Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation

Laine, Anna Liisa; Barrès, Benoît; Numminen, Elina; Sirén, Jukka

doi:10.7554/elife.47091

Cited by 13 publications

(15 citation statements)

References 50 publications

(77 reference statements)

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“…Dispersal of microbes is likely to be key in maintaining microbiome diversity and reducing variation in microbiome composition between individual hosts (Alberdi et al, 2016;Adair and Douglas, 2017;Macke et al, 2017b). Hence, processes involved in structuring the GM might often involve multiple spatial scales (Penczykowski et al, 2016;Norman and Koskella, 2017;Laine et al, 2019). In this way, the GM could be regarded as a local community colonized from a regional species pool, i.e., the microbial pool present in the environment (Shapira, 2016;Foster et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Diet and Genotype of an Aquatic Invertebrate Affect the Composition of Free-Living Microbial Communities

et al. 2020

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In spite of the growing interest in the role of the gut microbiome (GM) in host physiology and health, the mechanisms governing its assembly and its effects on the environment are poorly understood. In this article, we show that the host genotype and the GM of Daphnia influence the community structure of the surrounding bacterioplankton (BPK). When Daphnia genotypes were placed in an identical environment, both the GM and BPK showed a genotype and diet-dependent taxonomic composition. Overall, the GM strongly differed from the BPK in taxonomic composition and was characterized by a lower α-diversity, suggesting a selective rejecting of bacteria from the regional species pool. In a microbiome transplant experiment, the assembly of both the GM and BPK was strongly affected by the host genotype and the inoculum to which germ-free Daphnia were exposed. The combination of these results suggests a strong interaction between the host genotype, its GM and free-living microbial communities. Currently, it is generally assumed that an animal's diet has a strong effect on the animal's GM, but only a negligible (if any) effect on the surrounding environment. However, our results indicate that the diet/microbiome inocula have a small effect on the gut community and a large effect on the community in the surrounding environment. This structuring genotype × microbiome × environment effect is an essential prerequisite that could indicate that microbiomes play an important role in eco-evolutionary processes.

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Section: Introductionmentioning

confidence: 99%

Diet and Genotype of an Aquatic Invertebrate Affect the Composition of Free-Living Microbial Communities

et al. 2020

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“…The low levels of gene flow among anther‐smut fungi parasitizing different hosts found in Microbotryum fungi stand in stark contrast to frequent reports of signatures of introgression in other fungal pathogens, such as crop pathogens or human disease‐associated pathogens (Feurtey & Stukenbrock, 2018). Few studies have focused on the diversification of fungal pathogens in natural host communities, while several evolutionary processes, such as the time scale of divergence, host density and heterogeneity, are probably very different from those occurring on human‐modified environment pathogens (Laine, 2005; Laine, Barrès, Numminen, & Siren, 2019; Stukenbrock & McDonald, 2008). To understand how biodiversity arises and what the mechanisms of host–pathogen evolution are over large evolutionary scales, we need more studies on co‐evolutionary histories of parasites and their hosts in natural ecosystems.…”

Section: Discussionmentioning

confidence: 99%

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

et al. 2020

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Study of the congruence of population genetic structure between hosts and pathogens gives important insights into their shared phylogeographical and coevolutionary histories. We studied the population genetic structure of castrating anther‐smut fungi (genus Microbotryum) and of their host plants, the Silene nutans species complex, and the morphologically and genetically closely related Silene italica, which can be found in sympatry. Phylogeographical population genetic structure related to persistence in separate glacial refugia has been recently revealed in the S. nutans plant species complex across Western Europe, identifying several distinct lineages. We genotyped 171 associated plant–pathogen pairs of anther‐smut fungi and their host plant individuals using microsatellite markers and plant chloroplastic single nucleotide polymorphisms. We found clear differentiation between fungal populations parasitizing S. nutans and S. italica plants. The population genetic structure of fungal strains parasitizing the S. nutans plant species complex mirrored the host plant genetic structure, suggesting that the pathogen was isolated in glacial refugia together with its host and/or that it has specialized on the plant genetic lineages. Using random forest approximate Bayesian computation (ABC‐RF), we found that the divergence history of the fungal lineages on S. nutans was congruent with that previously inferred for the host plant and probably occurred with ancient but no recent gene flow. Genome sequences confirmed the genetic structure and the absence of recent gene flow between fungal genetic lineages. Our analyses of individual host–pathogen pairs contribute to a better understanding of co‐evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies remain scarce.

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“…My models (like many others) use an optimistic assumption that any two simultaneous sexuals are capable of finding each other. Real-life search can be very limited; for example, strains of the facultative sexual pathogen Podosphaera plantaginis must coinfect the same plant leaf for outcrossing to occur (Laine et al 2019). Restricted spatial search is particularly likely to create mate limitation in species that do not perform mating-type switching.…”

Section: Ementioning

confidence: 99%

When Synchrony Makes the Best of Both Worlds Even Better: How Well Do We Really Understand Facultative Sex?

Kokko

2020

The American Naturalist

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Biological diversity abounds in potential study topics. Studies of model systems have their advantages, but reliance on a few well-understood cases may create false impressions of what biological phenomena are the norm. Here I focus on facultative sex, which is often hailed as offering the best of both worlds, in that rare sex offers benefits almost equal to obligate sex and avoids paying most of the demographic costs. How well do we understand when and why this form of sexual reproduction is expected to prevail? I show several gaps in the theoretical literature and, by contrasting asynchronous with synchronous sex, highlight the need to link sex theories to the theoretical underpinnings of bet hedging, on the one hand, and to mate limitation considerations, on the other. Condition-dependent sex and links between sex with dispersal or dormancy appear understudied. While simplifications are justifiable as a simple assumption structure enhances analytical tractability, much remains to be done to incorporate key features of real sex to the main theoretical edifice.

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Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation

Cited by 13 publications

References 50 publications

Diet and Genotype of an Aquatic Invertebrate Affect the Composition of Free-Living Microbial Communities

Diet and Genotype of an Aquatic Invertebrate Affect the Composition of Free-Living Microbial Communities

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

When Synchrony Makes the Best of Both Worlds Even Better: How Well Do We Really Understand Facultative Sex?

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