Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size

ABSTRACT Many insects and other animals host heritable endosymbionts that alter host fitness and reproduction. The prevalence of facultative endosymbionts can fluctuate in host populations across time and geography for reasons that are poorly understood. This is particularly true for maternally tran...

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Main Authors: Jason M. Graham, Joseph Klobusicky, Michael T. J. Hague
Format: Article
Language:English
Published: Wiley 2025-08-01
Series:Ecology and Evolution
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Online Access:https://doi.org/10.1002/ece3.71989
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author Jason M. Graham
Joseph Klobusicky
Michael T. J. Hague
author_facet Jason M. Graham
Joseph Klobusicky
Michael T. J. Hague
author_sort Jason M. Graham
collection DOAJ
description ABSTRACT Many insects and other animals host heritable endosymbionts that alter host fitness and reproduction. The prevalence of facultative endosymbionts can fluctuate in host populations across time and geography for reasons that are poorly understood. This is particularly true for maternally transmitted Wolbachia bacteria, which infect roughly half of all insect species. For instance, the frequencies of several wMel‐like Wolbachia, including wMel in host Drosophila melanogaster, fluctuate over time in certain host populations, but the specific conditions that generate temporal variation in Wolbachia prevalence are unresolved. We implemented a discrete generation model in the new R package symbiontmodeler to evaluate how finite‐population stochasticity contributes to Wolbachia fluctuations over time in simulated host populations under a variety of conditions. Using empirical estimates from natural Wolbachia‐Drosophila systems, we explored how stochasticity is determined by a broad range of factors, including host population size, maternal transmission rates, and Wolbachia effects on host fitness (modeled as fecundity) and reproduction (cytoplasmic incompatibility; CI). While stochasticity generally increases when host fitness benefits and CI are relaxed, we found that a decline in the maternal transmission rate had the strongest relative impact on increasing the size of fluctuations. We infer that non‐ or weak‐CI‐causing strains like wMel, which often show evidence of imperfect maternal transmission, tend to generate larger stochastic fluctuations compared to strains that cause strong CI, like wRi in D. simulans. Additional factors, such as fluctuating host fitness effects, are required to explain the largest examples of temporal variation in Wolbachia. The conditions we simulate here using symbiontmodeler serve as a jumping‐off point for understanding drivers of temporal and spatial variation in the prevalence of Wolbachia, the most common endosymbionts found in nature.
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spelling doaj-art-5c5cfb09217d499a9b97babf65d1fefb2025-08-20T03:44:00ZengWileyEcology and Evolution2045-77582025-08-01158n/an/a10.1002/ece3.71989Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population SizeJason M. Graham0Joseph Klobusicky1Michael T. J. Hague2Mathematics Department University of Scranton Scranton Pennsylvania USAMathematics Department University of Scranton Scranton Pennsylvania USABiology Department University of Scranton Scranton Pennsylvania USAABSTRACT Many insects and other animals host heritable endosymbionts that alter host fitness and reproduction. The prevalence of facultative endosymbionts can fluctuate in host populations across time and geography for reasons that are poorly understood. This is particularly true for maternally transmitted Wolbachia bacteria, which infect roughly half of all insect species. For instance, the frequencies of several wMel‐like Wolbachia, including wMel in host Drosophila melanogaster, fluctuate over time in certain host populations, but the specific conditions that generate temporal variation in Wolbachia prevalence are unresolved. We implemented a discrete generation model in the new R package symbiontmodeler to evaluate how finite‐population stochasticity contributes to Wolbachia fluctuations over time in simulated host populations under a variety of conditions. Using empirical estimates from natural Wolbachia‐Drosophila systems, we explored how stochasticity is determined by a broad range of factors, including host population size, maternal transmission rates, and Wolbachia effects on host fitness (modeled as fecundity) and reproduction (cytoplasmic incompatibility; CI). While stochasticity generally increases when host fitness benefits and CI are relaxed, we found that a decline in the maternal transmission rate had the strongest relative impact on increasing the size of fluctuations. We infer that non‐ or weak‐CI‐causing strains like wMel, which often show evidence of imperfect maternal transmission, tend to generate larger stochastic fluctuations compared to strains that cause strong CI, like wRi in D. simulans. Additional factors, such as fluctuating host fitness effects, are required to explain the largest examples of temporal variation in Wolbachia. The conditions we simulate here using symbiontmodeler serve as a jumping‐off point for understanding drivers of temporal and spatial variation in the prevalence of Wolbachia, the most common endosymbionts found in nature.https://doi.org/10.1002/ece3.71989Drosophilaendosymbiosishost–microbe interactionmaternal transmissionwMelWolbachia
spellingShingle Jason M. Graham
Joseph Klobusicky
Michael T. J. Hague
Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
Ecology and Evolution
Drosophila
endosymbiosis
host–microbe interaction
maternal transmission
wMel
Wolbachia
title Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
title_full Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
title_fullStr Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
title_full_unstemmed Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
title_short Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population Size
title_sort stochastic fluctuations of the facultative endosymbiont wolbachia due to finite host population size
topic Drosophila
endosymbiosis
host–microbe interaction
maternal transmission
wMel
Wolbachia
url https://doi.org/10.1002/ece3.71989
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