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1. Protist symbionts of termites: diversity, distribution, and coevolution

   https://doi.org/10.1111/brv.13038  

   Gile, Gillian H. (December 2023, Biological Reviews)

   ABSTRACT The symbiosis between termites and their hindgut protists is mutually obligate and vertically inherited. It was established by the late Jurassic in the cockroach ancestors of termites as they transitioned to wood feeding. Since then, protist symbionts have been transmitted from host generation to host generation by proctodeal trophallaxis (anal feeding). The protists belong to multiple lineages within the eukaryotic superphylum Metamonada. Most of these lineages have evolved large cells with complex morphology, unlike the non‐termite‐associated Metamonada. The species richness and taxonomic composition of symbiotic protist communities varies widely across termite lineages, especially within the deep‐branching clade Teletisoptera. In general, closely related termites tend to harbour closely related protists, and deep‐branching termites tend to harbour deep‐branching protists, reflecting their broad‐scale co‐diversification. A closer view, however, reveals a complex distribution of protist lineages across hosts. Some protist taxa are common, some are rare, some are widespread, and some are restricted to a single host family or genus. Some protist taxa can be found in only a few, distantly related, host species. Thus, the long history of co‐diversification in this symbiosis has been complicated by lineage‐specific loss of symbionts, transfer of symbionts from one host lineage to another, and by independent diversification of the symbionts relative to their hosts. This review aims to introduce the biology of this important symbiosis and serve as a gateway to the diversity and systematics literature for both termites and protists. A searchable database with all termite‐protist occurrence records and taxonomic references is provided as a supplementary file to encourage and facilitate new research in this field. 

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2. The Complete Protist Symbiont Communities of Coptotermes formosanus and Coptotermes gestroi : Morphological and Molecular Characterization of Five New Species

   https://doi.org/10.1111/jeu.12815  

   Jasso‐Selles, Daniel E.; De Martini, Francesca; Velenovsky, IV, Joseph F.; Mee, Evan D.; Montoya, Samantha J.; Hileman, Jonathon T.; Garcia, Mikaela D.; Su, Nan‐Yao; Chouvenc, Thomas; Gile, Gillian H. (August 2020, Journal of Eukaryotic Microbiology)

   Abstract Coptotermes formosanusShiraki andCoptotermes gestroi(Wasmann) (Blattoidea: Rhinotermitidae) are invasive subterranean termite pest species with a major global economic impact. However, the descriptions of the mutualistic protist communities harbored in their respective hindguts remain fragmentary. TheC. formosanushindgut has long been considered to harbor three protist species,Pseudotrichonympha grassii(Trichonymphida),Holomastigotoides hartmanni, andCononympha(Spirotrichonympha)leidyi(Spirotrichonymphida), but molecular data have suggested that the diversity may be higher. Meanwhile, theC. gestroicommunity remains undescribed except forPseudotrichonympha leei. To complete the characterization of these communities, hindguts of workers from both termite species were investigated using single‐cell PCR, microscopy, cell counts, and 18S rRNA amplicon sequencing. The two hosts were found to harbor intriguingly parallel protist communities, each consisting of onePseudotrichonymphaspecies, twoHolomastigotoidesspecies, and twoCononymphaspecies. All protist species were unique to their respective hosts, which last shared a common ancestor ~18 MYA. The relative abundances of protist species in each hindgut differed remarkably between cell count data and 18S rRNA profiles, calling for caution in interpreting species abundances from amplicon data. This study will enable future research inC. formosanusandC. gestroihybrids, which provide a unique opportunity to study protist community inheritance, compatibility, and potential contribution to hybrid vigor. 

