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Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite

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Abstract

Some species of termites evolved an outstanding reproductive strategy called asexual queen succession (AQS), in which the primary queen is replaced by multiple parthenogenetically produced daughters (neotenics) that mate with the primary king. When the primary king is eventually replaced, this time by sexually produced neotenic king(s), sex-asymmetric inbreeding occurs and the queen’s genome is more transmitted than that of the king, thereby increasing the reproductive value of female dispersers, and female-biased population sex ratio is expected. Yet, the life cycle, the breeding system dynamics and AQS modalities differ between AQS species, thereby modifying the relative genetic contribution of primary reproductives in the colony and thus also the equilibrium sex ratio. We estimated colonial and population sex ratio over two consecutive dispersal periods in a French Guiana population of Cavitermes tuberosus (Termitinae) in which the founding queen may be replaced only after colony maturity, some neotenic females may be sexually produced, and some female dispersers arise through parthenogenesis. Colonial sex ratio varied among colonies: primary-headed nests with higher within-nest relatedness produced more females than neotenic-headed nests with lower relatedness among individuals. Over the two dispersal periods, the population investment sex ratio fluctuated around 1:1, thereby confirming that AQS breeding system is not necessarily linked with female-biased sex ratio. The balanced alate sex ratio, combined with the occurrence of sexually produced neotenic queens, is possibly the outcome of a queen-king conflict between the primary reproductives.

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References

  • Aron S (2012) Primary sex ratio regulation by queens in ants (Formicidae) and other social Hymenoptera. Myrmecological News 17:63–80

    Google Scholar 

  • Boomsma JJ (1996) Split sex ratios and queen-male conflict over sperm allocation. Proc R Soc B 263:697–704

    Article  Google Scholar 

  • Boomsma JJ, Grafen A (1991) Colony-level sex ratio selection in the eusocial Hymenoptera. J Evol Biol 4:383–407

    Article  Google Scholar 

  • Boomsma JJ, Grafen A (1990) Intraspecific variation in ant sex ratios and the Trivers-Hare hypothesis. Evolution 44:1026–1034

    Article  PubMed  CAS  Google Scholar 

  • Boomsma JJ, Nachman G (2002) Analysis of sex ratios in social insects. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 93–111

    Chapter  Google Scholar 

  • Bourguignon T, Šobotník J, Lepoint G, Martin JM, Hardy OJ, Dejean A, Roisin Y (2011) Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios. Ecol Entomol 36:261–269

    Article  Google Scholar 

  • Bourke AFG (2015) Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory. J Evol Biol 28:2106–2111

    Article  PubMed  CAS  Google Scholar 

  • Bourke AFG (2005) Genetics, relatedness and social behaviour in insect societies. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI Publishing, Wallingford, pp 1–30

    Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Monographs in behavior and ecology. Princeton University Press, Princeton

    Google Scholar 

  • Brown WD, Keller L (2000) Colony sex ratios vary with queen number but not relatedness asymmetry in the ant Formica exsecta. Proc R Soc B 267:1751–1757

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Springer-Verlag, New York

    Google Scholar 

  • Buxton RD (1981) Changes in the composition and activities of termite communities in relation to changing rainfall. Oecologia 51:371–378

    Article  PubMed  CAS  Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, New York

    Google Scholar 

  • DeHeer CJ, Vargo EL (2006) An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav Ecol Sociobiol 59:753–761

    Article  Google Scholar 

  • Deslippe RJ, Savolainen R (1995) Sex investment in a social insect: the proximate role of food. Ecology 76:375–382

    Article  Google Scholar 

  • 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, pp 1–26

    Google Scholar 

  • Emerson AE (1925) The termites of Kartabo, Bartica District, British Guiana. Zoologica 6:291–459

    Google Scholar 

  • Fougeyrollas R, Dolejšová K, Sillam-Dussès D, Roy V, Hanus R, Roisin Y (2015) Asexual queen succession in the higher termite Embiratermes neotenicus. Proc R Soc B 282:20150260

