Abstract
Mating induces a range of physiological changes in female insects. In species that mate during several reproductive bouts throughout their life, mating causes an increase in oviposition, affects immune function, and decreases female lifespan and receptivity to further mating. Social Hymenoptera (ants, social bees, and wasps) are unique, since queens mate during a single reproductive effort at the beginning of their life. Their reproductive strategy is thus fundamentally different from that of other insects and one might expect the effects of mating on social Hymenoptera queens to be altered. We tested the effect of mating and multiple mating on the expression of six genes likely to be involved in post-mating changes, in queens of the ant Lasius niger L. We show that mating induces oviposition, and is followed by an up-regulation of vitellogenin and defensin expression. The expression of juvenile hormone esterase, insulin receptor 2, Cu−Zn superoxide dismutase 1, and prophenoloxidase is not significantly affected by mating. Queen-mating frequency did not affect the expression of the tested genes. Altogether, our results indicate that certain effects of mating on female insect physiology are generalized across species independent of their mating strategies, while others seem species specific.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360
Baer B (2011) The copulation biology of ants (Hymenoptera: formicidae). Mymecol News 14:55–68
Baer B, Armitage SAO, Boomsma JJ (2006) Sperm storage induces an immunity cost in ants. Nature 441:872–875. https://doi.org/10.1038/nature04698
Borovsky D, Carlson DA, Hancock RG, Rembold H, Van Handel E (1994) De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochem Mol Biol 24:437–444. https://doi.org/10.1016/0965-1748(94)90038-8
Broughton SJ, Piper MDW, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, Partridge L (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila; from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102:3105–3110. https://doi.org/10.1073/pnas.0405775102
Bulet P, Stocklin R (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept Lett 12:3–11. https://doi.org/10.2174/0929866053406011
Castella G, Christe P, Chapuisat M (2009) Mating triggers dynamic immune regulations in wood ant queens. J Evol Biol 22:564–570. https://doi.org/10.1111/j.1420-9101.2008.01664.x
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47. https://doi.org/10.1016/S0169-5347(02)00004-6
Chapuisat M (1998) Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. Mol Ecol 7:1097–1105. https://doi.org/10.1046/j.1365-294x.1998.00422.x
Chérasse S, Aron S (2017) Measuring inotocin receptor gene expression in chronological order in ant queens. Horm Behav 96:116–121. https://doi.org/10.1016/j.yhbeh.2017.09.009
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA et al (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 104:7128–7133. https://doi.org/10.1073/pnas.0701909104
Cusson M, Delisle J (1996) Effect of mating on plasma juvenile hormone esterase activity in females of Choristoneura fumiferana and C. rosaceana. Arch Insect Biochem Physiol 32:585–599. https://doi.org/10.1002/(SICI)1520-6327(1996)32:3/4%3c585:AID-ARCH30%3e3.0.CO;2-6
Dávila F, Chérasse S, Boomsma JJ, Aron S (2015) Ant sperm storage organs do not have phenoloxidase constitutive immune activity. J Insect Physiol 78:9–14. https://doi.org/10.1016/j.jinsphys.2015.04.005
Dávila F, Botteaux A, Bauman D, Chérasse S, Aron S (2018) Antibacterial activity of male and female sperm-storage organs in ants. J Exp Biol 221:jeb175158. https://doi.org/10.1242/jeb.175158
den Boer SPA, Baer B, Dreier S, Aron S, Nash DR, Boomsma JJ (2009) Prudent sperm use by leaf-cutter ant queens. Proc R Soc Lond B Biol Sci 276:3945–3953. https://doi.org/10.1098/rspb.2009.1184
Engelmann F (1979) Insect vitellogenin: identification, biosynthesis, and role in vitellogenesis. Adv Insect Phys 14:49–108. https://doi.org/10.1016/S0065-2806(08)60051-X
Fan Y, Rafaeli A, Gileadi C, Kubli E, Applebaum SW (1999) Drosophila melanogaster sex peptide stimulates juvenile hormone synthesis and depresses sex pheromone production in Helicoverpa armigera. J Insect Physiol 45:127–133. https://doi.org/10.1016/S0022-1910(98)00106-1
Fan Y, Rafaeli A, Moshitzky P, Kubli E, Choffat Y, Applebaum SW (2000) Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females. Insect Biochem Mol Biol 30:805–812. https://doi.org/10.1016/S0965-1748(00)00052-7
Fedorka KM, Zuk M, Mousseau TA (2004) Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58:2478–2485. https://doi.org/10.1111/j.0014-3820.2004.tb00877.x
Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197. https://doi.org/10.1002/arch.940290208
Finch CE, Ruvkun G (2001) The genetics of aging. Annu Rev Genomics Hum Genet 2:435–462. https://doi.org/10.1146/annurev.genom.2.1.435
Fjerdingstad EJ, Gertsch PJ, Keller L (2002) Why do some social insect queens mate with several males? Testing the sex-ratio manipulation hypothesis in Lasius niger. Evolution 56:553–562. https://doi.org/10.1111/j.0014-3820.2002.tb01366.x
Fjerdingstad EJ, Gertsch PJ, Keller L (2003) The relationship between multiple mating by queens, within colony genetic variability and fitness in the ant Lasius niger. J Evol Biol 16:844–853. https://doi.org/10.1046/j.1420-9101.2003.00589.x
Flatt T, Tu M-P, Tatar M (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 27:999–1010. https://doi.org/10.1002/bies.20290
Gilbert LI, Granger NA, Roe RM (2000) The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem Mol Biol 30:617–644. https://doi.org/10.1016/S0965-1748(00)00034-5
Hartfelder K (2000) Insect juvenile hormone: from “status quo” to high society. Braz J Med Biol Res 33:157–177. https://doi.org/10.1590/S0100-879X2000000200003
Hoffmann JA, Hetru C (1992) Insect defensins: inducible antibacterial peptides. Immunol Today 13:411–415. https://doi.org/10.1016/0167-5699(92)90092-L
Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:958–960. https://doi.org/10.1038/40130
Kocher SD, Richard F-J, Tarpy DR, Grozinger CM (2008) Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9:232. https://doi.org/10.1186/1471-2164-9-232
Kocher SD, Tarpy DR, Grozinger CM (2010) The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression. Insect Mol Biol 19:153–162. https://doi.org/10.1111/j.1365-2583.2009.00965.x
Lawniczak MKN, Begun DJ (2004) A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47:900–910. https://doi.org/10.1139/G04-050
Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T (2007) Mating and immunity in invertebrates. Trends Ecol Evol 22:48–55. https://doi.org/10.1016/j.tree.2006.09.012
Manfredini F, Brown MJ, Vergoz V, Oldroyd BP (2015) RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens. BMC genomics 16:563. https://doi.org/10.1186/s12864-015-1750-7
McGraw LA, Gibson G, Clark AG, Wolfner MF (2004) Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr Biol 14:1509–1514. https://doi.org/10.1016/j.cub.2004.08.028
Moshitzky P, Fleischmann I, Chaimov N, Saudan P, Klauser S, Kubli E et al (1996) Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch Insect Biochem Physiol 32:363–374. https://doi.org/10.1002/(SICI)1520-6327(1996)32:3/4%3c363:AID-ARCH9%3e3.0.CO;2-T
Nakhleh J, El Moussawi L, Osta MA (2017) The melanization response in insect immunity. Adv In Insect Phys 52:83–109. https://doi.org/10.1016/bs.aiip.2016.11.002
Niño EL, Tarpy DR, Grozinger CM (2013) Honey bee queen post-mating changes. Insect Mol Biol 22:233–244. https://doi.org/10.1111/imb.12016
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rolff J, Siva-Jothy MT (2002) Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc Natl Acad Sci USA 99:9916–9918. https://doi.org/10.1073/pnas.152271999
Schmittgen TD, Zakrajsek BA (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46:69–81. https://doi.org/10.1016/S0165-022X(00)00129-9
Schrempf A, Heinze J, Cremer S (2005) Sexual cooperation: mating increases longevity in ant queens. Curr Biol 15:267–270. https://doi.org/10.1016/j.cub.2005.01.036
Seehuus S-C, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 103:962–967. https://doi.org/10.1073/pnas.0502681103
Shirk PD, Bhaskaran G, Röller H (1980) The transfer of juvenile hormone from male to female during mating in the Cecropia silkmoth. Experientia 36:682–683. https://doi.org/10.1007/BF01970138
Shirk PD, Bhaskaran G, Röller H (1983) Developmental physiology of corpora allata and accessory sex glands in the Cecropia silkmoth. J Exp Zool 227:69–79. https://doi.org/10.1002/jez.1402270111
Siva-Jothy MT, Tsubaki Y, Hooper RE (1998) Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiol Entomol 23:274–277. https://doi.org/10.1046/j.1365-3032.1998.233090.x
Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol A 130:191–199. https://doi.org/10.1007/BF00614605
Tatar M, Kopelman A, Epstein D, Tu M-P, Yin C-M, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–110. https://doi.org/10.1126/science.1057987
Tian H, Bradleigh Vinson S, Coates CJ (2004) Differential gene expression between alate and dealate queens in the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: formicidae). Insect Biochem Mol Biol 34:937–949. https://doi.org/10.1016/j.ibmb.2004.06.004
