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Fertile diploid males in the ant Cataglyphis cursor: a potential cost of thelytoky?

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Abstract

Under the hymenopteran single-locus complementary sex-determination system, production of diploid males results from homozygosity at the sex-determiner locus. This arises when both parents transmit identical alleles at the locus to the offspring. In species reproducing asexually through thelytokous parthenogenesis, production of diploid males may also occur when the sex locus undergoes recombination and becomes homozygous in the offspring. Diploid males represent a substantial genetic load in hymenopteran populations because they often produce unviable sperm or sire sterile triploid female offspring. In the Mediterranean ant Cataglyphis cursor, the queen and workers can produce female offspring through automictic thelytokous parthenogenesis with central fusion, a mode of parthenogenesis that increases homozygosity. We report, for the first time, the presence of about 39 % of colonies producing adult diploid males (seven colonies out of 18). Overall, 8 % of adult males were diploid (12 diploid males out of the 146 males genotyped). Genotyping workers from the seven colonies producing diploid males showed that three diploid males were sons of queens and produced by thelytoky, six were probably sons of workers also produced by thelytoky and three were non-natal. Furthermore, the mating of a diploid male with two virgin queens in the laboratory led to the production of sterile triploid workers, which shows that diploid males in C. cursor are fertile, mate successfully and produce viable and functional but probably sterile female offspring. Because diploid males originate from thelytokous reproduction, they are only produced during sexual production and hence do not impair colony growth, which could explain why they are not removed at early brood stages.

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References

  • Aron S, De Menten L, Van Bockstaele D (2003) Brood sex ratio determination by flow cytometry in ants. Mol Ecol Notes 3:471–475

    Article  CAS  Google Scholar 

  • Aron S, Timmermans I, Pearcy M (2011) Ant queens adjust egg fertilization to benefit from both sexual and asexual reproduction. Biol Letters 7:571–573

    Article  CAS  Google Scholar 

  • Asplen MK, Whitfield JB, de Boer JG, Heimpel GE (2009) Ancestral state reconstruction analysis of hymenopteran sex determination mechanisms. J Evol Biol 22:1762–1769

    Article  PubMed  CAS  Google Scholar 

  • Baudry E, Kryger P, Allsopp M, Koeniger N, Vautrin D, Mougel F, Cornuet J-M, Solignac M (2004) Whole-genome scan in thelytokous-laying workers of the Cape Honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167:243–252

    Article  PubMed  CAS  Google Scholar 

  • Beekman M, Allsopp MH, Jordan LA, Lim J, Oldroyd BP (2009) A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis. Mol Ecol 18:2722–2727

    Article  PubMed  Google Scholar 

  • Cagniant H (1979) La parthénogenese thélytoque et arrhénotoque chez la fourmi Cataglyphis cursor Fonsc. (Hym., Form.). Cycle biologique en élevage des colonies avec reine et des colonies sans reine. Insect Soc 26:51–60

    Article  Google Scholar 

  • Charlesworth D, Willis JH (2009) Fundamental concepts in genetics. The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  PubMed  CAS  Google Scholar 

  • Chéron B, Cronin AL, Doums C, Federici P, Haussy C, Tirard C, Monnin T (2011a) Unequal resource allocation among colonies produced by fission in the ant Cataglyphis cursor. Ecology 92:1448–1458

    Article  PubMed  Google Scholar 

  • Chéron B, Monnin T, Federici P, Doums C (2011b) Variation in patriline reproductive success during queen production in orphaned colonies of the thelytokous ant Cataglyphis cursor. Mol Ecol 20:2011–2022

    Article  PubMed  Google Scholar 

  • Clémencet J, Viginier B, Doums C (2005) Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers. Mol Ecol 14:3735–3744

    Article  PubMed  Google Scholar 

  • Cook J, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286

    Article  PubMed  CAS  Google Scholar 

  • Cournault L, Aron S (2008) Rapid determination of sperm number in ant queens by flow cytometry. Insect Soc 55:283–287

    Article  Google Scholar 

  • Cournault L, Aron S (2009) Diploid males, diploid sperm production, and triploid females in the ant Tapinoma erraticum. Naturwissenschaften 96:1393–1400

    Article  PubMed  CAS  Google Scholar 

  • Cronin AL, Monnin T, Haussy C, Doums C (2011) Opportunities for mate choice in the fission-performing ant Cataglyphis cursor. Ecol Entomol 36:522–525

    Article  Google Scholar 

  • Cronin AL, Molet M, Doums C, Monnin T, Peeters C (2013) Recurrent evolution of dependent colony foundation across eusocial insects. Annu Rev Entomol 58:37–55

    Google Scholar 

  • Crozier RH, Fjerdingstad EJ (2001) Polyandry in social Hymenoptera: disunity in diversity. Ann Zool Fenn 38:267–285

    Google Scholar 

  • Darvill B, Lepairs O, Woodall LC, Goulson D (2012) Triploid bumblebees indicate a direct cost of inbreeding in fragmented populations. Mol Ecol 21:3988–3995

    Article  PubMed  CAS  Google Scholar 

  • Doums C, Cronin AL, Ruel C, Fédérici P, Haussy C, Tirard C, Monnin T (2013) Facultative use of thelytokous parthenogenesis for queen production in the polyandrous ant Cataglyphis cursor. J Evol Biol 26:1431–1444

    Google Scholar 

  • Engelstadter J (2008) Constraints on the evolution of asexual reproduction. BioEssays 30:1138–1150

