SS to progeny, SS, and Hamiltonella in particular, would maintain high frequencies or become fixed in natural populations. However, worldwide, surveys indicate that A. pisum SS are found at intermediate frequencies in nature (Sandström et al 2001;Tsuchida et al 2002;Simon et al 2003;Oliver et al 2006). Here, we examined the fitness costs and benefits to SS infection in two types of experiments.…”

Section: Introductionmentioning

confidence: 99%

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Population dynamics of defensive symbionts in aphids

et al. 2007

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Vertically transmitted micro-organisms can increase in frequency in host populations by providing net benefits to hosts. While laboratory studies have identified diverse beneficial effects conferred by inherited symbionts of insects, they have not explicitly examined the population dynamics of mutualist symbiont infection within populations. In the pea aphid, Acyrthosiphon pisum, the inherited facultative symbiont, Hamiltonella defensa, provides protection against parasitism by the wasp, Aphidius ervi. Despite a high fidelity of vertical transmission and direct benefits of infection accruing to parasitized aphids, Hamiltonella remains only at intermediate frequencies in natural populations. Here, we conducted population cage experiments to monitor the dynamics of Hamiltonella and of another common A. pisum symbiont, Serratia symbiotica, in the presence and absence of parasitism. We also conducted fitness assays of Hamiltonellainfected aphids to search for costs to infection in the absence of parasitism. In the population cages, we found that the frequency of A. pisum infected with Hamiltonella increased dramatically after repeated exposure to parasitism by A. ervi, indicating that selection pressures from natural enemies can lead to the increase of particular inherited symbionts in insect populations. In our laboratory fitness assays, we did not detect a cost to infection with Hamiltonella, but in the population cages not exposed to parasitism, we found a significant decline in the frequency of both Hamiltonella and Serratia. The declining frequencies of Hamiltonella-infected aphids in population cages in the absence of parasitism indicate a probable cost to infection and may explain why Hamiltonella remains at intermediate frequencies in natural populations.

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“…The pea aphid, A. pisum, consists of a series of host-adapted populations that are specialized on different host plant species or genera [47][48][49]. These host-adapted populations tend to carry different species of secondary symbionts, suggesting that the symbionts might play an active role in host use and specialization on certain plant species, although these differences are not fixed between populations [32,[50][51][52][53]. Manipulation experiments have shown that the effects of the secondary symbionts on host use are complex and vary with aphid and/or symbiont genotype [54 -56].…”

Section: Are Heritable Endosymbionts Affecting Important Ecological Tmentioning

confidence: 99%

Bacterial symbionts in insects or the story of communities affecting communities

Ferrari

Vavre

2011

Phil. Trans. R. Soc. B

293

270

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Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.

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Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid,Acyrthosiphon pisum

Cited by 284 publications

References 32 publications

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

Population dynamics of defensive symbionts in aphids

Bacterial symbionts in insects or the story of communities affecting communities

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