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Mating triggers an up-regulation of vitellogenin and defensin in ant queens

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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, CuZn 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.

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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.

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Correspondence to Serge Aron.

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The authors declare that they have no conflict of interest.

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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.

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Sarah Chérasse and Pauline Dacquin are co-first authors.

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359_2019_1362_MOESM1_ESM.pdf

Supplementary material 1 Fig. S1. Effect of mating on prophenoloxidase, juvenile hormone esterase, insulin receptor 2 and CuZn 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 CuZn 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, CuZn 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, CuZn 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)

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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

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  • DOI: https://doi.org/10.1007/s00359-019-01362-0

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