Shellman-Reeve, J. S. Courting strategies and conflicts in a monogamous, biparental termite. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 266, 137–144 (1999).
Google Scholar
Boomsma, J. J. Beyond promiscuity: mate-choice commitments in social breeding. Philos. Trans. R. Soc. B: Biol. Sci. 368 (2013).
Nichols, H. J. The causes and consequences of inbreeding avoidance and tolerance in cooperatively breeding vertebrates. J. Zool. 303, 1–14 (2017).
Google Scholar
Clutton-Brock, T. H. Female transfer and inbreeding avoidance in social mammals. Nature 337, 70–72 (1989).
Google Scholar
Wolff, J. O. Parents suppress reproduction and stimulate dispersal in opposite-sex juvenile white-footed mice. Nature 359, 409–410 (1992).
Google Scholar
Abbott, D. In Primate Social Conflict (eds W. A. Mason & S. P. Mendoza) 331–372 (State University of New York Press, 1993).
Koenig, W. D., Haydock, J. & Stanback, M. T. Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition. Am. Nat. 151, 243–255 (1998).
Google Scholar
Hanby, J. P. & Bygott, J. D. Emigration of subadult lions. Anim. Behav. 35, 161–169 (1987).
Google Scholar
Brooked, M. G., Rowley, I., Adams, M. & Baverstock, P. R. Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav. Ecol. Sociobiol. 26, 191–199 (1990).
Google Scholar
Amos, B., Schlotterer, C. & Tautz, D. Social structure of pilot whales revealed by analytical DNA proftling. Science 260, 670–672 (1993).
Google Scholar
Sillero-Zubiri, C., Gottelli, D. & Macdonald, D. W. Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav. Ecol. Sociobiol. 38, 331–340 (1996).
Google Scholar
Husseneder, C., Simms, D. M. & Ring, D. R. Genetic diversity and genotypic differentiation between the sexes in swarm aggregations decrease inbreeding in the Formosan subterranean termite. Insectes Sociaux 53, 212–219 (2006).
Google Scholar
Blouin, S. F. & Blouin, M. Inbreeding avoidance behaviors. Trends Ecol. Evol. 3, 230–233 (1988).
Google Scholar
Pusey, A. & Wolf, M. Inbreeding avoidance in animals. Trends Ecol. Evol. 11, 201–206 (1996).
Google Scholar
Gerlach, G. & Lysiak, N. Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim. Behav. 71, 1371–1377 (2006).
Google Scholar
Hurst, J. L. et al. Individual recognition in mice mediated by major urinary proteins. Nature 414, 631–634 (2001).
Google Scholar
Vargo, E. L. & Husseneder, C. In Biology of termites: A modern synthesis (eds D.E. Bignell, Yves Roisin, & Nathan Lo) 133–164 (Springer, 2011).
Shellman-Reeve, J. S. Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): response to nitrogen availability. Behav. Ecol. Sociobiol. 26, 389–397 (1990).
Google Scholar
Cole, E. L., Ilieş, I. & Rosengaus, R. B. Competing physiological demands during incipient colony foundation in a social insect: consequences of pathogenic stress. Front. Ecol. Evol. 6 (2018).
Traniello, J. F. A., Rosengaus, R. B. & Savoie, K. The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc. Natl Acad. Sci. 99, 6838–6842 (2002).
Google Scholar
Cremer, S., Armitage, S. A. O. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).
Google Scholar
Rosengaus, R. B., Traniello, J. F. A. & Bulmer, M. In biology of termites: a modern synthesis (eds D. E. Bignell, Yves Roisin & Nathan Lo) 165–191 (Springer, 2011).
Cole, E. L., Bayne, H. & Rosengaus, R. B. Young but not defenceless: antifungal activity during embryonic development of a social insect. R. Soc. Open Sci. 7, 191418–191418 (2020).
Google Scholar
Rosengaus, R. B. & Traniello, J. F. Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav. Ecol. Sociobiol. 50, 546–556 (2001).
Google Scholar
Cole, E. L. & Rosengaus, R. B. Pathogenic dynamics during colony ontogeny reinforce potential drivers of termite eusociality: mate assistance and biparental care. Front. Ecol. Evol. 7 (2019).
Chouvenc, T. The relative importance of queen and king initial weights in termite colony foundation success. Insectes Sociaux 66, 177–184 (2019).
Google Scholar
Matsuura, K. & Kobayashi, N. Termite queens adjust egg size according to colony development. Behav. Ecol. 21, 1018–1023 (2010).
Google Scholar
Calleri, D. V., McGrail Reid, E., Rosengaus, R. B., Vargo, E. L. & Traniello, J. F. A. Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc. R. Soc. B: Biol. Sci. 273, 2633–2640 (2006).
