Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agresti A, Liu I-M (1999) Modeling a categorical variable allowing arbitrarily many category choices. Biometrics 55:936–943. https://doi.org/10.1111/j.0006-341X.1999.00936.x
Balmand S, Lohs C, Aksoy S, Heddi A (2013) Tissue distribution and transmission routes for the tsetse fly endosymbionts. J Invertebr Pathol 112:S116–S122. https://doi.org/10.1016/j.jip.2012.04.002
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. P Natl Acad Sci USA 115:6506–6511. https://doi.org/10.1073/pnas.1711842115
Bilder CR, Loughin TM (2004) Testing for marginal independence between two categorical variables with multiple responses. Biometrics 60:241–248. https://doi.org/10.1111/j.0006-341X.2004.00147.x
Bilder CR, Loughin TM, Nettleton D (2000) Multiple marginal independence testing for pick any/c variables. Commun Stat Simul Comput 29:1285–1316. https://doi.org/10.1080/03610910008813665
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. https://doi.org/10.1186/s40168-018-0470-z
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Bourguignon T, Lo N, Dietrich C, Šobotník J, Sidek S, Roisin Y, Brune A, Evans TA (2018) Rampant host switching shaped the termite gut microbiome. Curr Biolo 28:649–654. https://doi.org/10.1016/j.cub.2018.01.035
Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. https://doi.org/10.1038/nrmicro2262
Brossette L, Meunier J, Dupont S, Bagnères AG, Lucas C (2019) Unbalanced biparental care during colony foundation in two subterranean termites. Ecol Evol 9:192–200. https://doi.org/10.1002/ece3.4710
Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180. https://doi.org/10.1038/nrmicro3182
Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166. https://doi.org/10.1146/annurev-micro-092412-155715
Brune A, Ohkuma M (2011) Role of the termite gut microbiota in symbiotic digestion. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, The Netherlands, pp 439–475
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Chouvenc T (2019) The relative importance of queen and king initial weights in termite colony foundation success. Insectes Soc 66:177–184. https://doi.org/10.1007/s00040-019-00690-3
Chouvenc T (2022) Eusociality and the transition from biparental to alloparental care in termites. Funct Ecol. https://doi.org/10.1111/1365-2435.14183
Chouvenc T, Helmick EE, Su N-Y (2015) Hybridization of two major termite invaders as a consequence of human activity. PLoS ONE 10:e0120745. https://doi.org/10.1371/journal.pone.0120745
Chouvenc T, Scheffrahn RH, Mullins AJ, Su N-Y (2017) Flight phenology of two Coptotermes species (Isoptera: Rhinotermitidae) in southeastern Florida. J Econ Entomol 110:1693–1704. https://doi.org/10.1093/jee/tox136
Chouvenc T, Šobotník J, Engel MS, Bourguignon T (2021) Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cell Mol Life Sci 78:2749–2769. https://doi.org/10.1007/s00018-020-03728-z
Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL (2017) Horizontal transmission of intracellular insect symbionts via plants. Front Microbiol 8:2237. https://doi.org/10.3389/fmicb.2017.02237
Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. P Natl Acad Sci USA 9:424–428. https://doi.org/10.1073/pnas.9.12.424
Cleveland LR (1924) The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol Bull 46:203–227. https://doi.org/10.2307/1536724
Cleveland LR (1925) The feeding habit of termite castes and its relation to their intestinal flagellates. Biol Bull 48:295–308. https://doi.org/10.2307/1536598
Collins NM (1981) The role of termites in the decomposition of wood and leaf litter in the Southern Guinea savanna of Nigeria. Oecologia 51:389–399. https://doi.org/10.1007/BF00540911
Cook TJ, Gold RE (1998) Organization of the symbiotic flagellate community in three castes of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 31:25–39
Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P, Esposito F, Bandi C, Daffonchio D, Favia G (2008) Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol 18:R1087–R1088. https://doi.org/10.1016/j.cub.2008.10.040
Dan H, Ikeda N, Fujikami M, Nakabachi A (2017) Behavior of bacteriome symbionts during transovarial transmission and development of the asian citrus psyllid. PLoS ONE 12:e0189779. https://doi.org/10.1371/journal.pone.0189779
