Dataset Information

Fitness costs of symbiont switching using entomopathogenic nematodes as a model.

ABSTRACT: Steinernematid nematodes form obligate symbioses with bacteria from the genus Xenorhabdus. Together Steinernema nematodes and their bacterial symbionts successfully infect, kill, utilize, and exit their insect hosts. During this process the nematodes and bacteria disassociate requiring them to re-associate before emerging from the host. This interaction can be complicated when two different nematodes co-infect an insect host.Non-cognate nematode-bacteria pairings result in reductions for multiple measures of success, including total progeny production and virulence. Additionally, nematode infective juveniles carry fewer bacterial cells when colonized by a non-cognate symbiont. Finally, we show that Steinernema nematodes can distinguish heterospecific and some conspecific non-cognate symbionts in behavioral choice assays.Steinernema-Xenorhabdus symbioses are tightly governed by partner recognition and fidelity. Association with non-cognates resulted in decreased fitness, virulence, and bacterial carriage of the nematode-bacterial pairings. Entomopathogenic nematodes and their bacterial symbionts are a useful, tractable, and reliable model for testing hypotheses regarding the evolution, maintenance, persistence, and fate of mutualisms.

SUBMITTER: McMullen JG

PROVIDER: S-EPMC5392933 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Fitness costs of symbiont switching using entomopathogenic nematodes as a model.

McMullen John G JG Peterson Brittany F BF Forst Steven S Blair Heidi Goodrich HG Stock S Patricia SP

BMC evolutionary biology 20170417 1

<h4>Background</h4>Steinernematid nematodes form obligate symbioses with bacteria from the genus Xenorhabdus. Together Steinernema nematodes and their bacterial symbionts successfully infect, kill, utilize, and exit their insect hosts. During this process the nematodes and bacteria disassociate requiring them to re-associate before emerging from the host. This interaction can be complicated when two different nematodes co-infect an insect host.<h4>Results</h4>Non-cognate nematode-bacteria pairin ...[more]

PMID: 28412935

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Project description:Nicrophorus vespilloides is a social beetle that rears its offspring on decomposing carrion. Wild beetles are frequently associated with two types of macrobial symbionts, mites, and nematodes. Although these organisms are believed to be phoretic commensals that harmlessly use beetles as a means of transfer between carcasses, the role of these symbionts on N. vespilloides fitness is poorly understood. Here, we show that nematodes have significant negative effects on beetle fitness across a range of worm densities and also quantify the density-dependent transmission of worms between mating individuals and from parents to offspring. Using field-caught beetles, we provide the first report of a new nematode symbiont in N. vespilloides, most closely related to Rhabditoides regina, and show that worm densities are highly variable across individuals isolated from nature but do not differ between males and females. Next, by inoculating mating females with increasing densities of nematodes, we show that worm infections significantly reduce brood size, larval survival, and larval mass, and also eliminate the trade-off between brood size and larval mass. Finally, we show that nematodes are efficiently transmitted between mating individuals and from mothers to larvae, directly and indirectly via the carcass, and that worms persist through pupation. These results show that the phoretic nematode R. regina can be highly parasitic to burying beetles but can nevertheless persist because of efficient mechanisms of intersexual and intergenerational transmission. Phoretic species are exceptionally common and may cause significant harm to their hosts, even though they rely on these larger species for transmission to new resources. However, this harm may be inevitable and unavoidable if transmission of phoretic symbionts requires nematode proliferation. It will be important to determine the generality of our results for other phoretic associates of animals. It will equally be important to assess the fitness effects of phoretic species under changing resource conditions and in the field where diverse interspecific interactions may exacerbate or reduce the negative effects of phoresy.

Project description:A total of 30 different agricultural fields in the Golden Triangle Region of Montana, USA were surveyed, and 150 soil samples were evaluated for the presence of entomopathogenic nematodes (EPNs). The authors isolated EPNs from 10% of the collected samples. The recovered isolates were identified as Steinernema feltiae and Heterorhabditis bacteriophora by using morphological and molecular analysis. Steinernema feltiae was found from two fields, Kalispell (S. feltiae 1) and Choteau (S. feltiae 2). Steinernema feltiae (1 and 2) differed significantly from each other in terms of morphological characters for infective juveniles (distance from anterior end to excretory pore and nerve ring) and 1st generation males (body length, spicule length, gubernaculum length, oesophagus, tail, and anal body diameter). Steinernema feltiae 2 and H. bacteriophora were recovered from the same field in Choteau. All these species were recovered from wheat fields with sandy clay loam and loam soils with 3.3 to 3.4% organic matter content and pH 8.A total of 30 different agricultural fields in the Golden Triangle Region of Montana, USA were surveyed, and 150 soil samples were evaluated for the presence of entomopathogenic nematodes (EPNs). The authors isolated EPNs from 10% of the collected samples. The recovered isolates were identified as Steinernema feltiae and Heterorhabditis bacteriophora by using morphological and molecular analysis. Steinernema feltiae was found from two fields, Kalispell (S. feltiae 1) and Choteau (S. feltiae 2). Steinernema feltiae (1 and 2) differed significantly from each other in terms of morphological characters for infective juveniles (distance from anterior end to excretory pore and nerve ring) and 1st generation males (body length, spicule length, gubernaculum length, oesophagus, tail, and anal body diameter). Steinernema feltiae 2 and H. bacteriophora were recovered from the same field in Choteau. All these species were recovered from wheat fields with sandy clay loam and loam soils with 3.3 to 3.4% organic matter content and pH 8.

Dataset Information

Fitness costs of symbiont switching using entomopathogenic nematodes as a model.

Publications

Fitness costs of symbiont switching using entomopathogenic nematodes as a model.

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