Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis

Abstract Background and Aims The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? Methods We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. Key Results Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. Conclusions Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.

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Elucidation of the Transmission Patterns of an Insect-Borne Bacterium

Applied and Environmental Microbiology ◽

10.1128/aem.69.8.4403-4407.2003 ◽

2003 ◽

Vol 69 (8) ◽

pp. 4403-4407 ◽

Cited By ~ 70

Author(s):

A. C. Darby ◽

A. E. Douglas

Keyword(s):

Vertical Transmission ◽

Acyrthosiphon Pisum ◽

Deterministic Model ◽

Transmission Rate ◽

Horizontal Transmission ◽

Natural Populations ◽

Oral Route ◽

Pea Aphid ◽

Diagnostic Pcr ◽

Modes Of Transmission

ABSTRACT Quantitative data on modes of transmission are a crucial element in understanding the ecology of microorganisms associated with animals. We investigated the transmission patterns of a γ-proteobacterium informally known as pea aphid Bemisia-like symbiont (PABS), also known as T-type, which is widely but not universally distributed in natural populations of the pea aphid, Acyrthosiphon pisum. The vertical transmission of PABS to asexual and sexual morphs and sexually produced eggs was demonstrated by a diagnostic PCR-based assay, and the maximum estimated failure rate was 2%. Aphids naturally lacking PABS acquired PABS bacteria administered via the diet, and the infection persisted by vertical transmission for at least three aphid generations. PABS was also detected in two of five aphid honeydew samples tested and in all five siphuncular fluid samples tested but in none of 15 samples of salivary secretions from PABS-positive aphids. However, PABS-negative aphids did not acquire PABS when they were cocultured with PABS-positive aphids; the maximal estimated level of horizontal transmission was 18%. A deterministic model indicated that the force of infection by a horizontal transmission rate of 3% is sufficient to maintain a previously described estimate of the prevalence of PABS-positive aphids (37%), if the vertical transmission rate is 98%. We concluded that PABS infections in A. pisum can be maintained by high vertical transmission rates and occasional horizontal transmission, possibly via the oral route, in the absence of selection either for or against aphids bearing this bacterium.

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Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses

10.1101/412882 ◽

2018 ◽

Cited By ~ 2

Author(s):

Shelbi L Russell

Keyword(s):

Vertical Transmission ◽

Horizontal Transmission ◽

Transmission Mode ◽

Symbiotic Associations ◽

Transmission Modes ◽

Symbiont Transmission ◽

Environment Type ◽

Full Separation ◽

Host Evolution ◽

Host Tissues

AbstractSymbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. Anecdotal observations suggest that symbionts of terrestrial hosts tend to be strictly vertically inherited through host tissues, whereas symbionts of marine hosts tend towards horizontal transmission. Aside from a few cursory investigations, the rates and distributions of transmission modes have not been investigated in depth across associations, despite the consequences for symbiont and host evolution. To address this empirically and estimate the rate of each mode, I compiled data from the literature and for associations between transmission mode and the environment, transmission route, symbiont function, and taxa involved in the symbiosis. Of the 441 analyzed symbioses, 50.1% were strictly vertically transmitted, 34.0% exhibited some form of mixed mode transmission, and 15.9% were strictly horizontally transmitted. Binning symbioses by their environment revealed a significant skew towards vertical transmission on land and horizontal transmission in aquatic environments, with mixed modes abundant in both. However, host and symbiont taxa were not randomly distributed, which prevented the full separation of these variables. Overall, the data suggest that many symbiotic taxa are capable of horizontal transmission and barriers exist that reduce the rate of these events. Thus, both the environment type and host/symbiont taxa combined influence symbiont transmission mode evolution.One sentence summaryThrough an intensive analysis of the literature on symbiosis transmission modes, estimated rates for each transmission mode were calculated, revealing bias for horizontal transmission in the ocean and vertical transmission on land.

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Can Differences in Symbiont Transmission Mode Explain the Abundance and Distribution of Fungus-Growing Termites in West Africa?

