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Many host-symbiont relationships are maintained through vertical transmission. While maternal symbiont transmission is common, biparental transmission is relatively rare. Protist-dependent termites are eusocial insects that harbor obligate, cellulolytic protists in their hindguts. Protists are vertically transmitted by winged reproductives (alates), which disperse to biparentally establish new colonies. Vertical transmission in protist-dependent termites is imperfect, as the protist communities of alates are often incomplete. Biparental transmission of protists may make it unnecessary for alates to harbor complete communities, as colonies would acquire symbionts from both founding kings and queens, which together may harbor sufficient inoculums. To investigate this hypothesis, the protist communities of Coptotermes gestroi and C. formosanus alates and colonies were examined using 18S rRNA amplicon sequencing. The complete protist communities of these Coptotermes species are composed of five parabasalid species each. Whereas alates often harbored 1–3 protist species, nearly all colonies harbored 4–5 species, implying biparental transmission. The probability of each protist species being present in at least one founding alate was used to determine expected protist occurrence in colonies. For most protists, expected and observed occurrence did not significantly differ, suggesting that each protist species only needs to be harbored by one founding alate to be acquired by colonies. Our results imply that biparental transmission allows founding reproductives to transmit adequate symbiont communities to colonies despite their individual communities being incomplete. We discuss biparental transmission in protist-dependent termites in the context of other biparentally transmitted symbioses. 

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.