A theoretical model for host-controlled regulation of symbiont density
There is growing empirical evidence that animal hosts actively control the density of their mutualistic symbionts according to their requirements. Such active regulation can be facilitated by compartmentalization of symbionts within host tissues, which confers a high degree of control of the symbiosis to the host. Here, we build a general theoretical framework to predict the underlying ecological drivers and evolutionary consequences of host-controlled endosymbiont density regulation for a mutually obligate association between a host and a compartmentalized, vertically transmitted symbiont. Building on the assumption that the costs and benefits of hosting a symbiont population increase with symbiont density, we use state-dependent dynamic programming to determine an optimal strategy for the host, i.e., that which maximizes host fitness, when regulating the density of symbionts. Simulations of active host-controlled regulation governed by the optimal strategy predict that the density of the symbiont should converge to a constant level during host development, and following perturbation. However, a similar trend also emerges from alternative strategies of symbiont regulation. The strategy which maximizes host fitness also promotes symbiont fitness compared to alternative strategies, suggesting that active host-controlled regulation of symbiont density could be adaptive for the symbiont as well as the host. Adaptation of the framework allowed the dynamics of symbiont density to be predicted for other host-symbiont ecologies, such as for non-essential symbionts, demonstrating the versatility of this modelling approach.
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Subjects: | L72 - Organismes nuisibles des animaux, U10 - Informatique, mathématiques et statistiques, modèle mathématique, symbiose, symbiote, dynamique des populations, hôte, http://aims.fao.org/aos/agrovoc/c_24199, http://aims.fao.org/aos/agrovoc/c_7563, http://aims.fao.org/aos/agrovoc/c_7562, http://aims.fao.org/aos/agrovoc/c_6111, http://aims.fao.org/aos/agrovoc/c_3673, |
Online Access: | http://agritrop.cirad.fr/607757/ http://agritrop.cirad.fr/607757/1/J%20of%20Evolutionary%20Biology%20-%202023%20-%20Whittle%20-%20A%20theoretical%20model%20for%20host%E2%80%90controlled%20regulation%20of%20symbiont%20density%20%281%29.pdf |
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dig-cirad-fr-6077572024-01-29T06:21:14Z http://agritrop.cirad.fr/607757/ http://agritrop.cirad.fr/607757/ A theoretical model for host-controlled regulation of symbiont density. Whittle Mathilda, Bonsall Michael B., Barreaux Antoine, Ponton Fleur, English Sinead. 2023. Journal of Evolutionary Biology, 36 (12), n.spéc. The Evolutionary Significance of Animal Microbiomes : 1731-1744.https://doi.org/10.1111/jeb.14246 <https://doi.org/10.1111/jeb.14246> A theoretical model for host-controlled regulation of symbiont density Whittle, Mathilda Bonsall, Michael B. Barreaux, Antoine Ponton, Fleur English, Sinead eng 2023 Journal of Evolutionary Biology L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 There is growing empirical evidence that animal hosts actively control the density of their mutualistic symbionts according to their requirements. Such active regulation can be facilitated by compartmentalization of symbionts within host tissues, which confers a high degree of control of the symbiosis to the host. Here, we build a general theoretical framework to predict the underlying ecological drivers and evolutionary consequences of host-controlled endosymbiont density regulation for a mutually obligate association between a host and a compartmentalized, vertically transmitted symbiont. Building on the assumption that the costs and benefits of hosting a symbiont population increase with symbiont density, we use state-dependent dynamic programming to determine an optimal strategy for the host, i.e., that which maximizes host fitness, when regulating the density of symbionts. Simulations of active host-controlled regulation governed by the optimal strategy predict that the density of the symbiont should converge to a constant level during host development, and following perturbation. However, a similar trend also emerges from alternative strategies of symbiont regulation. The strategy which maximizes host fitness also promotes symbiont fitness compared to alternative strategies, suggesting that active host-controlled regulation of symbiont density could be adaptive for the symbiont as well as the host. Adaptation of the framework allowed the dynamics of symbiont density to be predicted for other host-symbiont ecologies, such as for non-essential symbionts, demonstrating the versatility of this modelling approach. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/607757/1/J%20of%20Evolutionary%20Biology%20-%202023%20-%20Whittle%20-%20A%20theoretical%20model%20for%20host%E2%80%90controlled%20regulation%20of%20symbiont%20density%20%281%29.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1111/jeb.14246 10.1111/jeb.14246 info:eu-repo/semantics/altIdentifier/doi/10.1111/jeb.14246 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1111/jeb.14246 info:eu-repo/semantics/dataset/purl/https://doi.org/10.5061/dryad.xgxd254nh |