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2020.600318 ◽

2020 ◽

Vol 8 ◽

Author(s):

Judith Korb ◽

Simon Kolotchèlèma Silué ◽

N'golo Abdoulaye Koné

Keyword(s):

Vertical Transmission ◽

National Parks ◽

Horizontal Transmission ◽

Species Abundance ◽

Transmission Mode ◽

Termite Species ◽

Symbiont Transmission ◽

Ecological Dominance ◽

Study Sites ◽

Abundance And Distribution

Fungus-growing termites (Isoptera: Macrotermitinae) dominate African savannah ecosystems where they play important roles in ecosystem functioning. Their ecological dominance in these ecosystems has been attributed to living in an ectosymbiosis with fungi of the genus Termitomyces (Lyophyllaceae). Evolutionary theory predicts that the transmission mode of a symbiont determines cooperation and conflict between host and symbiont with vertical transmission (co-transmission of host and symbiont offspring to the next generation) leading to less conflict than horizontal transmission (symbionts are acquired by the host from the environment). Thus, one can hypothesize associations with vertical transmission to be ecological more successful than those with horizontal transmission. We tested this by analyzing whether there is an association between transmission mode and fungus-growing termite species abundance and distribution in West-African savannah and forest ecosystems. We used data from a total of 78 study sites comprising protected National Parks as well as anthropogenically disturbed ecosystems, covering Benin, Côte d'Ivoire, and Togo. Our results showed that, in contrast to expectation, species with horizontal symbiont transmission were more common. We encountered more often species with horizontal than vertical transmission. This result might be due to the fact that only five out of the 25 identified fungus-growing termite species had vertical transmission. Yet, species with horizontal transmission also had higher relative abundances within study sites than those with vertical transmission. Thus, transmission mode is unlikely to explain abundance differences between fungus-growing termite species.

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Evolution of symbiont transmission in conditional mutualisms in spatially and temporally variable environments

10.1101/2020.05.05.079103 ◽

2020 ◽

Author(s):

Alexandra Brown ◽

Erol Akçay

Keyword(s):

Vertical Transmission ◽

Horizontal Transmission ◽

Environmental Variation ◽

Transmission Mode ◽

Trade Off ◽

Symbiotic Relationships ◽

Physiological Constraints ◽

Fitness Effects ◽

Variable Environments ◽

Symbiont Transmission

AbstractSymbiotic relationships affect the fitness and organismal function of virtually all organisms. In many cases, the fitness effects of symbiosis may be beneficial or harmful depending on the environment. The hosts of such symbionts are favored to acquire them only when the symbiont is beneficial. However, it is not clear whether such selection favors vertical or horizontal transmission, both, or neither. To address this question, we model the evolution of transmission mode in a conditional mutualism experiencing spatial and temporal environmental variation. We find that when symbionts affect host lifespan, but not fecundity, horizontal transmission can contain them to beneficial environments. Vertical transmission can produce symbiont containment when the environmental state is synchronized across locations. We also find an emergent trade-off between horizontal and vertical transmission, suggesting that physiological constraints are not required for the evolution of limits on the total amount of transmission.

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A symbiont's dispersal strategy: condition-dependent dispersal underlies predictable variation in direct transmission among hosts

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2081 ◽

2015 ◽

Vol 282 (1819) ◽

pp. 20152081 ◽

Cited By ~ 8

Author(s):

James Skelton ◽

Robert P. Creed ◽

Bryan L. Brown

Keyword(s):