    Article  PubMed  Google Scholar 

  • Fougeyrollas R, Křivánek J, Roy V, Dolejšová K, Frechault S, Roisin Y, Hanus R, Sillam-Dussès D (2017) Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus. Mol Ecol 26:3295–3308

    Article  PubMed  CAS  Google Scholar 

  • Fournier D, Hanus R, Roisin Y (2015) Development and characterization of microsatellite markers from the humivorous termite Cavitermes tuberosus (Isoptera: Termitinae) using pyrosequencing technology. Conserv Genet Resour 7:521–524

    Article  Google Scholar 

  • Fournier D, Hellemans S, Hanus R, Roisin Y (2016) Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proc R Soc B 283:20160196

    Article  PubMed  CAS  Google Scholar 

  • Fournier D, Keller L, Passera L, Aron S (2003) Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula. Evolution 57:1336–1342

    Article  PubMed  Google Scholar 

  • Goodnight KF, Queller DC (2000) Relatedness 5.0.8. Goodnight Software, Houston

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. I, II. J Theor Biol 7:1–52

    Article  PubMed  CAS  Google Scholar 

  • Hellemans S, Bourguignon T, Kyjaková P, Hanus R, Roisin Y (2017a) Mitochondrial and chemical profiles reveal a new genus and species of Neotropical termite with snapping soldiers, Palmitermes impostor (Termitidae: Termitinae). Invertebr Syst 31:394–405. https://doi.org/10.1071/IS16089

    Article  CAS  Google Scholar 

  • Hellemans S, Fournier D, Hanus R, Roisin Y (2017b) Secondary queens in the parthenogenetic termite Cavitermes tuberosus develop through a transitional helper stage. Evol Dev 19:253–262

    Article  PubMed  Google Scholar 

  • Hellemans S, Fournier D, Hanus R, Roisin Y (2016) Investigating key traits for AQS emergence in Termitinae. In: Proceedings of the 6th European meeting of the international union for the study of social insects. Helsinki, Finland

  • Helms KR, Fournier D, Keller L, Passera L, Aron S (2004) Colony sex ratios in the facultatively polygynous ant Pheidole pallidula: a reanalysis with new data. Evolution 58:1141–1142

    Article  PubMed  Google Scholar 

  • Herfs A (1951) Der Schwarmflug von Reticulitermes lucifugus Rossi. Zeitschrift fuer Angew Entomol 33:69–77

    Article  Google Scholar 

  • Howard KJ, Thorne BL (2011) Eusocial evolution in termites and hymenoptera. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 97–132

    Google Scholar 

  • Jiménez-Muñoz JC, Mattar C, Barichivich J, Santamaría-Artigas A, Takahashi K, Malhi Y, Sobrino JA, van der Schrier G (2016) Record-breaking warming and extreme drought in the Amazon rainforest during the course of El Niño 2015–2016. Sci Rep 6:33130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones SC, La Fage JP, Howard RW (1988) Isopteran sex ratios: phylogenetic trends. Sociobiology 14:89–156

    Google Scholar 

  • Josens G (1982) Le bilan énergétique de Trinervitermes geminatus Wasmann (Termitidae, Nasutitermitinae). I. Mesures de biomasses, d’équivalents énergétiques, de longévité et de production en laboratoire. Insectes Soc 29:297–307

    Google Scholar 

  • Kawatsu K (2013) Sexual conflict over the maintenance of sex: effects of sexually antagonistic coevolution for reproductive isolation of parthenogenesis. PLoS One 8:e58141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kobayashi K, Hasegawa E, Yamamoto Y, Kawatsu K, Vargo EL, Yoshimura J, Matsuura K (2013) Sex ratio biases in termites provide evidence for kin selection. Nat Commun 4:2048