De Martini F, Coots NL, Jasso-Selles DE, Shevat J, Ravenscraft A, Stiblík P, Šobotník J, Sillam-Dussès D, Scheffrahn RH, Carrijo TF, Gile GH (2021) Biogeography and independent diversification in the protist symbiont community of Heterotermes tenuis. Front Ecol Evol 9:640625. https://doi.org/10.3389/fevo.2021.640625
De Vooght L, Caljon G, Van Hees J, Van Den Abbeele J (2015) Paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly. Mol Biol Evol 32:1977–1980. https://doi.org/10.1093/molbev/msv077
del Campo J, James ER, Hirakawa Y, Fiorito R, Kolisko M, Irwin NAT, Mathur V, Boscaro V, Hehenberger E, Karnkowska A, Scheffrahn RH, Keeling PJ (2017) Pseudotrichonympha leei, Pseudotrichonympha lifesoni, and Pseudotrichonympha pearti, new species of parabasalian flagellates and the description of a rotating subcellular structure. Sci Rep 7:16349. https://doi.org/10.1038/s41598-017-16259-8
Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516. https://doi.org/10.1590/S1519-566X2001000400001
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37. https://doi.org/10.1146/annurev.ento.43.1.17
Douglas AE (2016) How multi-partner endosymbioses function. Nat Rev Microbiol 14:731–743. https://doi.org/10.1038/nrmicro.2016.151
Ebert D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst 44:623–643. https://doi.org/10.1146/annurev-ecolsys-032513-100555
Eggleton P (2011) An introduction to termites: biology, taxonomy, and functional morphology. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, The Netherlands, pp 1–26
Eggleton P (2020) The state of the world’s insects. Annu Rev Environ Resour 45:61–82. https://doi.org/10.1146/annurev-environ-012420-050035
Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 2009:1–27. https://doi.org/10.1206/651.1
Fisher RM, Henry LM, Cornwallis CK, Kiers ET, West SA (2017) The evolution of host-symbiont dependence. Nat Commun 8:15973. https://doi.org/10.1038/ncomms15973
Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68:389–396. https://doi.org/10.1128/AEM.68.1.389-396.2002
Grassé P-P, Noirot C (1945) La transmission des flagellés symbiotiques et les aliments des termites. Bull Biol France Belg 79:273–297
Griffiths HM, Ashton LA, Evans TA, Parr CL, Eggleton P (2019) Termites can decompose more than half of deadwood in tropical rainforest. Curr Biol 29:R118–R119. https://doi.org/10.1016/j.cub.2019.01.012
Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237. https://doi.org/10.1038/nmeth.1184
Honigberg BM (1970) Protozoa associated with termites and their role in digestion. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, New York, New York, pp 1–36
Inagaki T, Yanagihara S, Fuchikawa T, Matsuura K (2020) Gut microbial pulse provides nutrition for parental provisioning in incipient termite colonies. Behav Ecol Sociobiol 74:64. https://doi.org/10.1007/s00265-020-02843-y
Inagaki T, Nozaki T, Matsuura K (2022) Rapid elimination of symbiotic intestinal protists during the neotenic differentiation in a subterranean termite, Reticulitermes speratus. Insectes Soc. https://doi.org/10.1007/s00040-022-00877-1
Jasso-Selles DE, De Martini F, Freeman KD, Garcia MD, Merrell TL, Scheffrahn RH, Gile GH (2017) The parabasalid symbiont community of Heterotermes aureus: molecular and morphological characterization of four new species and reestablishment of the genus Cononympha. Eur J Protistol 61:48–63. https://doi.org/10.1016/j.ejop.2017.09.001
Jasso-Selles DE, De Martini F, Velenovsky IV JF, Mee ED, Montoya SJ, Hileman JT, Garcia MD, Su N-Y, Chouvenc T, Gile GH (2020) The complete protist symbiont communities of Coptotermes formosanus and Coptotermes gestroi: morphological and molecular characterization of five new species. J Eukaryot Microbiol 67:626–641. https://doi.org/10.1111/jeu.12815
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112. https://doi.org/10.1146/annurev.ecolsys.29.1.83
Kirby H (1937) Host-parasite relations in the distribution of protozoa in termites. Univ Calif Publ Zool 41:189–212
Kitade O, Matsumoto T (1993) Symbiotic protistan faunae of Reticulitermes (Isoptera: Rhinotermitidae) in the Japan archipelago. Sociobiology 23:135–153
Kitade O, Hayashi Y, Takatsuto K, Matsumoto T (2012) Variation and diversity of symbiotic protist composition in the damp-wood termite hodotermopsis sjoestedti. Jpn J Protozool 45:29–36. https://doi.org/10.18980/jjprotozool.45.1-2_29
