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Parental Care Alters the Egg Microbiome of Maritime Earwigs

  • Invertebrate Microbiology
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Abstract

Recruitment of beneficial microbes to protect offspring, often reducing the energetic costs of care, is now recognized as an important component of parental care in many animals. Studies on earwigs (order Dermaptera) have revealed that removal of females from egg tending increases mortality of eggs due to fungal infections, possibly caused by changes in the bacterial microbiome on the egg surface. We used a controlled female-removal experiment to evaluate whether female nest attendance in the maritime earwig, Anisolabis maritima, influences the bacterial microbiome on the egg surface. Further, we analyzed the microbiomes of mothers and their eggs to determine if there are a core set of bacteria transferred to eggs through female care. Microbiomes were analyzed using 16S rRNA bacterial DNA sequencing, revealing that bacterial operational taxonomic unit (OTU) richness and diversity were both significantly higher for female attended versus unattended eggs. The core microbiome of adult females contained bacteria which have the potential to carry anti-fungal characteristics; these bacteria were found in higher presence and relative abundance on eggs where females were allowed to provide care. These results demonstrate that female egg attendance significantly impacts the bacterial microbiome of A. maritima eggs, and identifies specific bacteria within the egg microbiome that should be investigated further for beneficial anti-fungal properties in this system.

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Data Availability

Microbiome DNA sequence data are publicly accessible on the Sequence Read Archive (SRA) database under the BioProject accession number: PRJNA630101.

References

  1. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press

  2. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100(916):687–690

    Article  Google Scholar 

  3. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldinc, Chicago, pp 136–179

    Google Scholar 

  4. Woolfenden GE, Fitzpatrick JW (1984) The Florida scrub jay: demography of a cooperative-breeding bird. Princeton University Press, New Jersey

    Google Scholar 

  5. Creel SR, Rabenold KN (1994) Inclusive fitness and reproductive strategies in dwarf mongooses. Behav Ecol 5:339–348. https://doi.org/10.1093/beheco/5.3.339

    Article  Google Scholar 

  6. König B (1997) Cooperative care of young in mammals. Naturwissenschaften 84:95–104

    Article  PubMed  Google Scholar 

  7. Zink (2000) The evolution of intraspecific brood parasitism in birds and insects. Am Nat 155:395–405. https://doi.org/10.2307/3078874

    Article  PubMed  Google Scholar 

  8. Zink AG (2001) The optimal degree of parental care asymmetry among communal breeders. Anim Behav 61:439–446. https://doi.org/10.1006/anbe.2000.1609

    Article  Google Scholar 

  9. Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39:343–363. https://doi.org/10.1146/annurev.ecolsys.39.110707.173354

    Article  Google Scholar 

  10. Zink AG, Lyon BE (2016) Evolution of conspecific brood parasitism versus cooperative breeding as alternative reproductive tactics. Am Nat 187:35–47. https://doi.org/10.1086/684127

    Article  PubMed  Google Scholar 

  11. Bristow CM (1983) Treehoppers transfer parental care to ants: a new benefit of mutualism. Science 220:532–533. https://doi.org/10.1126/science.220.4596.532

    Article  CAS  PubMed  Google Scholar 

  12. Zink AG (2003) Quantifying the costs and benefits of parental care in female treehoppers. Behav Ecol 14:687–693. https://doi.org/10.1093/beheco/arg044

    Article  Google Scholar 

  13. Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11:e1001631. https://doi.org/10.1371/journal.pbio.1001631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475–479. https://doi.org/10.1016/j.cub.2004.12.084

    Article  CAS  PubMed  Google Scholar 

  15. Kaiwa N, Hosokawa T, Nikoh N, Tanahashi M, Moriyama M, Meng XY, Maeda T, Yamaguchi K, Shigenobu S, Ito M, Fukatsu T (2014) Symbiont-supplemented maternal investment underpinning host’s ecological adaptation. Curr Biol 24:2465–2470. https://doi.org/10.1016/j.cub.2014.08.065

    Article  CAS  PubMed  Google Scholar 

  16. Flórez LV, Biedermann PH, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 32:904–936. https://doi.org/10.1039/C5NP00010F