    Article  PubMed  CAS  Google Scholar 

  • Krishna K, Grimaldi DA, Krishna V, Engel MS (2013a) Treatise on the Isoptera of the World. 6. Termitidae (Part Three), Incertae sedis, taxa excluded from Isoptera. Bull Am Museum Nat Hist 377:1989–2432

    Article  Google Scholar 

  • Krishna K, Grimaldi DA, Krishna V, Engel MS (2013b) Treatise on the Isoptera of the World. 1. Introduction. Bull Am Museum Nat Hist 377:1–200

    Article  Google Scholar 

  • Kümmerli R, Keller L (2011) Between-year variation in population sex ratio increases with complexity of the breeding system in Hymenoptera. Am Nat 177:835–846

    Article  PubMed  Google Scholar 

  • Lacy RC (1980) The evolution of eusociality in termites: a haplodiploid analogy? Am Nat 116:449–451

    Article  Google Scholar 

  • Lenz M, Runko S (1993) Long-term impact of orphaning on field colonies of Coptotermes lacteus (Froggatt) (Isoptera: Rhinotermitidae). Insectes Soc 40:439–456

    Article  Google Scholar 

  • Luchetti A, Velonà A, Mueller M, Mantovani B (2013) Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae). Insectes Soc 60:203–211

    Article  Google Scholar 

  • Mathews AGA (1977) Studies on Termites from the Mato Grosso State, Brazil. Academia Brasileira de Ciências, Rio de Janeiro

    Google Scholar 

  • Matsuura K (2011) Sexual and asexual reproduction in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 255–277

    Google Scholar 

  • Matsuura K (2017) Evolution of asexual queen succession system and its underlying mechanisms in termites. J Exp Biol 220:63–72

    Article  PubMed  Google Scholar 

  • Matsuura K, Vargo EL, Kawatsu K, Labadie PE, Nakano H, Yashiro T, Tsuji K (2009) Queen succession through asexual reproduction in termites. Science 323:1687

    Article  PubMed  CAS  Google Scholar 

  • Matsuura K, Mizumoto N, Kobayashi K, Nozaki T, Fujita T, Yashiro T, Fuchikawa T, Mitaka Y, Vargo EL (2018) A genomic imprinting model of termite caste determination: not genetic but epigenetic inheritance influences offspring caste fate. Am Nat 191:677–690

    Article  PubMed  Google Scholar 

  • McMahan EA, Sen-Sarma PK, Kumar S (1983) Biometric, polyethism, and sex ratio studies of Nasutitermes dunensis Chatterjee and Thakur (Isoptera: Termitidae). Ann Entomol 1:15–25

    Google Scholar 

  • Myles TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–91

    Google Scholar 

  • Nielsen MG, Josens G (1978) Production by ants and termites. In: Brian MV (eds) Production ecology of ants and termites. Cambridge University Press, Cambridge, pp 45–53

    Google Scholar 

  • Noirot C (1955) Recherches sur le polymorphisme des termites supérieurs. Ann des Sci Nat Zool (11ème série) 27:399–595

    Google Scholar 

  • Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New-York, pp 233–282

    Chapter  Google Scholar 

  • Peakall R, Smouse PE (2012) GenALEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing, Vienna, Austria

  • Roisin Y (2001) Caste sex ratios, sex linkage, and reproductive strategies in termites. Insectes Soc 48:224–230

    Article  Google Scholar 

  • Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 95–119

    Chapter  Google Scholar 

  • Roisin Y, Korb J (2011) Social organisation and the status of workers in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 133–164

    Google Scholar 

  • Roisin Y, Lenz M (2002) Origin of male-biased sex allocation in orphaned colonies of the termite, Coptotermes lacteus. Behav Ecol Sociobiol 51:472–479

    Article  Google Scholar 

  • Roonwal ML (1975) Sex ratios and sexual dimorphism in termites. J Sci Ind Res (India) 34:402–416

    Google Scholar 

  • Sands WA (1965) A late development and colony foundation in five species of Trinervitermes (Isoptera, Nasutitermitinae) in Nigeria, West Africa. Insectes Soc 12:117–130

