TY - JOUR
T1 - Vertical transmission of cellulolytic protists in termites is imperfect, but sufficient, due to biparental transmission
AU - Velenovsky, Joseph F.
AU - De Martini, Francesca
AU - Hileman, Jonathon T.
AU - Gordon, Johnalyn M.
AU - Su, Nan Yao
AU - Gile, Gillian H.
AU - Chouvenc, Thomas
N1 - Funding Information:
The authors thank Jean Palacios for assisting during hindgut dissections and Zachary Kaplan, Alvin Puzio, and Reynaldo Moscat for providing termite colony maintenance. They also thank Christopher Bilder of The University of Nebraska-Lincoln and Edwin Burgess of The University of Florida for providing statistical advice. This research was supported primarily by NSF-DEB grant No. 1754083 to TC, and in part by USDA-NIFA Hatch Project No. FLA-FTL-005660/No. 1014604 and UF/IFAS Early Career Scientist Seed Grant No. REA1801100 to TC and NSF-DEB grant No. 2045329 to GHG.
Funding Information:
The authors thank Jean Palacios for assisting during hindgut dissections and Zachary Kaplan, Alvin Puzio, and Reynaldo Moscat for providing termite colony maintenance. They also thank Christopher Bilder of The University of Nebraska-Lincoln and Edwin Burgess of The University of Florida for providing statistical advice. This research was supported primarily by NSF-DEB grant No. 1754083 to TC, and in part by USDA-NIFA Hatch Project No. FLA-FTL-005660/No. 1014604 and UF/IFAS Early Career Scientist Seed Grant No. REA1801100 to TC and NSF-DEB grant No. 2045329 to GHG.
Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Nature B.V.
PY - 2023/5
Y1 - 2023/5
N2 - 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.
AB - 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.
KW - Flagellates
KW - Microbiome
KW - Protozoa
KW - Social insects
KW - Subterranean termites
UR - http://www.scopus.com/inward/record.url?scp=85154591257&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85154591257&partnerID=8YFLogxK
U2 - 10.1007/s13199-023-00917-9
DO - 10.1007/s13199-023-00917-9
M3 - Article
AN - SCOPUS:85154591257
SN - 0334-5114
VL - 90
SP - 25
EP - 38
JO - Symbiosis
JF - Symbiosis
IS - 1
ER -