Skip to main content
SpringerLink
Log in

The specificity of sperm-mediated paternal effects in threespine sticklebacks

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Parental effects may help offspring respond to challenging environments, but whether parental exposure to different environmental challenges induces similar responses in offspring is largely unknown. We compared the offspring of threespine stickleback (Gasterosteus aculeatus) fathers who had been exposed to a potentially threatening stimulus (net), a native predator (sculpin), or who had been left unexposed (control). Relative to offspring of control fathers, offspring of sculpin-exposed fathers were more responsive (greater change in activity) to a simulated sculpin predator attack, while offspring of net-exposed fathers were less responsive (fewer antipredator behaviors) and showed altered stress responses compared to the control. To evaluate whether parental exposure primes offspring to respond to specific stimuli (e.g., offspring of net-exposed fathers respond most strongly to a net), we then exposed offspring of each paternal treatment to nets, native sculpin models, or non-native trout models. Paternal treatment did not influence offspring response to different stimuli; instead, offspring were generally more responsive to the native sculpin predator compared to nets or non-native trout predator, suggesting that sticklebacks have innate predator recognition of native predators. Collectively, these results underscore that, while parental exposure to non-ecologically relevant stressors elicits effects in intergenerational studies, these findings may not mirror those produced when parents encounter ecologically relevant stressors. Knowing that parental effects can be predator-specific furthers our understanding of the ways in which parental effects may evolve to be adaptive and suggests the potential for transgenerational plasticity to affect how animals respond to human induced environmental change, including non-native predators.

Significance statement

Despite extensive evidence for parental effects, we have very little knowledge regarding whether parental effects are stimuli-specific. Here, we found that paternal exposure to different, potentially stressful stimuli prior to fertilization has specific effects on offspring traits: paternal exposure to a model of a sculpin (a native predator) heightened offspring responsivity to simulated predation risk, while paternal exposure to an artificial stimulus/stressor (net) reduced offspring antipredator behavior relative to the control. We found no evidence that offspring responded more strongly to the stimulus that their father encountered; instead, offspring were overall more responsive to a sculpin predator compared to a net or non-native trout. Overall, these results suggest that sperm-mediated paternal effects can be highly specific, and while non-ecologically relevant stimuli elicit effects in intergenerational studies, these effects may differ from those that occur when parents are exposed to native, ecologically relevant stimuli.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Code availability

Not applicable

References

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Atherton JA, McCormick MI (2020) Parents know best: transgenerational predator recognition through parental effects. PeerJ 8:e9340

    Article  PubMed  PubMed Central  Google Scholar 

  • Bali A, Jaggi AS (2015) Electric foot shock stress: a useful tool in neuropsychiatric studies. Rev Neurosci 26:655–677

    Article  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bell AM, Hellmann JK (2019) An integrative framework for understanding the mechanisms and multigenerational consequences of transgenerational plasticity. Annu Rev Ecol Evol Syst 50:97–118

    Article  Google Scholar 

  • Bonduriansky R, Day T (2008) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst 40:103–125

    Article  Google Scholar 

  • Borg B (1982) Seasonal effects of photoperiod and temperature on spermatogenesis and male secondary sexual characters in the three-spined stickleback, Gasterosteus aculeatus L. Can J Zool 60:3377–3386

    Article  Google Scholar 

  • Brunton PJ (2013) Effects of maternal exposure to social stress during pregnancy: consequences for mother and offspring. Reproduction 146:R175–R189

    Article  CAS  PubMed  Google Scholar 

  • Caton JS, Crouse MS, Reynolds LP, Neville TL, Dahlen CR, Ward AK, Swanson KC (2019) Maternal nutrition and programming of offspring energy requirements. Transl Anim Sci 3:976–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chivers DP, Brown GE, Smith RJF (1995) Acquired recognition of chemical stimuli from pike, Esox lucius, by Brook Sticklebacks, Culaea inconstans (Osteichthyes, Gasterosteidae). Ethology 99:234–242

    Article  Google Scholar 

  • Crean AJ, Marshall DJ (2009) Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos Trans R Soc B 364:1087–1096

    Article  Google Scholar 

  • Dias BG, Ressler KJ (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17:89–96