    Article  Google Scholar 

  • Sulca J, Takahashi K, Espinoza JC et al (2018) Impacts of different ENSO flavors and tropical Pacific convection variability (ITCZ, SPCZ) on austral summer rainfall in South America, with a focus on Peru. Int J Climatol 38:420–435

    Article  Google Scholar 

  • Thorne BL (1983) Alate production and sex ratio in colonies of the Neotropical termite Nasutitermes corniger (Isoptera; Termitidae). Oecologia 58:103–109

    Article  PubMed  Google Scholar 

  • Trivers R, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263

    Article  PubMed  CAS  Google Scholar 

  • Trivers R, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    Article  PubMed  CAS  Google Scholar 

  • Tsuji K (1996) Queen-male conflict over sperm use in social insects. Trends Ecol Evol 11:490–491

    Article  PubMed  CAS  Google Scholar 

  • Vanthournout B, Busck MM, Bechsgaard J, Hendrickx F, Schramm A, Bilde T (2018) Male spiders control offspring sex ratio through greater production of female-determining sperm. Proc R Soc B 285:20172887

    Article  PubMed  CAS  Google Scholar 

  • Vargo EL, Labadie PE, Matsuura K (2012) Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc R Soc B Biol Sci 279:813–819

    Article  Google Scholar 

  • Vincke PP, Tilquin JP (1978) A sex-linked ring quadrivalent in Termitidae (Isoptera). Chromosoma 67:151–156

    Article  Google Scholar 

  • Wild G, Taylor PD (2005) A kin-selection approach to the resolution of sex-ratio conflict between mates. J Theor Biol 236:126–136

    Article  PubMed  Google Scholar 

  • Yanega D (1993) Environmental influences on male production and social structure in Halictus rubicundus (Hymenoptera: Halictidae). Insectes Soc 40:169–180

    Article  Google Scholar 

  • Yashiro T, Matsuura K (2014) Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction. Proc Natl Acad Sci USA 111:17212–17217

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to Philippe Cerdan, Régis Vigouroux, and the staff of the Laboratoire Environnement HYDRECO of Petit Saut (EDF-CNEH) for logistic support during the field work.

Funding

This work was supported by a PhD fellowship (SH) and grants from the Belgian National Fund for Scientific Research F.R.S.-FNRS (DF and YR: FRFC grant nos. 2.4594.12; DF: J.0110.17), the Research Mobility Project between the Belgian National Fund for Scientific Research FRS-FNRS and the Czech Academy of Sciences (RH and YR: FNRS-17-02) and the project RVO 61388963 (RH, IOCB, Prague).

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Authors and Affiliations

  1. Evolutionary Biology and Ecology, Université libre de Bruxelles, Avenue F.D. Roosevelt 50, CP 160/12, 1050, Brussels, Belgium

    S. Hellemans, D. Fournier & Y. Roisin

  2. Chemistry of Social Insects, Institute of Organic Chemistry and Biochemistry, Czech Academy of Sciences, Flemingovo n. 2, 166 10, Prague 6, Czech Republic

    R. Hanus

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  1. S. Hellemans
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  2. D. Fournier
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Contributions

SH, DF and YR designed the study. SH, RH and YR collected the material. SH performed the molecular laboratory work and genetic analyses. SH, DF and YR carried out the statistical analyses. All authors contributed significantly to the manuscript and approved the final version.

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Correspondence to S. Hellemans.

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Data Archiving

The full dataset of genotypes used is available in the Dryad Data Repository (https://doi.org/10.5061/dryad.01c53v5).

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We dedicate this work to the memory of Philippe Cerdan (1959–2018), co-director of HYDRECO laboratory of Petit Saut in French Guiana.

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Hellemans, S., Fournier, D., Hanus, R. et al. Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite. Insect. Soc. 66, 129–138 (2019). https://doi.org/10.1007/s00040-018-0667-y

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