Vertical transmission of cellulolytic protists in termites is imperfect, but sufficient, due to biparental transmission

Velenovsky, Joseph F.; Martini, Francesca; Hileman, Jonathon T.; Gordon, Johnalyn M.; Su, Nan‐Yao; Gile, Gillian H.; Chouvenc, Thomas

doi:10.1007/s13199-023-00917-9

Cited by 9 publications

(17 citation statements)

References 83 publications

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“…This result was consistent with previous studies examining Reticulitermes grassei [23] and Coptotermes sp. [25]. Velenovsky et al (2023) suggested that biparental transmission contributes significantly to the high rates of occurrence of protist species in field colonies of Coptotermes sp.…”

Section: Discussionmentioning

confidence: 99%

“…Alates emerge from last-instar nymphs in the colony through adult eclosion and remain in the nest prior to swarming flight. To facilitate wider dispersion, their weight declines before flight, and they carry a very small number of protists [22-25], thus causing a significant bottleneck in protist community transmission. Therefore, investigating the dynamics of protist communities during this period is important in order to understand how termites overcome the significant bottleneck effect that occurs every generation.…”

Section: Introductionmentioning

confidence: 99%

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Transmission dynamics of symbiotic protist communities in the termite gut: association with host adult eclosion and dispersal

Inagaki,

Igai,

Takahashi

et al. 2023

Preprint

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The fidelity of vertical transmission is a critical factor in maintaining mutualistic associations with microorganisms. The obligate mutualism between termites and intestinal protist communities has been maintained for over 130 million years, suggesting the faithful transmission of diverse protist species across host generations. Although a severe bottleneck can occur when alates disperse with gut protists, how protist communities are maintained during this process remains largely unknown. In this study, we examined the dynamics of intestinal protist communities during adult eclosion and alate dispersal in the termiteReticulitermes speratus. We found that the protist community structure in last-instar nymphs differed significantly from that in workers and persisted intact during adult eclosion, in contrast to moults between workers, in which all protists disappeared from the gut. The number of protists in nymphs and alates was substantially lower than in workers, whereas the proportion of protist species exhibiting low abundance in workers was higher in nymphs and alates. Using a simulation-based approach, we demonstrate that such changes in the protist community composition of nymphs and alates improve the transmission efficiency of whole protist species. This study thus provides novel insights into how termites have maintained mutualistic relationships with diverse gut microbiota for generations.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transmission dynamics of symbiotic protist communities in the termite gut: association with host adult eclosion and dispersal

Inagaki,

Igai,

Takahashi

et al. 2023

Preprint

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show abstract

“…An explanation for this is that intrinsic N 2 fixation may occur in the gut in quantities sufficient to maintain the colony, and to account for unavoidable loss through volatilization or denitrification (Mullins and Cochran 1975). It is unclear whether the nitrogen fixation in the gut of the Rhinotermitidae is from soil-derived diazotrophs, or rather intrinsic, specific symbionts passed down through vertical transmission (Velenovsky et al 2023). Perhaps it is a mixture of the 2.…”

Section: Discussionmentioning

confidence: 99%

Nitrogen fixation in different termite lineages and diets

Mullins,

2023

Annals of the Entomological Society of America

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Nitrogen fixation is often cited as an important nitrogen source for termites. However, the rate of nitrogen fixation between experiments and termite species is highly variable due to termite diversity and sampling limitations. New evidence suggests that subterranean termites (Coptotermes formosanus Shiraki) (Blattodea, Rhinotermitidae) seek alternative dietary nitrogen sources for colony growth and development. This study compares N2 fixation rates and nitrogenase gene expression rates to a diverse assemblage of feeding groups. It was observed that nitrogenase expression was much higher in one-piece nesting termites from the family Kalotermitidae which lack access to soil. On the other hand, subterranean termites from the family Rhinotermitidae fix nitrogen at much lower rates, not differing from ambient nitrogenase activity in soil.

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“…Perhaps in order to be lightweight for flying, alates leave the nest with a relatively small mass of hindgut symbionts, which frequently means that one or more protist species is missing (May, 1941). In a recent molecular analysis of C. formosanus and Coptotermes gestroi, 97% of field-caught alates and 53% of laboratory-reared colonies were found to be missing one or more protist species (Velenovsky et al, 2023). Deficient protist communities in alates can be complemented by the mate's community in many cases, but if both alates are missing the same symbiont, the new colony will lack it too.…”

Section: The Symbiosismentioning

confidence: 99%

“…Host reproductive biology supports this view: recall that alates often leave their parental colonies with a deficient symbiont fauna that might or might not be complemented by their mating partner. Symbiont-deficient alates have been repeatedly observed in the field, as have symbiont-deficient colonies (Kitade & Matsumoto, 1993b;Michaud et al, 2020;Velenovsky et al, 2023). If the loss of a symbiont species happens so frequently at the population level, it stands to reason that this process would influence the distribution of protists across hosts on deeper evolutionary timescales as well.…”

Section: Co-phylogenetic Signal Decaymentioning

confidence: 99%

Protist symbionts of termites: diversity, distribution, and coevolution

Gile

2023

Biological Reviews

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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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Vertical transmission of cellulolytic protists in termites is imperfect, but sufficient, due to biparental transmission

Cited by 9 publications

References 83 publications

Transmission dynamics of symbiotic protist communities in the termite gut: association with host adult eclosion and dispersal

Transmission dynamics of symbiotic protist communities in the termite gut: association with host adult eclosion and dispersal

Nitrogen fixation in different termite lineages and diets

Protist symbionts of termites: diversity, distribution, and coevolution

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