Shifting focus from resistance to disease tolerance: A review on hybrid house mice

Balard, Alice; Heitlinger, Emanuel

doi:10.1002/ece3.8889

Cited by 9 publications

(10 citation statements)

References 116 publications

(182 reference statements)

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“…For physiological resistance, investment in resistance rather than tolerance could indicate altruism by infected hosts. Resistance that controls the number of parasites on an infected host reduces transmission to conspecifics [64] but may trade off with tolerance of those parasites [14][15][16][17]. Resistance may improve infection outcomes by decreasing parasite burdens or worsen infection outcomes if the sacrifice in tolerance matters more than the reduction in parasite burden.…”

Section: Discussionmentioning

confidence: 99%

Associating with kin selects against disease tolerance

Walsman,

Lambe,

Stephenson

2023

Preprint

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Behavioural and physiological immunity are key to slowing epidemic spread. Here, we explore the evolutionary and epidemic consequences of their different costs for the evolution of tolerance vs. resistance: behavioural resistance affects social cohesion, with associated group-level costs, while physiological resistance costs should accrue to the individual. Further, the transmission-reduction benefits of resistance accrue differently to susceptible hosts and those already infected; infected hosts only benefit indirectly, by reducing transmission to kin. We therefore model the coevolution of transmission-reducing defences expressed in susceptible hosts with those expressed in infected hosts, as a function of kin association, and analyse the effect on population-level outcomes. Using parameter values for guppies,Poecilia reticulata, and their gyrodactylid parasites, we find that: 1) either susceptible or infected hosts should invest heavily in preventing infection, but not both; 2) kin association drives investment in physiological resistance more strongly than in behavioural resistance; 3) even weak levels of kin association can favour altruistic infected hosts that invest heavily in resistance (vs. selfish tolerance), eliminating the disease. Overall, our finding that weak kin association affects the coevolution of infected and susceptible investment in both behavioural and physiological immunity suggests that kin selection may affect disease dynamics across systems.

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Section: Discussionmentioning

confidence: 99%

Associating with kin selects against disease tolerance

Walsman,

Lambe,

Stephenson

2023

Preprint

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“…In particular, there is an interaction between inflammation, immune gene expression and the gut microbiome that appears to cause hybrid mice to exhibit defects in immunoregulation. This may be one reason why hybrid individuals are restricted to a narrow tension zone where the two parent subspecies co‐occur (Balard & Heitlinger, 2022; Barton & Hewitt, 1985). A range of additional studies, including hybridization of sika deer ( Cervus nippon ) and elk ( Cervus elaphus ) (Li et al., 2016), lake whitefish lineages ( Coregonus clupeaformis ) (Sevellec et al., 2019), blunt snout bream ( Megalobrama amblycephala ) and topmouth culter ( Culter alburnus ) (Li et al., 2018) and desert ( Neotoma lepida ) and Bryant's ( Neotoma bryanti ) woodrats (Nielsen et al., 2023) have reiterated the finding that hybrid animals often exhibit altered microbiomes relative to their progenitors (i.e.…”

Section: Introductionmentioning

confidence: 99%

A conceptual framework for host‐associated microbiomes of hybrid organisms

Camper,

Laughlin,

Malagon

et al. 2024

Methods Ecol Evol

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Hybridization between organisms from evolutionarily distinct lineages can have profound consequences on organismal ecology, with cascading effects on fitness and evolution. Most studies of hybrid organisms have focused on organismal traits, for example, various aspects of morphology and physiology. However, with the recent emergence of holobiont theory, there has been growing interest in understanding how hybridization impacts and is impacted by host‐associated microbiomes. Better understanding of the interplay between host hybridization and host‐associated microbiomes has the potential to provide insight into both the roles of host‐associated microbiomes as dictators of host performance as well as the fundamental rules governing host‐associated microbiome assembly. Unfortunately, there is a current lack of frameworks for understanding the structure of host‐associated microbiomes of hybrid organisms. In this paper, we develop four conceptual models describing possible relationships between the host‐associated microbiomes of hybrids and their progenitor or ‘parent’ taxa. We then integrate these models into a quantitative ‘4H index’ and present a new R package for calculation, visualization and analysis of this index. We demonstrate how the 4H index can be used to compare hybrid microbiomes across disparate plant and animal systems. Our analyses of these data sets show variation in the 4H index across systems based on host taxonomy, host site and microbial taxonomic group. Our four conceptual models, paired with our 4H index and associated visualization tools, facilitate comparison across hybrid systems. This, in turn, allows for systematic exploration of how different aspects of host hybridization impact the host‐associated microbiomes of hybrid organisms.

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“…Microbiome composition could be such a transgressive trait, and an aberrant microbiome in house mice might indicate dysbiosis, which could have a fitness effect [19]. In the HMHZ, a transgressive abundance of parasites (increased host resistance) has been detected [24, 25], but even for pathogens the effects on fitness are not clear [26, 27]. As fitness effects of microbiomes and the concept of dysbiosis are even more disputed [28], we here abstain from concluding effects on host health, fitness or even species barriers.…”

Section: Introductionmentioning

confidence: 99%

“…Addressing the effects of hybridisation on species composition within a cohesive analysis is not trivial. In multigeneration admixed hybrids, admixture effects should be analysed as a gradient [24, 27]. Additionally, species composition as a response is a complex multivariate measure [30].…”

Section: Introductionmentioning

confidence: 99%

Subspecies divergence, hybridisation and the spatial environment shape phylosymbiosis in the microbiome of house mice

Ferreira,

Jarquín-Díaz,

Planillo

et al. 2023

Preprint

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Closely related host species share similar symbionts, yet how host genetics and the environment affect symbiont communities at different stages of host genetic divergence remains largely unknown. Similarly, it is unclear whether host-symbiont associations result from or contribute to host divergence.We examined the intestinal community of 619 wild-caught mice from Germany’s European house mouse hybrid zone. Here, hybridisation upon secondary contact reflects divergence and could be traced gradually.Temporal and spatial factors were strong predictors of microbiome composition. Subspecies divergence predicted the composition similarity of the overall microbiome, specifically in the bacteria, parasite and fungal components. The effect of hybridisation was generally weak but significant for the fungal component. We confirmed our results in experiments with wild-derived inbred mice: subspecies’ genetic distances and hybridisation predicted the overall microbiome composition, and hybridisation further predicted fungal similarities among individuals. Fungi seemed more stable to the community perturbation of infection than other components of the microbiome.Differences between subspecies were more substantial across different microbiome components than those associated with hybridisation. Diverged microbiomes are a product of host divergence and are maintained by host genetics upon large environmental effects. These results provide a unique perspective into the ecoevolutionary processes shaping phylosymbiosis.

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Shifting focus from resistance to disease tolerance: A review on hybrid house mice

Cited by 9 publications

References 116 publications

Associating with kin selects against disease tolerance

Associating with kin selects against disease tolerance

A conceptual framework for host‐associated microbiomes of hybrid organisms

Subspecies divergence, hybridisation and the spatial environment shape phylosymbiosis in the microbiome of house mice

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