Google Scholar
DeHeer, C. J. & Vargo, E. L. An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav. Ecol. Sociobiol. 59, 753–761 (2006).
Google Scholar
Aguero, C. M., Eyer, P.-A., Martin, J. S., Bulmer, M. S. & Vargo, E. L. Natural variation in colony inbreeding does not influence susceptibility to a fungal pathogen in a termite. Ecol. Evol. 11, 3072–3083 (2021).
Google Scholar
Aguero, C., Eyer, P. A. & Vargo, E. L. Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen. Sci. Rep. 10, 4212 (2020).
Google Scholar
Rosengaus, R. B. & Traniello, J. F. Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc. Natl Acad. Sci. 90, 6641–6645 (1993).
Google Scholar
Eyer, P.-A. et al. Extensive human-mediated jump dispersal within and across the native and introduced ranges of the invasive termite Reticulitermes flavipes. Mol. Ecol. 30, 3948–3964 (2021).
Google Scholar
Perdereau, E. et al. Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol. Ecol. 22, 1105–1119 (2013).
Google Scholar
Sinotte, V. M. et al. Female-biased sex allocation and lack of inbreeding avoidance in Cubitermes termites. Ecol. Evolution 11, 5598–5605 (2021).
Google Scholar
Li, G., Gao, Y., Sun, P., Lei, C. & Huang, Q. Factors affecting mate choice in the subterranean termite Reticulitermes chinensis (Isoptera: Rhinotermitidae). J. Ethol. 31, 159–164 (2013).
Google Scholar
Aguilera-Olivares, D., Flores-Prado, L., Véliz, D. & Niemeyer, H. Mechanisms of inbreeding avoidance in the one-piece drywood termite Neotermes chilensis. Insectes Sociaux 62, 237–245 (2015).
Google Scholar
Miyaguni, Y., Agarie, A., Sugio, K., Tsuji, K. & Kobayashi, K. Caste development and sex ratio of the Ryukyu drywood termite Neotermes sugioi and its potential mechanisms. Sci. Rep. 11, 15037 (2021).
Google Scholar
Nutting, W. L. In Biology of Termites (eds Kumar Krishna & Frances M. Weesner) 233–282 (Academic Press, 1969).
Fougeyrollas, R. et al. Dispersal and mating strategies in two neotropical soil-feeding termites, Embiratermes neotenicus and Silvestritermes minutus (Termitidae, Syntermitinae). Insectes Sociaux 65, 251–262 (2018).
Google Scholar
Shellman-Reeve, J. S. Genetic relatedness and partner preference in a monogamous, wood-dwelling termite. Anim. Behav. 61, 869–876 (2001).
Google Scholar
Zhang, Z.-Y. et al. Biochemical, molecular, and morphological variations of flight muscles before and after dispersal flight in a eusocial termite, Reticulitermes chinensis. Insect Sci. 28, 77–92 (2021).
Google Scholar
Mullins, A. J. et al. Dispersal flights of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 108, 707–719 (2015).
Google Scholar
Goodisman, M. A. D. & Crozier, R. H. Population and colony genetic structure of the primitive termite Mastotermes Darwiniensis. Evolution 56, 70–83 (2002).
Google Scholar
Schmidt, A. M., Jacklyn, P. & Korb, J. Isolated in an ocean of grass: low levels of gene flow between termite subpopulations. Mol. Ecol. 22, 2096–2105 (2013).
Google Scholar
Thompson, G. J., Lenz, M., Crozier, R. H. & Crespi, B. J. Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system. Aust. J. Zool. 55, 219–227 (2007).
Google Scholar
Vargo, E. L. Diversity of termite breeding systems. Insects 10, 52 (2019).
Google Scholar
Tranter, C., LeFevre, L., Evison, S. E. F. & Hughes, W. O. H. Threat detection: contextual recognition and response to parasites by ants. Behav. Ecol. 26, 396–405 (2014).
Google Scholar
Hussain, A., Tian, M.-Y., He, Y.-R., Bland, J. M. & Gu, W.-X. Behavioral and electrophysiological responses of Coptotermes formosanus Shiraki towards entomopathogenic fungal volatiles. Biol. Control 55, 166–173 (2010).
Google Scholar
Yanagawa, A., Imai, T., Akino, T., Toh, Y. & Yoshimura, T. Olfactory cues from pathogenic fungus affect the direction of motion of termites, Coptotermes formosanus. J. Chem. Ecol. 41, 1118–1126 (2015).
Google Scholar
Rosengaus, R. B., James, L.-T., Hartke, T. R. & Brent, C. S. Mate preference and disease risk in Zootermopsis angusticollis (Isoptera: Termopsidae). Environ. Entomol. 40, 1554–1565 (2011).