    Article  CAS  PubMed  Google Scholar 

  • Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75

    Article  PubMed  Google Scholar 

  • Donelan SC, Hellmann JK, Bell AM, Luttbeg B, Orrock JL, Sheriff MJ, Sih A (2020) Transgenerational plasticity in human-altered environments. Trends Ecol Evol 35:115–124

    Article  PubMed  Google Scholar 

  • Evans JP, Wilson AJ, Pilastro A, Garcia-Gonzalez F (2019) Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications. Reproduction 157:R109–R126

    Article  CAS  PubMed  Google Scholar 

  • Fischer S, Oberhummer E, Cunha-Saraiva F, Gerber N, Taborsky B (2017) Smell or vision? The use of different sensory modalities in predator discrimination. Behav Ecol Sociobiol 71:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM (2014) Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17:667–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giles N (1984) Development of the overhead fright response in wild and predator-naive three-spined sticklebacks, Gasterosteus aculeatus L. Anim Behav 32:276–279

    Article  Google Scholar 

  • Golub JL (2013) Embryonic learning in threespine stickleback (Gasterosteus aculeatus). PhD thesis, Clark University

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 1:1–22

  • Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • Hellmann JK, Bukhari SA, Deno J, Bell AM (2020a) Sex-specific plasticity across generations I: Maternal and paternal effects on sons and daughters. J Anim Ecol 89:2788–2799

    Article  PubMed  Google Scholar 

  • Hellmann JK, Carlson ER, Bell AM (2020b) Sex-specific plasticity across generations II: grandpaternal effects are lineage- and sex-specific. J Anim Ecol 89:2800–2812

    Article  PubMed  Google Scholar 

  • Herman J, Sultan S (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front Plant Sci 2:102

    Article  PubMed  PubMed Central  Google Scholar 

  • Hettyey A, Rölli F, Thürlimann N, Zürcher A-C, Van Buskirk J (2012) Visual cues contribute to predator detection in anuran larvae. Biol J Linn Soc 106:820–827

    Article  Google Scholar 

  • Hirvonen H, Ranta E, Piironen J, Laurila A, Peuhkuri N (2000) Behavioural responses of naive Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos 88:191–199

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Immler S (2018) The sperm factor: paternal impact beyond genes. Heredity 121:239–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, Czaran T (1995) The adaptive advantage of phenotypic memory in changing environments. Philos Trans R Soc B 350:133–141

    Article  CAS  Google Scholar 

  • Królikowska N, Szymkowiak J, Laidlaw RA, Kuczyński L (2016) Threat-sensitive anti-predator defence in precocial wader, the northern lapwing Vanellus vanellus. Acta Ethol 19:163–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Landeira-Dabarca A, Näslund J, Johnsson JI, Álvarez M (2019) Cue recognition and behavioural responses in the three-spined stickleback (Gasterosteus aculeatus) under risk of fish predation. Acta Ethol 22:209–221

    Article  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Ad Stud Behav 27:215–290

    Article  Google Scholar 

  • Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418–427

    Article  PubMed  Google Scholar 

  • McGhee KE, Feng S, Leasure S, Bell AM (2015) A female’s past experience with predators affects male courtship and the care her offspring will receive from their father. Proc R Soc B 282:20151840

    Article  PubMed  Google Scholar 

  • Mileva VR, Fitzpatrick JL, Marsh-Rollo S, Gilmour KM, Wood CM, Balshine S (2009) The stress response of the highly social African cichlid Neolamprologus pulcher. Physiol Biochem Zool 82:720–729

    Article  PubMed  Google Scholar 

  • Mommer BC, Bell AM (2013) A test of maternal programming of offspring stress response to predation risk in threespine sticklebacks. Physiol Behav 122:222–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Näslund J, Pettersson L, Johnsson JI (2016) Behavioural reactions of three-spined sticklebacks to simulated risk of predation—effects of predator distance and movement. FACETS 1:55–66

    Article  Google Scholar 

  • Oulton LJ, Haviland V, Brown C (2013) Predator recognition in rainbowfish, Melanotaenia duboulayi, embryos. PLoS One 8:e76061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, Myers RM, Mori S, Schluter D, Kingsley DM (2004) The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14:1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Potticary AL, Duckworth RA (2020) Multiple environmental stressors induce an adaptive maternal effect. Am Nat 196:487–500