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L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 |
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L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 Whittle, Mathilda Bonsall, Michael B. Barreaux, Antoine Ponton, Fleur English, Sinead A theoretical model for host-controlled regulation of symbiont density |
description |
There is growing empirical evidence that animal hosts actively control the density of their mutualistic symbionts according to their requirements. Such active regulation can be facilitated by compartmentalization of symbionts within host tissues, which confers a high degree of control of the symbiosis to the host. Here, we build a general theoretical framework to predict the underlying ecological drivers and evolutionary consequences of host-controlled endosymbiont density regulation for a mutually obligate association between a host and a compartmentalized, vertically transmitted symbiont. Building on the assumption that the costs and benefits of hosting a symbiont population increase with symbiont density, we use state-dependent dynamic programming to determine an optimal strategy for the host, i.e., that which maximizes host fitness, when regulating the density of symbionts. Simulations of active host-controlled regulation governed by the optimal strategy predict that the density of the symbiont should converge to a constant level during host development, and following perturbation. However, a similar trend also emerges from alternative strategies of symbiont regulation. The strategy which maximizes host fitness also promotes symbiont fitness compared to alternative strategies, suggesting that active host-controlled regulation of symbiont density could be adaptive for the symbiont as well as the host. Adaptation of the framework allowed the dynamics of symbiont density to be predicted for other host-symbiont ecologies, such as for non-essential symbionts, demonstrating the versatility of this modelling approach. |
format |
article |
topic_facet |
L72 - Organismes nuisibles des animaux U10 - Informatique, mathématiques et statistiques modèle mathématique symbiose symbiote dynamique des populations hôte http://aims.fao.org/aos/agrovoc/c_24199 http://aims.fao.org/aos/agrovoc/c_7563 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_6111 http://aims.fao.org/aos/agrovoc/c_3673 |
author |
Whittle, Mathilda Bonsall, Michael B. Barreaux, Antoine Ponton, Fleur English, Sinead |
author_facet |
Whittle, Mathilda Bonsall, Michael B. Barreaux, Antoine Ponton, Fleur English, Sinead |
author_sort |
Whittle, Mathilda |
title |
A theoretical model for host-controlled regulation of symbiont density |
title_short |
A theoretical model for host-controlled regulation of symbiont density |
title_full |
A theoretical model for host-controlled regulation of symbiont density |
title_fullStr |
A theoretical model for host-controlled regulation of symbiont density |
title_full_unstemmed |
A theoretical model for host-controlled regulation of symbiont density |
title_sort |
theoretical model for host-controlled regulation of symbiont density |
url |
http://agritrop.cirad.fr/607757/ http://agritrop.cirad.fr/607757/1/J%20of%20Evolutionary%20Biology%20-%202023%20-%20Whittle%20-%20A%20theoretical%20model%20for%20host%E2%80%90controlled%20regulation%20of%20symbiont%20density%20%281%29.pdf |
work_keys_str_mv |
AT whittlemathilda atheoreticalmodelforhostcontrolledregulationofsymbiontdensity AT bonsallmichaelb atheoreticalmodelforhostcontrolledregulationofsymbiontdensity AT barreauxantoine atheoreticalmodelforhostcontrolledregulationofsymbiontdensity AT pontonfleur atheoreticalmodelforhostcontrolledregulationofsymbiontdensity AT englishsinead atheoreticalmodelforhostcontrolledregulationofsymbiontdensity AT whittlemathilda theoreticalmodelforhostcontrolledregulationofsymbiontdensity AT bonsallmichaelb theoreticalmodelforhostcontrolledregulationofsymbiontdensity AT barreauxantoine theoreticalmodelforhostcontrolledregulationofsymbiontdensity AT pontonfleur theoreticalmodelforhostcontrolledregulationofsymbiontdensity AT englishsinead theoreticalmodelforhostcontrolledregulationofsymbiontdensity |
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1792500704395395072 |