Cellulolytic Protist Numbers Rise and Fall Dramatically in Termite Queens and Kings during Colony Foundation

Abstract

cAmong the best-known examples of mutualistic symbioses is that between lower termites and the cellulolytic flagellate protists in their hindguts. Although the symbiosis in worker termites has attracted much attention, there have been only a few studies of protists in other castes. We have performed the first examination of protist population dynamics in queens and kings during termite colony foundation. Protist numbers, as well as measurements of hindgut and reproductive tissue sizes, were undertaken at five time points over 400 days in incipient colonies of Reticulitermes speratus, as well as in other castes of mature colonies of this species. We found that protist numbers increased dramatically in both queens and kings during the first 50 days of colony foundation but began to decrease by day 100, eventually disappearing by day 400. Hindgut width followed a pattern similar to that of protist numbers, while ovary and testis widths increased significantly only at day 400. Kings were found to contain higher numbers of protists than queens in incipient colonies, which may be linked to higher levels of nutrient transfer from kings to queens than vice versa, as is known in some other termite species. Protists were found to be abundant in soldiers from mature colonies but absent in neotenics. This probably reflects feeding of soldiers by workers via proctodeal trophallaxis and of reproductives via stomodeal trophallaxis. The results reveal the dynamic nature of protist numbers during colony foundation and highlight the trade-offs that exist between reproduction and parental care during this critical phase of the termite life cycle.

Irreversible transfer of brood care duties and insights into the burden of caregiving in incipient subterranean termite colonies

“…This result showed that the only available worker had the ability to provide enough behavioural and nutritional support for the king and queen, but the burden of the brood was too much for this single worker, as only a handful of neonate individuals were able to develop and survive. One key observation from our study is that, as the king and queen became dependent, as a result of the loss of their symbiotic gut fauna (Shimada et al, 2013), and because only larvae of at least third instar (i.e. worker) have acquired symbiotic protozoa (Grassé & Noirot, 1945), a single worker can function as the sole source of re-inoculation for the rebounding colony after the loss of most of its brood and its entire workforce except for one worker.…”

“…() showed that artificial king and queen defaunation within the first 2 months in incipient colonies led to brood cannibalism, suggesting that without their symbionts, primary reproductives cannot provide nutritional care to the first neonates or themselves, as they became nutritionally dependent on their own brood through cannibalism, until the colony collapses. In addition, in Reticulitermes speratus (Kolbe), the gut fauna of the primary reproductives started decreasing at 100 days and eventually disappeared completely by 400 days, confirming that, relatively quickly after foundation and shortly after workers are produced, the ability of the king and queen to be caregivers and self‐sufficient progressively vanishes (Shimada et al, ). These previous observations all indicate that in our experiment, when all workers were removed at 150 days, a workerless family unit essentially lost its ability to digest wood and its nurturing ability, resulting in their rapid death.…”

Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host

“…Our findings are consistent with the notion that the microbiome of wood-dwelling species bears an imprint of its specialization on degrading a uniform wood diet, while the microbiome of the foraging species might reflect its adaption to access growth limiting 51 52 between protist generations. In return, protists and bacteria are vertically transmitted between termite generations via proctodeal trophallaxis during colony foundation [25].…”

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

“…In some social insect clades, the reproductive caste microbiome is distinct and drastically simplified compared to that of the worker caste. Foraging lower termite reproductives generally lack symbiotic protists that dominate the worker guts (Shimada et al, 2013;Inagaki and Matsuura, 2016), and the reproductive caste of Termitidae termites shows reduced diversity and disparate bacterial community composition (Otani et al, 2019) compared to the worker caste (Dietrich et al, 2014;Otani et al, 2014Otani et al, , 2016Otani et al, , 2019. Honey bee queens also host a simplified bacterial community that is significantly reduced compared to workers (Kapheim et al, 2015;Tarpy et al, 2015;Anderson et al, 2018).…”