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3. Context‐dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum

   https://doi.org/10.1111/mec.14449  

   Rock, Danielle I.; Smith, Andrew H.; Joffe, Jonah; Albertus, Amie; Wong, Narayan; O'Connor, Michael; Oliver, Kerry M.; Russell, Jacob A. (December 2017, Molecular Ecology)

   Abstract Animal‐associated microbiomes are often comprised of structured, multispecies communities, with particular microbes showing trends of co‐occurrence or exclusion. Such structure suggests variable community stability, or variable costs and benefits—possibilities with implications for symbiont‐driven host adaptation. In this study, we performed systematic screening for maternally transmitted, facultative endosymbionts of the pea aphid,Acyrthosiphon pisum. Sampling across six locales, with up to 5 years of collection in each, netted significant and consistent trends of community structure. Co‐infections betweenSerratia symbioticaandRickettsiella viridiswere more common than expected, whileRickettsiaand X‐type symbionts colonized aphids withHamiltonella defensamore often than expected.Spiroplasmaco‐infected with other endosymbionts quite rarely, showing tendencies to colonize as a single species monoculture. Field estimates of maternal transmission rates help to explain our findings: whileSerratiaandRickettsiellaimproved each other's transmission,Spiroplasmareduced transmission rates of co‐infecting endosymbionts. In summary, our findings show that North American pea aphids harbour recurring combinations of facultative endosymbionts. Common symbiont partners play distinct roles in pea aphid biology, suggesting the creation of “generalist” aphids receiving symbiont‐based defence against multiple ecological stressors. Multimodal selection, at the host level, may thus partially explain our results. But more conclusively, our findings show that within‐host microbe interactions, and their resulting impacts on transmission rates, are an important determinant of community structure. Widespread distributions of heritable symbionts across plants and invertebrates hint at the far‐reaching implications for these findings, and our work further shows the benefits of symbiosis research within a natural context. 

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

   https://doi.org/10.1093/aob/mcaa021  

   Gundel, Pedro E; Sun, Prudence; Charlton, Nikki D; Young, Carolyn A; Miller, Tom E; Rudgers, Jennifer A (February 2020, Annals of Botany)

   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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5. Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas

   https://doi.org/10.1128/mBio.02104-18  

   Campbell, Matthew A.; Łukasik, Piotr; Meyer, Mariah C.; Buckner, Mark; Simon, Chris; Veloso, Claudio; Michalik, Anna; McCutcheon, John P.; McFall-Ngai, Margaret J. (December 2018, mBio)

   ABSTRACT For insects that depend on one or more bacterial endosymbionts for survival, it is critical that these bacteria are faithfully transmitted between insect generations. Cicadas harbor two essential bacterial endosymbionts, “ Candidatus Sulcia muelleri” and “ Candidatus Hodgkinia cicadicola.” In some cicada species, Hodgkinia has fragmented into multiple distinct but interdependent cellular and genomic lineages that can differ in abundance by more than two orders of magnitude. This complexity presents a potential problem for the host cicada, because low-abundance but essential Hodgkinia lineages risk being lost during the symbiont transmission bottleneck from mother to egg. Here we show that all cicada eggs seem to receive the full complement of Hodgkinia lineages, and that in cicadas with more complex Hodgkinia this outcome is achieved by increasing the number of Hodgkinia cells transmitted by up to 6-fold. We further show that cicada species with varying Hodgkinia complexity do not visibly alter their transmission mechanism at the resolution of cell biological structures. Together these data suggest that a major cicada adaptation to changes in endosymbiont complexity is an increase in the number of Hodgkinia cells transmitted to each egg. We hypothesize that the requirement to increase the symbiont titer is one of the costs associated with Hodgkinia fragmentation. IMPORTANCE Sap-feeding insects critically rely on one or more bacteria or fungi to provide essential nutrients that are not available at sufficient levels in their diets. These microbes are passed between insect generations when the mother places a small packet of microbes into each of her eggs before it is laid. We have previously described an unusual lineage fragmentation process in a nutritional endosymbiotic bacterium of cicadas called Hodgkinia . In some cicadas, a single Hodgkinia lineage has split into numerous related lineages, each performing a subset of original function and therefore each required for normal host function. Here we test how this splitting process affects symbiont transmission to eggs. We find that cicadas dramatically increase the titer of Hodgkinia cells passed to each egg in response to lineage fragmentation, and we hypothesize that this increase in bacterial cell count is one of the major costs associated with endosymbiont fragmentation. 

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