Transmission Rate ◽

Horizontal Transmission ◽

Host Size ◽

Dispersal Strategy ◽

Contact Rates ◽

Symbiont Transmission ◽

Strategy Condition ◽

Living Organisms ◽

Host Infection ◽

Better Than

Direct horizontal transmission of pathogenic and mutualistic symbionts has profound consequences for host and symbiont fitness alike. While the importance of contact rates for transmission is widely recognized, the processes that underlie variation in transmission during contact are rarely considered. Here, we took a symbiont's perspective of transmission as a form of dispersal and adopted the concept of condition-dependent dispersal strategies from the study of free-living organisms to understand and predict variation in transmission in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. Field study showed that symbiont reproductive success was correlated with host size and competition among worms for microhabitats. Laboratory experiments demonstrated high variability in transmission among host contacts. Moreover, symbionts were more likely to disperse when host size and competition for microhabitat created a fitness environment below a discrete minimum threshold. A predictive model based on a condition-dependent symbiont dispersal strategy correctly predicted transmission in 95% of experimental host encounters and the exact magnitude of transmission in 67%, both significantly better than predictions that assumed a fixed transmission rate. Our work provides a dispersal-based understanding of symbiont transmission and suggests adaptive symbiont dispersal strategies can explain variation in transmission dynamics and complex patterns of host infection.

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Vertical transmission of zika virus in Aedes albopictus

PLoS Neglected Tropical Diseases ◽

10.1371/journal.pntd.0008776 ◽

2020 ◽

Vol 14 (10) ◽

pp. e0008776

Author(s):

Zetian Lai ◽

Tengfei Zhou ◽

Jiayong Zhou ◽

Shuang Liu ◽

Ye Xu ◽

...

Keyword(s):

Vertical Transmission ◽

Aedes Albopictus ◽

Reverse Transcription ◽

Zika Virus ◽

Transmission Rate ◽

Horizontal Transmission ◽

Infection Rates ◽

Transmission Rates ◽

Suckling Mice ◽

Reverse Transcription Pcr

Background Zika virus (ZIKV) is an arthropod-borne flavivirus transmitted by Aedes mosquitoes. Aedes albopictus is an important vector of ZIKV worldwide. To date, most experiments have focused on the vertical transmission of ZIKV in Ae. aegypti, while studies on Ae. albopictus are very limited. To explore vertical transmission in Ae. albopictus, a series of laboratory studies were carried out. Methodology/Principal findings In this study, Ae. albopictus were blood-fed with ZIKV-infectious blood, and the ovaries and offspring viral infection rates were analyzed by reverse transcription PCR (RT-PCR), real-time reverse transcription PCR (RT-qPCR) and immunohistochemistry (IHC). ZIKV was detected in the ovaries and oviposited eggs in two gonotrophic cycles. The minimum filial egg infection rates in two gonotrophic cycles were 2.06% and 0.69%, and the effective population transmission rate was 1.87%. The hatching, pupation, and emergence rates of infected offspring were not significantly different from those of uninfected offspring, indicating that ZIKV did not prevent the offspring from completing the growth and development process. ZIKV was detected in three of thirteen C57BL/6 suckling mice bitten by ZIKV-positive F1 females, and the viremia persisted for at least seven days. Conclusions/Significance ZIKV can be vertically transmitted in Ae. albopictus via transovarial transmission. The vertical transmission rates in F1 eggs and adults were 2.06% and 1.87%, respectively. Even though the vertical transmission rates were low, the female mosquitoes infected via the congenital route horizontally transmitted ZIKV to suckling mice through bloodsucking. This is the first experimental evidence of offspring with vertically transmitted ZIKV initiating new horizontal transmission. The present study deepens the understanding of the vertical transmission of flaviviruses in Aedes mosquitoes and sheds light on the prevention and control of mosquito-borne diseases.