    Article  PubMed  Google Scholar 

  17. Łukasik P, van Asch M, Guo H, Ferrari J, Charles J, Godfray H (2013) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 16:214–218

    Article  PubMed  Google Scholar 

  18. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810. https://doi.org/10.1038/nature06244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Whipps JM, Lewis K, Cooke RC (1988) Mycoparasitism and plant dis. control. In: Burge MN (ed) Fungi in biological control systems. Manchester University Press, Manchester, pp 161–187

    Google Scholar 

  20. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118. https://doi.org/10.1126/science.1058709

    Article  CAS  PubMed  Google Scholar 

  21. Huttenhower C, Gevers D, Knight R et al (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. https://doi.org/10.1038/nature11234

    Article  CAS  Google Scholar 

  22. Theis KR, Schmidt TM, Holekamp KE (2012) Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci Rep 2:615. https://doi.org/10.1038/srep00615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Swei A, Kwan JY (2017) Tick microbiome and pathogen acquisition altered by host blood meal. ISME J 11:813–816. https://doi.org/10.1038/ismej.2016.152

    Article  PubMed  Google Scholar 

  24. Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, Antonopoulos D, Umesaki Y, Chervonsky AV (2013) Gender bias in autoimmunity is influenced by microbiota. Immunity 39:400–412. https://doi.org/10.1016/j.immuni.2013.08.013

    Article  CAS  PubMed  Google Scholar 

  25. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. https://doi.org/10.1038/nrmicro2262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci 90:5695–5699. https://doi.org/10.1073/pnas.90.12.5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Walke JB, Harris RN, Reinert LK, Rollins-Smith LA, Woodhams DC (2011) Social immunity in amphibians: evidence for vertical transmission of innate defenses. Biotropica 43:396–400. https://doi.org/10.1111/j.1744-7429.2011.00787.x

    Article  Google Scholar 

  28. Wong JWY, Meunier J, Kölliker M (2013) The evolution of parental care in insects: the roles of ecology, life history and the social environment. Ecol Entomol 38:123–137. https://doi.org/10.1111/een.12000

    Article  Google Scholar 

  29. Salem H, Florez L, Gerardo N, Kaltenpoth M (2015) An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc R Soc B Biol Sci 282:282. https://doi.org/10.1098/rspb.2014.2957

    Article  Google Scholar 

  30. Eberle M, Mclean D (1982) Initiation and orientation of the symbiote migration in the human body louse Pediculus humanus L. J Insect Physiol 28:417–422. https://doi.org/10.1016/0022-1910(82)90068-3

    Article  Google Scholar 

  31. Estes AM, Hearn DJ, Snell-Rood EC et al (2013) Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae). PLoS ONE 8. https://doi.org/10.1371/journal.pone.0079061

  32. Bennett CB (1904) Earwigs (Anisolabia Maritima Bon.). Psyche: J Entomol 11:47–53. https://doi.org/10.1155/1904/60136

    Article  Google Scholar 

  33. Miller JS, Zink AG (2012) Parental care trade-offs and the role of filial cannibalism in the maritime earwig, Anisolabis maritima. Anim Behav 83:1387–1394. https://doi.org/10.1016/j.anbehav.2012.03.006

    Article  Google Scholar 

  34. Miller JS, Rudolph L, Zink AG (2011) Maternal nest defense reduces egg cannibalism by conspecific females in the maritime earwig Anisolabis maritima. Behav Ecol Sociobiol 65:1873–1879. https://doi.org/10.1007/s00265-011-1196-0

    Article  Google Scholar 

  35. Boos S, Meunier J, Pichon S, Kölliker M (2014) Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol 25:754–761. https://doi.org/10.1093/beheco/aru046

    Article  Google Scholar 

  36. Vancassel M (1984) Plasticity and adaptive radiation of Dermapteran parental behavior: results and perspectives. Adv Study Behav 14:51–80. https://doi.org/10.1016/s0065-3454(08)60299-5