Koidzumi M (1921) Studies on the intestinal protozoa found in the termites of Japan. Parasitology 13:235–309. https://doi.org/10.1017/S0031182000012506
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Koziol NA, Bilder CR (2014) MRCV: a package for analyzing categorical variables with multiple response options. R J 6:144–150. https://doi.org/10.32614/RJ-2014-014
Krishna K (1969) Introduction. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, New York, pp 1–17
Lai PY, Tamashiro M, Fujii JK (1983) Abundance and distribution of the three species of symbiotic protozoa in the hindgut of Coptotermes formosanus (Isoptera: Rhinotermitidae). Proc Hawaii Entomol Soc 24:271–276
LeBoeuf AC, Waridel P, Brent CS, Gonçalves AN, Menin L, Ortiz D, Riba-Grognuz O, Koto A, Soares ZG (2016) Oral transfer of chemical cues, growth proteins, and hormones in social insects. eLife 5:e20375. https://doi.org/10.7554/eLife.20375
Lewis JL, Forschler BT (2004) Protist communities from four castes and three species of Reticulitermes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 97:1242–1251. https://doi.org/10.1603/0013-8746(2004)097[1242:PCFFCA]2.0.CO;2
Lund MB, Holmstrup M, Lomstein BA, Damgaard C, Schramm A (2010) Beneficial effect of Verminephrobacter nephridial symbionts on the fitness of the earthworm Aporrectodea tuberculata. Appl Environ Microbiol 76:4738–4743. https://doi.org/10.1128/AEM.00108-10
May E (1941) The behavior of the intestinal protozoa of termites at the time of the last ecdysis. Trans Am Microsc Soc 60:281–292. https://doi.org/10.2307/3222824
McMahan EA (1969) Feeding relationships and radioisotope techniques. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, New York, pp 387–406
Michaud C, Hervé V, Dupont S, Dubreuil G, Bézier AM, Meunier J, Brune A, Dedeine F (2020) Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood-feeding termite. Mol Ecol 29:308–324. https://doi.org/10.1111/mec.15322
Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. P Natl Acad Sci USA 103:12803–12806. https://doi.org/10.1073/pnas.0605772103
Mullins A, Su N-Y (2018) Parental nitrogen transfer and apparent absence of N2 fixation during colony foundation in Coptotermes formosanus Shiraki. Insects 9:37. https://doi.org/10.3390/insects9020037
Nalepa CA (1984) Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). Behav Ecol Sociobiol 14:273–279. https://doi.org/10.1007/BF00299498
Nalepa CA (2011) Body size and termite evolution. Evol Biol 38:243–257. https://doi.org/10.1007/s11692-011-9121-z
Nalepa CA (2015) Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments. Ecol Entomol 40:323–335. https://doi.org/10.1111/een.12197
Nalepa CA (2017) What kills the hindgut flagellates of lower termites during the host molting cycle? Microorganisms 5:82. https://doi.org/10.3390/microorganisms5040082
Nalepa CA, Bignell DE, Bandi C (2001) Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Soc 48:194–201. https://doi.org/10.1007/PL00001767
Nishimura Y, Otagiri M, Yuki M, Shimizu M, Inoue J-i, Moriya S, Ohkuma M (2020) Division of functional roles for termite gut protists revealed by single-cell transcriptomes. ISME J 14:2449–2460. https://doi.org/10.1038/s41396-020-0698-z
Noirot C, Darlington JPEC (2000) Termite nests: architecture, regulation and defence. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 121–139
Nutting WL (1956) Reciprocal protozoan transfaunations between the roach, Cryptocercus, and the termite. Zootermopsis Biol Bull 110:83–90. https://doi.org/10.2307/1538895
Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, New York, pp 233–282
Ohkuma M, Brune A (2011) Diversity, structure, and evolution of the termite gut microbial community. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, The Netherlands, pp 413–438
Paz L-C, Schramm A, Lund MB (2017) Biparental transmission of Verminephrobacter symbionts in the earthworm Aporrectodea tuberculata (Lumbricidae). FEMS Microbiol Ecol 93:fix025. https://doi.org/10.1093/femsec/fix025
Peterson BF, Scharf ME (2016) Lower termite associations with microbes: synergy, protection, and interplay. Front Microbiol 7:422. https://doi.org/10.3389/fmicb.2016.00422
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rosengaus RB, Traniello JFA (1991) Biparental care in incipient colonies of the dampwood termite Zootermopsis angusticollis Hagen (Isoptera: Termopsidae). J Insect Behav 4:633–647. https://doi.org/10.1007/BF01048075