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An agent-based model of adaptation of holobionts with different microbial symbiont transmission modes

10.1101/2020.10.08.330902 ◽

2020 ◽

Author(s):

Siao Ye ◽

Zhu Liu ◽

Evan Siemann

Keyword(s):

Abiotic Stress ◽

Stress Tolerance ◽

Vertical Transmission ◽

Horizontal Transmission ◽

Agent Based Model ◽

Agent Based ◽

Transmission Modes ◽

Microbial Symbiont ◽

Symbiont Transmission ◽

Microbial Symbionts

ABSTRACTThe hologenome theory suggests that holobionts (host plus symbiont) with hosts that are only able to adapt slowly may be able to persist in deteriorating environmental conditions via rapid adaptation of their microbial symbionts. The effectiveness of such symbiont adaptation may vary depending on whether symbionts are passed directly to offspring (vertical transmission) or acquired from the environment (horizontal transmission). However, it has been suggested that holobionts with horizontal transmission cannot pass down their symbionts faithfully, preventing adaptation at the holobiont level because of host-symbiont disassociation between generations. Here we used an agent-based model to investigate whether holobionts with horizontal microbial symbiont transmission can adapt to increasing stress solely through symbiont adaptation and compared their adaptation to holobionts with vertical transmission. We found that holobionts with either transmission mode were able to adapt to increasing abiotic stress solely via symbiont adaptation. Moreover, those with horizontal transmission were more competitive than those with vertical transmission when hosts were able to selectively associate with the most suitable symbionts. However, those with horizontal transmission were less competitive than those with vertical transmission when symbiont establishment was random. Our results support the hologenome theory and demonstrate that holobionts with horizontal microbial symbiont transmission could adapt to increasing abiotic stress via their symbionts. We also showed that whether holobionts with horizontal or vertical symbiont transmission are favored in increasingly stressful conditions depends on the ability of hosts to recognize and foster microbial symbionts that confer stress tolerance.IMPORTANCESymbiotic organisms such as reef building corals are sensitive to environmental perturbations due to anthropogenic disturbances or climate change, and it is critical to understand whether they are able to adapt to previously unfavorable conditions. To date, studies have focused on the impacts of existing microbial symbiont variation on holobiont stress tolerance but here we use agent-based models to explore holobiont adaptation via symbiont adaptation. We studied both deterministic and stochastic processes in holobiont adaptation by investigating the following four factors: holobiont transmission modes, a host’s ability to recognize tolerance-conferring symbionts, a symbiont’s mutational variance, and rate of stress increase. Our simulation provides a comprehensive understanding of holobiont adaptation under stress, which not only has implications for future endangered symbiotic species management, but also provides fresh insight into species evolution as proposed by the hologenome theory.

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Mother-child transmission of Chagas disease: could coinfection with human immunodeficiency virus increase the risk?

Revista da Sociedade Brasileira de Medicina Tropical ◽

10.1590/s0037-86822009000200002 ◽

2009 ◽

Vol 42 (2) ◽

pp. 107-109 ◽

Cited By ~ 30

Author(s):

Pablo Gustavo Scapellato ◽

Edgardo Gabriel Bottaro ◽

María Teresa Rodríguez-Brieschke

Keyword(s):

Human Immunodeficiency Virus ◽

Trypanosoma Cruzi ◽

Chagas Disease ◽

Vertical Transmission ◽

Disease Transmission ◽

Transmission Rate ◽

Buffy Coat ◽

Child Transmission ◽

Serological Tests ◽

Immunodeficiency Virus

A study was conducted on all newborns from mothers with Chagas disease who were attended at Hospital Donación F. Santojanni between January 1, 2001, and August 31, 2007. Each child was investigated for the presence of Trypanosoma cruzi parasitemia through direct examination of blood under the microscope using the buffy coat method on three occasions during the first six months of life. Serological tests were then performed. Ninety-four children born to mothers infected with Trypanosoma cruzi were attended over the study period. Three of these children were born to mothers coinfected with the human immunodeficiency virus. Vertical transmission of Chagas disease was diagnosed in 13 children, in all cases by identifying parasitemia. The overall Chagas disease transmission rate was 13.8% (13/94). It was 100% (3/3) among the children born to mothers with HIV infection and 10.9% (10/91) among children born to mothers without HIV [Difference = 0.89; CI95 = 0.82-0.95; p = 0.0021]. We concluded that coinfection with HIV could increase the risk of vertical transmission of Chagas disease.

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