    Article  Google Scholar 

  37. Rankin SM, Storm SK, Pieto DL, Risser AL (1996) Maternal behavior and clutch manipulation in the ring-legged earwig (Dermaptera: Carcinophoridae). J Insect Behav 9:85–103. https://doi.org/10.1007/bf02213725

    Article  Google Scholar 

  38. Popham EJ (2009) The anatomy in relation to feeding habits of Forficula Auricularial. and other Dermaptera. Proc Zool Soc London 133:251–300. https://doi.org/10.1111/j.1469-7998.1959.tb05563.x

    Article  Google Scholar 

  39. Hack NL, Iyengar VK (2017) Big wigs and small wigs: time, sex, size and shelter affect cohabitation in the maritime earwig (Anisolabis maritima). PLoS One 12:e0185754. https://doi.org/10.1371/journal.pone.0185754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22:939–946. https://doi.org/10.1101/gr.128124.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Paulson JN, Stine OC, Bravo H C et al (2013) Differential abundance analysis for microbial marker-gene surveys. Nature methods 10:1200-1202. https://doi.org/10.1038/nmeth.2658

  42. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. https://doi.org/10.1186/s40168-017-0237-y

    Article  PubMed  PubMed Central  Google Scholar 

  43. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  46. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276

    Article  CAS  PubMed  Google Scholar 

  47. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. https://doi.org/10.1093/bioinformatics/btp636

    Article  CAS  PubMed  Google Scholar 

  48. Edmonds K, Williams L (2017) The role of the negative control in microbiome analyses. FASEB J 31:940–943

    Google Scholar 

  49. Kim D, Hofstaedter CE, Zhao C (2017) Optimizing methods and dodging pitfalls in microbiome research. Microbiome 5:52. https://doi.org/10.1186/s40168-017-0267-5

    Article  PubMed  PubMed Central  Google Scholar 

  50. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585. https://doi.org/10.1128/aem.01996-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lauková A, Kandričáková A, Imrichova J, Strompfova V et al (2013) Properties of Enterococcus thailandicus isolates from beavers. Afr J Microbiol Res 7:3569–3574. https://doi.org/10.5897/AJMR2013.5654

    Article  Google Scholar 

  52. Ahmadova A, Todorov SD, Hadji-Sfaxi I, Choiset Y, Rabesona H, Messaoudi S, Kuliyev A, Dora Gombossy de Melo Franco B, Chobert JM, Haertlé T (2013) Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolated from homemade Azerbaijani cheese. Anaerobe 20:42–49. https://doi.org/10.1016/j.anaerobe.2013.01.003

    Article  CAS  PubMed  Google Scholar 

  53. Sapountzis P, Gruntjes T, Otani S, Estevez J, da Costa RR, Plunkett III G, Perna NT, Poulsen M (2015) The Enterobacterium Trabulsiella odontotermitis presents novel adaptations related to its association with fungus-growing termites. Appl Environ Microbiol 81:6577–6588. https://doi.org/10.1128/aem.01844-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Chou J-H, Chen W-M, Arun AB, Young CC (2007) Trabulsiella odontotermitis sp. nov., isolated from the gut of the termite Odontotermes formosanus Shiraki. Int J Syst Evol Microbiol 57:696–700. https://doi.org/10.1099/ijs.0.64632-0

    Article  CAS  PubMed  Google Scholar 

  55. Mille-Lindblom C, Fischer H, Tranvik JL (2006) Antagonism between bacteria and fungi: substrate competition and a possible tradeoff between fungal growth and tolerance towards bacteria. Oikos 113:233–242

    Article  Google Scholar 

  56. Graham CE, Cruz MR, Garsin DA, Lorenz MC (2017) Enterococcus faecalisbacteriocin EntV inhibits hyphal morphogenesis, biofilm formation, and virulence of Candida albicans. Proc Natl Acad Sci 114:4507–4512. https://doi.org/10.1073/pnas.1620432114

  57. Belguesmia Y, Choiset Y, Rabesona H, Baudy-Floc’h M, le Blay G, Haertlé T, Chobert JM (2013) Antifungal properties of durancins isolated from Enterococcus duransA5-11 and of its synthetic fragments. Lett Appl Microbiol 56:237–244. https://doi.org/10.1111/lam.12037