    Article  PubMed  Google Scholar 

  • Ramsay JM, Feist GW, Varga ZM, Westerfield M, Kent ML, Schreck CB (2009) Whole-body cortisol response of zebrafish to acute net handling stress. Aquaculture 297:157–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Relyea RA (2004) Fine-tuned phenotypes; tadpole plasticity under 16 combinations of predators and competitors. Ecology 85:172–179

    Article  Google Scholar 

  • Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL (2013) Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 33:9003–9012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodgers AB, Morgan CP, Leu NA, Bale TL (2015) Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA 112:13699–13704

    Article  CAS  PubMed  Google Scholar 

  • Schneider ML, Coe CL (1993) Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J Dev Behav Pediatr 14:81–87

    Article  CAS  PubMed  Google Scholar 

  • Schneider NA, Griesser M (2012) Incubating females use dynamic risk assessment to evaluate the risk posed by different predators. Behav Ecol 24:47–52

    Article  Google Scholar 

  • Short AK, Fennell KA, Perreau VM, Fox A, O’Bryan MK, Kim JH, Bredy TW, Pang TY, Hannan AJ (2016) Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring. Transl Psychiatry 6:e837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein LR, Bell AM (2014) Paternal programming in sticklebacks. Anim Behav 95:165–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Stein LR, Bell AM (2019) The role of variation and plasticity in parental care during the adaptive radiation of three-spine sticklebacks. Evolution 73:1037–1044

    Article  PubMed  PubMed Central  Google Scholar 

  • Storm J, Lima S (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Am Nat 175:382–390

    Article  PubMed  Google Scholar 

  • Sultan SE, Barton K, Wilczek AM (2009) Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90:1831–1839

    Article  PubMed  Google Scholar 

  • Tariel J, Plénet S, Luquet É (2020) Transgenerational plasticity in the context of predator-prey interactions. Front Ecol Evol 8:319

    Article  Google Scholar 

Download references

Acknowledgements

Thank you to the Bell lab, Dr. Andrea Pilastro, and two anonymous reviewers for the helpful comments on the previous versions of this manuscript and to Ryan Earley for the help with the hormone assays.

Funding

This work was supported by the National Institutes of Health award number 2R01GM082937-06A1 to AMB and National Institutes of Health NRSA fellowship F32GM121033 to JKH.

Author information

Author notes

  1. Jennifer K. Hellmann

    Present address: Department of Biology, University of Dayton, Dayton, OH, 45469, USA

Authors and Affiliations

  1. Department of Evolution, Ecology and Behavior, School of Integrative Biology, University of Illinois Urbana-Champaign, Urbana, IL, 61801, USA

    Eunice Chen, Christian Zielinski, Jack Deno, Raiza Singh, Alison M. Bell & Jennifer K. Hellmann

  2. Carl R. Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL, 61801, USA

    Alison M. Bell

  3. Program in Ecology, Evolution and Conservation, University of Illinois Urbana-Champaign, Urbana, IL, 61801, USA

    Alison M. Bell

Authors
  1. Eunice Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian Zielinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jack Deno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Raiza Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alison M. Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jennifer K. Hellmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JH and AMB conceived of the study with input from EC, CZ, RS, and JD. EC and CZ collected the behavioral data and processed the cortisol samples for Part I with aid from JKH; RS and JD collected the behavioral data for Part II. JKH analyzed the data; EC wrote the first draft of the manuscript with aid from CZ and JKH; JKH, AMB, and EC edited the manuscript.

Corresponding author

Correspondence to Jennifer K. Hellmann.

Ethics declarations

Ethics approval

All methods, including euthanasia techniques, were approved by Institutional Animal Care and Use Committee at University of Illinois Urbana-Champaign (protocol ID 18080) and adhere to the guidelines set forth by the Animal Behavior Society/Association for the Study of Animal Behaviour.

Consent to participate

Not applicable

Consent for publication

All authors have given their consent for publication

Competing interests

The authors declare no competing interests.

Additional information

Communicated by A. Pilastro

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 195 kb)

ESM 2

(TXT 15 kb)

ESM 3

(TXT 8 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, E., Zielinski, C., Deno, J. et al. The specificity of sperm-mediated paternal effects in threespine sticklebacks. Behav Ecol Sociobiol 75, 68 (2021). https://doi.org/10.1007/s00265-021-03001-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-021-03001-8

Keywords

Search

Navigation