Rosengaus RB, Traniello JF (1993) Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. P Natl Acad Sci USA 90:6641–6645. https://doi.org/10.1073/pnas.90.14.6641
Rosengaus RB, Traniello JFA, Bulmer MS (2011) Ecology, behavior and evolution of disease resistance in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, The Netherlands, pp 165–191
Russell SL (2019) Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses: a systematic review and meta-analysis. FEMS Microbiol Lett 366:fnz013. https://doi.org/10.1093/femsle/fnz013
Russell SL, Chappell L, Sullivan W (2019) A symbiont’s guide to the germline. Curr Top Dev Biol 135:315–351. https://doi.org/10.1016/bs.ctdb.2019.04.007
Shellman-Reeve JS (1990) Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): response to nitrogen availability. Behav Ecol Sociobiol 26:389–397. https://doi.org/10.1007/BF00170895
Shellman-Reeve JS (1996) Operational sex ratios and lipid reserves in the dampwood termite Zootermopsis nevadensis (Hagen) (Isoptera: Termopsidae). J Kans Entomol Soc 69:139–146
Shimada K, Lo N, Kitade O, Wakui A, Maekawa K (2013) Cellulolytic protist numbers rise and fall dramatically in termite queens and kings during colony foundation. Eukaryot Cell 12:545–550. https://doi.org/10.1128/EC.00286-12
Sinotte V, Renelies-Hamilton J, Andreu-Sánchez S, Vasseur-Cognet M, Poulsen M (2022) Extensive inheritance of gut microbial communities in a superorganismal termite. Res Sq (preprint). https://doi.org/10.21203/rs.3.rs-1978279/v1
Skidmore IH, Hansen AK (2017) The evolutionary development of plant-feeding insects and their nutritional endosymbionts. Insect Sci 24:910–928. https://doi.org/10.1111/1744-7917.12463
Stoklosa AM, Ulyshen MD, Fan Z, Varner M, Seibold S, Müller J (2016) Effects of mesh bag enclosure and termites on fine woody debris decomposition in a subtropical forest. Basic Appl Ecol 17:463–470. https://doi.org/10.1016/j.baae.2016.03.001
Su N-Y, Scheffrahn RH, Weissling T (1997) A new introduction of a subterranean termite, Coptotermes havilandi Holmgren (Isoptera: Rhinotermitidae) in Miami, Florida. Fla Entomol 80:408–411
Taerum SJ, De Martini F, Liebig J, Gile GH (2018) Incomplete co-cladogenesis between Zootermopsis termites and their associated protists. Environ Entomol 47:184–195. https://doi.org/10.1093/ee/nvx193
Velenovsky IV JF, Gile GH, Su N-Y, Chouvenc T (2021) Dynamic protozoan abundance of Coptotermes kings and queens during the transition from biparental to alloparental care. Insectes Soc 68:33–40. https://doi.org/10.1007/s00040-021-00808-6
Viana F, Paz L-C, Methling K, Damgaard CF, Lalk M, Schramm A, Lund MB (2018) Distinct effects of the nephridial symbionts Verminephrobacter and Candidatus Nephrothrix on reproduction and maturation of its earthworm host Eisenia andrei. FEMS Microbiol Ecol 94:fix178. https://doi.org/10.1093/femsec/fix178
Watanabe K, Yukuhiro F, Matsuura Y, Fukatsu T, Noda H (2014) Intrasperm vertical symbiont transmission. P Natl Acad Sci USA 111:7433–7437. https://doi.org/10.1073/pnas.1402476111
Weesner FM (1960) Evolution and biology of the termites. Annu Rev Entomol 5:153–170. https://doi.org/10.1146/annurev.en.05.010160.001101
Weesner FM (1969) External anatomy. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, New York, pp 19–47
Weesner FM (1970) Termites of the nearctic region. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, New York, New York, pp 477–525
Whitford WG, Steinberger Y, Ettershank G (1982) Contributions of subterranean termites to the “economy” of Chihuahuan desert ecosystems. Oecologia 55:298–302. https://doi.org/10.1007/BF00376915
Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge, Massachusetts
Yoshimura T (1995) Contribution of the protozoan fauna to nutritional physiology of the lower termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Wood Res 82:68–129
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Velenovsky, J.F., De Martini, F., Hileman, J.T. et al. Vertical transmission of cellulolytic protists in termites is imperfect, but sufficient, due to biparental transmission. Symbiosis 90, 25–38 (2023). https://doi.org/10.1007/s13199-023-00917-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-023-00917-9