    Article  CAS  PubMed  Google Scholar 

  58. Martin JD, Mundt JO (1972) Enterococci in insects. Appl Environ Microbiol 24:575–580

    Article  CAS  Google Scholar 

  59. Yun J-H, Roh SW, Whon TW, Jung MJ, Kim MS, Park DS, Yoon C, Nam YD, Kim YJ, Choi JH, Kim JY, Shin NR, Kim SH, Lee WJ, Bae JW (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264. https://doi.org/10.1128/aem.01226-14

    Article  PubMed  PubMed Central  Google Scholar 

  60. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757. https://doi.org/10.1086/284741

    Article  Google Scholar 

  61. Flöder S, Sommer U (1999) Diversity in planktonic communities: an experimental test of the intermediate disturbance hypothesis. Limnol Oceanogr 44:1114–1119. https://doi.org/10.4319/lo.1999.44.4.1114

    Article  Google Scholar 

  62. Meunier J, Kolliker M (2012) When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs. Biol Lett 8:547–550. https://doi.org/10.1098/rsbl.2012.0151

    Article  PubMed  PubMed Central  Google Scholar 

  63. Kramer J, Körner M, Diehl JM, Scheiner C, Yüksel-Dadak A, Christl T, Kohlmeier P, Meunier J (2017) When earwig mothers do not care to share: parent–offspring competition and the evolution of family life. Funct Ecol 31:2098–2107. https://doi.org/10.1111/1365-2435.12915

  64. Suzuki S (2011) Provisioning mass by females of the maritime earwig, Anisolabis maritima, is not adjusted based on the number of young. J Insect Sci 11:1–7. https://doi.org/10.1673/031.011.16001

  65. Kaltenpoth M, Winter SA, Kleinhammer A (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiol Ecol 69:373–383. https://doi.org/10.1111/j.1574-6941.2009.00722.x

  66. Martín-Vivaldi M, Soler JJ, Peralta-Sánchez JM, Arco L, Martín-Platero AM, Martínez-Bueno M, Ruiz-Rodríguez M, Valdivia E (2014) Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J Anim Ecol 83:1289–1301. https://doi.org/10.1111/1365-2656.12243

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Acknowledgments

A special thanks to the Student Enrichment Office (SEO) at San Francisco State University for their continued support, as well as members of the Swei, Zink, and Vredenburg labs. Further, we thank Adrienne Lee for the help with maintaining earwig nests, Michele Conrad of the GTAC for the help with molecular work, and the Moreau Lab at University of Chicago for their assistance in the analyses of microbiome sequence data. J. Greer would like to thank his grandfather, James Curtis, grandmother, Marjorie Curtis, and mother, Robin Curtis-Greer, for their unwavering encouragement and support.

Funding

This study was funded by a National Science Foundation Grant IOS-1258133 awarded to Drs. Andrew Zink and Vance Vredenburg as well as NSF grants to Andrea Swei (DBI-1427772, DEB-1745411, DEB-175037) and a Miseq Mini Grant awarded to Jordan Greer. Jordan Greer also received financial support from a MBRS-RISE fellowship awarded via the National Institutes of Health (R25-GM059298) and the Genentech Foundation MS Dissertation Scholarship.

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Jordan Greer designed the project, collected specimens and samples, conducted DNA-based lab work, collected and analyzed the data, and contributed to the manuscript. Andrea Swei contributed to the analysis of the microbiome data, contributed reagents and analytical tools, and contributed to the manuscript. Vance Vredenburg contributed analytical tools, helped with intellectual design, and contributed to the manuscript. Andrew Zink designed the project, collected specimens, analyzed data, and contributed to the manuscript. The first draft of the manuscript was written by Jordan Greer and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Jordan A. Greer.

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Greer, J.A., Swei, A., Vredenburg, V.T. et al. Parental Care Alters the Egg Microbiome of Maritime Earwigs. Microb Ecol 80, 920–934 (2020). https://doi.org/10.1007/s00248-020-01558-x

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