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M et al (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115. https://doi.org/10.1093/nar/gks596
Venkatesh K, Crawford CL, Roe RM (1988) Characterization and the developmental role of plasma juvenile hormone esterase in the adult cabbage looper, Trichoplusia ni. Insect Biochem 18:53–61. https://doi.org/10.1016/0020-1790(88)90036-4
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:134–139
Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33:3–14. https://doi.org/10.1051/apido:2001001
West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12:1003–1012. https://doi.org/10.1046/j.1420-9101.1999.00119.x
Wolfner MF (2002) The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88:85–93. https://doi.org/10.1038/sj.hdy.6800017
Acknowledgements
This work was supported by a FRIA (FC05038) scholarship (to SC) and a CDR funding (Grant Number J.0151.16) (to SA) from the Belgian National Fund for Scientific Research (FRS-FNRS). We thank the Van Buuren–Jaumotte–Demoulin fund for encouraging this research project. We also thank Eric R. Lucas and Laurent Keller (Université de Lausanne) for allowing us to use their Lasius niger transcriptome for primer design.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
The species Lasius niger is not listed on the IUCN Red List of Threatened Species. The ants were handled humanely in accordance with current ethical standards. Special ethical approval is not required to carry out this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Sarah Chérasse and Pauline Dacquin are co-first authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
359_2019_1362_MOESM1_ESM.pdf
Supplementary material 1 Fig. S1. Effect of mating on prophenoloxidase, juvenile hormone esterase, insulin receptor 2 and Cu−Zn superoxide dismutase expression in Lasius niger ant queens. The box and whiskers plots show log10 transformed relative fold changes in prophenoloxidase, juvenile hormone esterase, insulin receptor 2 and Cu−Zn superoxide dismutase gene expression for virgin (no mating), monandrous (mating with a single male) and polyandrous (mating with two male) Lasius niger ant queens. Gene expression was measured 1 and 5 days after mating. Each box corresponds to gene expression measured in eight queens. The midline of each box is the median; the lower and upper edges of the boxes are the first and third quartiles, respectively. The whiskers extend to the most extreme data points that are less than 1.5 times the distance between the first and third quartile away from the lower or upper edges of the box. Above this distance, values are given as outliers (open circles). Letters above the upper whiskers indicate statistically significant differences (or not, when letters are the same) between virgin, monandrous and polyandrous queens. (PDF 651 kb)
359_2019_1362_MOESM2_ESM.docx
Supplementary material 2 Table S1. Primer information. Forward and reverse primer sequences for the housekeeping gene, elongation factor 1α, and the genes of interest, vitellogenin, juvenile hormone esterase, insulin receptor 2, Cu−Zn superoxide dismutase 1, prophenoloxidase and defensin. Melting temperatures (Tm) and amplicon sizes are given for each primer pair. (DOCX 17 kb)
359_2019_1362_MOESM3_ESM.xlsx
Supplementary material 3 Table S2. Gene expression fold change. Relative fold changes in the expression of vitellogenin, juvenile hormone esterase, insulin receptor 2, Cu−Zn superoxide dismutase 1, prophenoloxidase and defensin for virgin, monandrous and polyandrous Lasius niger ant queens. Gene expression was measured 1 day after mating in a first group of queens and 5 days after mating in a second group. The weight and number of eggs laid by each individual queen are also given. (XLSX 18 kb)
359_2019_1362_MOESM4_ESM.xlsx
Supplementary material 4 Table S3. Genotype data. Raw genotype data (microsatellite loci: Ln10-53, Ln10-282, Ln10-174, Ln1-5) for queens 1 day and 5 days after mating. For each queen, the spermatheca, one leg and, when present, eggs were analyzed. This data was used to determine queen-mating frequency. (XLSX 55 kb)
Rights and permissions
About this article
Cite this article
Chérasse, S., Dacquin, P. & Aron, S. Mating triggers an up-regulation of vitellogenin and defensin in ant queens. J Comp Physiol A 205, 745–753 (2019). https://doi.org/10.1007/s00359-019-01362-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-019-01362-0