    Article  PubMed  CAS  Google Scholar 

  • Fournier D, Bataille G, Timmermans I, Aron S (2008) Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim Behav 75:151–158

    Article  Google Scholar 

  • Goudie F, Allsopp MH, Beekman M, Oxley PR, Lim J, Oldroyd BP (2012) Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis Mellifera Capensis). Evolution 66:1897–1906

    Article  PubMed  Google Scholar 

  • Harpur BA, Sobhani M, Zaed A (2013) A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. Entomol Exp Appl 146:156–164

    Article  Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230

    Article  PubMed  CAS  Google Scholar 

  • Kellner K, Heinze J (2011) Mechanism of facultative parthenogenesis in the ant Platythyrea punctata. Evol Ecol 25:77–89

    Article  Google Scholar 

  • Krieger MJB, Ross KG, Chang CWY, Keller L (1999) Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity 82:142–150

    Article  Google Scholar 

  • Lenoir A, Quérard L, Pondicq N, Berton F (1988) Reproduction and dispersal in the ant Cataglyphis cursor (Hymenoptera, Formicidae). Psyche 95:21–44

    Article  Google Scholar 

  • Liebert AE, Sumana A, Starks PT (2005) Diploid males and their triploid offspring in the paper wasp Polistes dominulus. Biol Letters 1:200–203

    Article  Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560

    Article  PubMed  CAS  Google Scholar 

  • Nanork P, Chapman NC, Wongsiri S, Lim J, Gloag RS, Oldroyd BP (2007) Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol Ecol 16:1107–1114

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164

    Article  PubMed  Google Scholar 

  • Pamilo P, Sundstrom L, Forteluis W, Rosengren R (1994) Diploid males and colony level selection in Formica ants. Ethol Ecol Evol 6:221–235

    Article  Google Scholar 

  • Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:1780–1783

    Article  PubMed  CAS  Google Scholar 

  • Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382

    Article  PubMed  CAS  Google Scholar 

  • Pearcy M, Timmermans I, Allard D, Aron S (2009) Multiple mating in the ant Cataglyphis cursor: testing the sperm limitation and the diploid male load hypotheses. Insect Soc 56:94–102

    Article  Google Scholar 

  • Pearcy M, Hardy O, Aron S (2011) Automictic parthenogenesis and rate of transition to homozygosity. Heredity 107:187–188

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rabeling C, Kronauer DJ (2013) Thelytokous parthenogenesis in eusocial Hymenoptera. Annu Rev Entomol 58:273–292

    Article  PubMed  CAS  Google Scholar 

  • Rey O, Loiseau A, Facon B, Foucaud J, Orivel J, Cornuet JM, Robert S, Dobigny G, Delabie JHC, Mariano CDF, Estoup A (2011) Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers. Mol Biol Evol 28:2591–2601

    Article  PubMed  CAS  Google Scholar 

  • Ross KG, Fletcher DJC (1986) Diploid male production—a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera, Formicidae). Behav Ecol Sociobiol 19:283–291

    Article  Google Scholar 

  • Santomauro G, Oldham NJ, Boland W, Engels W (2004) Cannibalism of diploid drone larvae in the honey bee (Apis mellifera) is released by odd pattern of cuticular substances. J Apicult Res 43:69–74

    Google Scholar 

  • Schmeider S, Colinet D, Poirié M (2012) Tracking back the nascence of a new sex determination pathway to the ancestor of bees and ants. Nature Comm 3:895

    Article  Google Scholar 

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC, Boca Raton

    Google Scholar 

  • Takahashi J, Ayabe T, Mitsuhata M, Shimizu I, Ono M (2008) Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae). Insect Soc 55:43–50

    Article  Google Scholar 

  • van Wilgenburg E, Driessen G, Beukeboom L (2006) Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? Front Zool 3:1–15

    Article  PubMed  Google Scholar 

  • Verma S, Ruttner F (1983) Cytological analysis of thelytokous parthenogenesis in the Cape honey bee Apis mellifera capensis. Apidologie 14:41–57

    Article  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163–E179

    Article  PubMed  Google Scholar 

  • Wenseleers T, Van Oystaeyen A (2011) Unusual modes of reproduction in social insects: shedding light on the evolutionary paradox of sex. BioEssays 33:927–937

    Article  PubMed  Google Scholar 

  • Whitehorn PR, Tinsley MC, Brown MJF, Darvill B, Goulson D (2009) Impacts of inbreeding on bumblebee colony fitness under field conditions. BMC Evol, Biol, 9

    Google Scholar 

  • Woyke J (1963) What happens to diploid drone larvae in a honeybee colony? J Apicult Res 2:73–75

    Google Scholar 

  • Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci U S A 102:10742–10746

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank T. Monnin, A. Cronin, B. Gassner and two anonymous referees for their insightful comments and English improvement of the manuscript. We are grateful to the Coast Conservation Office (“Conservatoire du littoral”) for allowing the collection of colonies in a protected bird nesting area. Part of this work was funded by ANR (Agence Nationale pour la Recherche) ANR-06-BLAN-0268 to C. Doums and P. Fédérici. SA thanks the Belgian FRS-FNRS for its financial support.

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The authors declare that they have no conflicts of interest.

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We declare that our study complies with the current laws in France.

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Correspondence to Claudie Doums.

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Communicated by M. Beekman

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Doums, C., Ruel, C., Clémencet, J. et al. Fertile diploid males in the ant Cataglyphis cursor: a potential cost of thelytoky?. Behav Ecol Sociobiol 67, 1983–1993 (2013). https://doi.org/10.1007/s00265-013-1606-6

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