Google Scholar
Beani, L. et al. Cuticular hydrocarbons as cues of sex and health condition in Polistes dominula wasps. Insectes Sociaux 66, 543–553 (2019).
Google Scholar
Waser, P. M., Austad, S. N. & Keane, B. When should animals tolerate inbreeding? Am. Nat. 128, 529–537 (1986).
Google Scholar
Bengtsson, B. O. Avoiding inbreeding: at what cost? J. Theor. Biol. 73, 439–444 (1978).
Google Scholar
Lehmann, L. & Perrin, N. Inbreeding avoidance through kin recognition: Choosy females boost male dispersal. Am. Nat. 162, 638–652 (2003).
Google Scholar
Basalingappa, S. Environmental hazards to reproductives of Odontotermes assmuthi Holgrem. Indian Zool. 1, 45–50 (1970).
Darlington, J., Sands, W. & Pomeroy, D. Distribution and post-settlement survival in the field by reproductive pairs of Hodotermes mossambicus hagen (isoptera, hodotermitida). Insectes Sociaux 24, 353–358 (1977).
Google Scholar
Dial, K. P. & Vaughan, T. A. Opportunistic predation on alate termites in Kenya. Biotropica 19, 185–187 (1987).
Google Scholar
Korb, J. & Salewski, V. Predation on swarming termites by birds. Afr. J. Ecol. 38, 173–174 (2000).
Google Scholar
Schwenke, R. A., Lazzaro, B. P. & Wolfner, M. F. ReproduCtion–immunity Trade-offs In Insects. Annu. Rev. Entomol. 61, 239–256 (2016).
Google Scholar
Calleri, D. II, Rosengaus, R. & Traniello, J. A. Disease and colony foundation in the dampwood termite Zootermopsis angusticollis: The survival advantage of nestmate pairs. Naturwissenschaften 92, 300–304 (2005).
Google Scholar
Fei, H. X. & Henderson, G. Comparative study of incipient colony development in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera,Rhinotermitidae). Insectes Sociaux 50, 226–233 (2003).
Google Scholar
Rosengaus, R. B., Cornelisse, T., Guschanski, K. & Traniello, J. F. A. Inducible immune proteins in the dampwood termite Zootermopsis angusticollis. Naturwissenschaften 94, 25–33 (2007).
Google Scholar
Rosengaus, R. B., Traniello, J. F. A., Chen, T., Brown, J. J. & Karp, R. D. Immunity in a social insect. Naturwissenschaften 86, 588–591 (1999).
Google Scholar
Sun, Q., Haynes, K. F., Hampton, J. D. & Zhou, X. Sex-specific inhibition and stimulation of worker-reproductive transition in a termite. Sci. Nat. 104, 79 (2017).
Google Scholar
Eyer, P.-A. et al. Inbreeding tolerance as a pre-adapted trait for invasion success in the invasive ant Brachyponera chinensis. Mol. Ecol. 27, 4711–4724 (2018).
Google Scholar
Barrett, S. C. H. & Charlesworth, D. Effects of a change in the level of inbreeding on the genetic load. Nature 352, 522 (1991).
Google Scholar
Crnokrak, P. & Spencer, C. H. B. Perspective: purging the genetic load. A review of the experimental evidence. Evolution 56, 2347–2358 (2002).
Google Scholar
Day, S. B., Bryant, E. H. & Meffert, L. M. The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57, 1314–1324 (2003).
Google Scholar
Syren, R. M. & Luykx, P. Permanent segmental interchange complex in the termite Incisitermes schwarzi. Nature 266, 167–168 (1977).
Google Scholar
Fontana, F. Multiple reciprocal chromosomal translocations and their role in the evolution of sociality in termites. Ethol. Ecol. Evolution 3, 15–19 (1991).
Google Scholar
Matsuura, K. A test of the haplodiploid analogy hypothesis in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 95, 646–649 (2002).
Google Scholar
Yashiro, T. et al. Enhanced heterozygosity from male meiotic chromosome chains is superseded by hybrid female asexuality in termites. Proc. Natl. Acad. Sci. 118, e2009533118 (2021).
Charlesworth, B. & Wall, J. D. Inbreeding, heterozygote advantage and the evolution of neo-X and neo-Y sex chromosomes. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 266, 51–56 (1999).
Google Scholar
Hellemans, S. et al. Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae). BMC Evol. Biol. 19, 131 (2019).
Google Scholar
Vargo, E. L., Labadie, P. E. & Matsuura, K. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc. R. Soc. B: Biol. Sci. 279, 813–819 (2012).
Google Scholar
Matsuura, K. et al. Queen succession through asexual reproduction in termites. Science 323, 1687–1687 (2009).
Google Scholar
Cremer, S., Pull, C. D. & Fürst, M. A. Social immunity: emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2018).
