Temperature influences outcomes of an environmentally acquired symbiosis

Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24-40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia's in vitro thermal optima did not predict in vivo outcomes. Regardless, strain- and temperature- dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.

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Publication Details

Journal
The ISME Journal
Published
2025-01-01
DOI
https://doi.org/10.1093/ismejo/wraf056
Citations
5
Primary Topic
Insect symbiosis and bacterial influences
Type
article
Field-Weighted Citation Impact
8.36
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article

Temperature influences outcomes of an environmentally acquired symbiosis

Johnathan Adamson, A. A. Fadaei Tehrani, Alison Ravenscraft, Patrick T. Stillson et al.
5 citations
The ISME Journal
Insect symbiosis and bacterial influences
8.36
article

Temperature influences outcomes of an environmentally acquired symbiosis

Johnathan Adamson, A. A. Fadaei Tehrani, Alison Ravenscraft, Patrick T. Stillson, Katherine M. Martinez
article en
5 citations

Abstract

Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24-40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia's in vitro thermal optima did not predict in vivo outcomes. Regardless, strain- and temperature- dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.

The ISME JournalVol. 19(1)
Emory University (US), The University of Texas at Dallas (US), The University of Texas at Arlington (US)
Life in Land
Openalex Percentile: Top 3%
Insect symbiosis and bacterial influences
8.36
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