Google Scholar
Van Meyel, S., Körner, M. & Meunier, J. Social immunity: why we should study its nature, evolution and functions across all social systems. Curr. Opin. Insect Sci. 28, 1–7 (2018).
Google Scholar
Cotter, S. C. & Kilner, R. M. Personal immunity versus social immunity. Behav. Ecol. 21, 663–668 (2010).
Google Scholar
Liu, L., Zhao, X.-Y., Tang, Q.-B., Lei, C.-L. & Huang, Q.-Y. The mechanisms of social immunity against fungal infections in eusocial insects. Toxins 11, 244 (2019).
Google Scholar
Chouvenc, T. & Su, N. Y. When subterranean termites challenge the rules of fungal epizootics. Plos One 7, e34484 (2012).
Google Scholar
Davis, H. E., Meconcelli, S., Radek, R. & McMahon, D. P. Termites shape their collective behavioural response based on stage of infection. Sci. Rep. 8, 14433–14433 (2018).
Google Scholar
Cassidy, S. T. et al. Disease defences across levels of biological organization: individual and social immunity in acorn ants. Anim. Behav. 179, 73–81 (2021).
Google Scholar
López-Uribe, M. M., Sconiers, W. B., Frank, S. D., Dunn, R. R. & Tarpy, D. R. Reduced cellular immune response in social insect lineages. Biol. Lett. 12, 20150984 (2016).
Google Scholar
He, S. et al. Evidence for reduced immune gene diversity and activity during the evolution of termites. Proc. R. Soc. B: Biol. Sci. 288, 20203168 (2021).
Google Scholar
Viljakainen, L. et al. Rapid evolution of immune proteins in social insects. Mol. Biol. Evol. 26, 1791–1801 (2009).
Google Scholar
Meusemann, K., Korb, J., Schughart, M. & Staubach, F. No evidence for single-copy immune-gene specific signals of selection in termites. Front. Ecol. Evol. 8 (2020).
Otani, S., Bos, N. & Yek, S. H. Transitional complexity of social insect immunity. Front. Ecol. Evol. 4 (2016).
Barribeau, S. M. et al. A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biol. 16, 83 (2015).
Google Scholar
de Boer, R. A., Vega-Trejo, R., Kotrschal, A. & Fitzpatrick, J. L. Meta-analytic evidence that animals rarely avoid inbreeding. Nat. Ecol. Evol. 5, 949–964 (2021).
Google Scholar
Szulkin, M., Stopher, K. V., Pemberton, J. M. & Reid, J. M. Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol. Evol. 28, 205–211 (2013).
Google Scholar
Fox, C. W. & Reed, D. H. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evol. 65, 246–258 (2011).
Google Scholar
Kokko, H., Ots, I. & Tregenza, T. When not to avoid inbreeding. Evolution 60, 467–475 (2006).
Google Scholar
Zayed, A. & Packer, L. Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc. Natl Acad. Sci. USA 102, 10742–10746 (2005).
Google Scholar
Ross, K. G. & Fletcher, D. J. C. Diploid male production — a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 19, 283–291 (1986).
Google Scholar
Eyer, P.-A., Salin, J., Helms, A. M. & Vargo, E. L. Distinct chemical blends produced by different reproductive castes in the subterranean termite Reticulitermes flavipes. Sci. Rep. 11, 4471 (2021).
Google Scholar
Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
Google Scholar
Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).
Google Scholar
Wang, J. Coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 11, 141–145 (2011).
Google Scholar
Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
Google Scholar
Rosengaus, R. B., Moustakas, J. E., Calleri, D. V. & Traniello, J. F. A. Nesting ecology and cuticular microbial loads in dampwood (Zootermopsis angusticollis) and drywood termites (Incisitermes minor, I. schwarzi, Cryptotermes cavifrons). J. Insect Sci. 3, 31 (2003).
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. 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 (2013).
Google Scholar
White, T. J., Burns, T., Lee, S. & Taylor, J. in PCR protocols: A guide to methods and applications (eds. M. A. Innis, D. H. Gelfand, J. J. Snisky, & T. J. White) 315–322 (Academic Press, 1990).
Aguero, C. M., Eyer, P.-A., Crippen, T. L. & Vargo, E. L. Reduced environmental microbial diversity on the cuticle and in the galleries of a subterranean termite compared to surrounding soil. Microb. Ecol. 81, 1054–1063 (2021).
Google Scholar
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).
Google Scholar
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
Google Scholar
Hamady, M., Lozupone, C. & Knight, R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4, 17–27 (2010).
Google Scholar
Therneau, T. & Grambsch, P. Modeling Survival Data: Extending the Cox Model (Springer, 2000).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Google Scholar
