Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Indirect cue of paternity uncertainty does not affect nest site selection or parental care in a Pacific toadfish

Abstract

Parents are expected to reduce offspring investment when confronted with reliable cues of compromised parentage, yet establishing which cues are reliable is an empirical challenge. Presenting a potential cuckolder to a breeding male is often used in experiments as an indirect cue of paternity loss. However, determining the reliability and hence the utility of this cue is an important but often-overlooked research step. Furthermore, cues of compromised parentage are typically manipulated only during the narrow time window(s) when copulations take place, and so we currently have a poor understanding of whether these cues also convey useful information at other critical timepoints in the reproductive cycle, such as during nest site selection. Here, we present a series of field and laboratory studies using a paternal care giving toadfish, the plainfin midshipman fish (Porichthys notatus) to address these questions. We tested whether the presence of a potential cuckolder near a potential nesting site reduces the odds that males will choose to nest at that site, or reduces the amount of care they provide for offspring. Overall, we found no clear effect of cuckolder presence on the likelihood that a male would occupy nor abandon a nesting site, nor on the amount of paternal care provided. The presentation of a single sneaker male may have been too weak a signal of cuckoldry to elicit a response from guarder males. Alternatively, a single sneaker male may not represent a severe enough threat to paternity to warrant a response. We highlight the importance of considering the diverse range of natural history and ecological factors that underlie paternity cue utility across different model organisms.

Significance statement

Breeding decisions, such as which nesting sites to occupy or how much to invest into offspring, may be affected by external cues of parentage loss (e.g. cuckoldry) or risk thereof. Here, we tested whether the presence of a cuckolder male in the breeding environment affects male nest site selection and paternal care. Despite being a commonly used putative indirect cue of sperm competition and paternity loss, we found no clear evidence that the presence of a single sneaker male affected these breeding decisions. Our results underscore the importance of first establishing the utility of various cues, which involves considering the ecological context from which the cues arise, before using them to assess the mechanisms underlying animal decision-making.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Alonzo SH (2010) Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol Evol 25:99–108. https://doi.org/10.1016/j.tree.2009.07.012

  2. Alonzo SH, Klug H (2012) Paternity, maternity, and parental care. In: Royle NJ, Smiseth PT, Kölliker M (eds) Evolution of parental care. Oxford University Press, Oxford, pp 189–205

  3. Anderson-Bergman C (2017) icenReg: regression models for interval censored data in R. J stat Softw 81:1–23. https://doi.org/10.18637/jss.v081.i12

  4. Arora HL (1948) Observations on the habits and early life history of the batrachoid fish, Porichthys notatus Girard. Copeia 1948:89–93

  5. ASAB/ABS (2018) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 135:I–X. https://doi.org/10.1016/j.anbehav.2017.10.001

  6. Bass AH, Marchaterre MA (1989) Sound-generating (sonic) motor system in a teleost fish (Porichthys notatus): sexual polymorphism in the ultrastructure of myofibrils. J Comp Neurol 286:154–169. https://doi.org/10.1002/cne.902860203

  7. Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

  8. Bose APH, Borowiec B, Scott G, Balshine S (2019a) Nesting on high: reproductive and physiological consequences of breeding in the intertidal zone. Evol Ecol 33:21–36. https://doi.org/10.1007/s10682-019-09970-7

  9. Bose APH, Cogliati KM, Howe HS, Balshine S (2014) Factors influencing cannibalism in the plainfin midshipman fish. Anim Behav 96:159–166. https://doi.org/10.1016/j.anbehav.2014.08.008

  10. Bose APH, Cogliati KM, Luymes N, Bass AH, Marchaterre MA, Sisneros JA, Bolker BM, Balshine S (2018) Phenotypic traits and resource quality as factors affecting male reproductive success in a toadfish. Behav Ecol 29:496–507. https://doi.org/10.1093/beheco/ary002

  11. Bose APH, Kou HH, Balshine S (2016) Impacts of direct and indirect paternity cues on paternal care in a singing toadfish. Behav Ecol 27:1507–1514. https://doi.org/10.1093/beheco/arw075

  12. Bose APH, Lau MJ, Cogliati KM, Neff B, Balshine S (2019b) Cannibalism of young is related to low paternity and nest take-overs in an intertidal fish. Anim Behav 153:41–48. https://doi.org/10.1016/j.anbehav.2019.04.018

  13. Bose APH, McClelland GB, Balshine S (2015) Cannibalism, competition, and costly care in the plainfin midshipman fish, Porichthys notatus. Behav Ecol 27:628–636. https://doi.org/10.1093/beheco/arv203

  14. Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96:213–232. https://doi.org/10.1111/j.1439-0310.1994.tb01011.x

  15. Cogliati KM, Balshine S, Neff BD (2014b) Competition and cuckoldry: estimating fitness of alternative reproductive tactics in plainfin midshipman. Behaviour 151:1209–1227. https://doi.org/10.1163/1568539X-00003180

  16. Cogliati KM, Mistakidis A, Marentette JR, Lau A, Bolker BM, Neff BD, Balshine S (2014a) Comparing population level sexual selection in a species with alternative reproductive tactics. Behav Ecol 25:1524–1533. https://doi.org/10.1093/beheco/aru147

  17. Cogliati KM, Neff BD, Balshine S (2013) High degree of paternity loss in a species with alternative reproductive tactics. Behav Ecol Sociobiol 67:399–408. https://doi.org/10.1007/s00265-012-1460-y

  18. Collette B, Acero A, Betancur R, Cotto A, Rojas P (2010) Porichthys notatus. The IUCN Red List of Threatened Species. Version 2014.3, www.iucnredlist.org

  19. Crean AJ, Marshall DJ (2008) Gamete plasticity in a broadcast spawning marine invertebrate. P Natl Acad Sci USA 105:13508–13513. https://doi.org/10.1073/pnas.0806590105

  20. Demartini EE (1988) Spawning success of the male plainfin midshipman. I. Influences of male body size and area of spawning site. J Exp Mar Biol Ecol 121:177–192. https://doi.org/10.1016/0022-0981(88)90254-7

  21. Demartini EE (1991) Spawning success of the male plainfin midshipman. II. Substratum as a limiting spatial resource. J Exp Mar Biol Ecol 146:235–251. https://doi.org/10.1016/0022-0981(91)90028-U

  22. Eggers S, Griesser M, Nystrand M, Ekman J (2006) Predation risk induces changes in nest-site selection and clutch size in the Siberian jay. Proc R Soc Lond B 273:701–706. https://doi.org/10.1098/rspb.2005.3373

  23. Fitzpatrick JL, Earn DJ, Bucking C, Craig PM, Nadella S, Wood CM, Balshine S (2015) Postcopulatory consequences of female mate choice in a fish with alternative reproductive tactics. Behav Ecol 27:312–320. https://doi.org/10.1093/beheco/arv159

  24. Griffin AS, Alonzo SH, Cornwallis CK (2013) Why do cuckolded males provide paternal care? PLoS Biol 11:e1001520. https://doi.org/10.1371/journal.pbio.1001520

  25. Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616. https://doi.org/10.7717/peerj.616

  26. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425

  27. Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643. https://doi.org/10.1111/j.1558-5646.2009.00924.x

  28. Jamieson I (1995) Do female fish prefer to spawn in nests with eggs for reasons of mate choice copying or egg survival? Am Nat 145:824–832. https://doi.org/10.1086/285770

  29. Kempenaers B, Sheldon BC (1997) Studying paternity and paternal care: pitfalls and problems. Anim Behav 53:423–427. https://doi.org/10.1006/anbe.1996.0377

  30. Kraak SBM (1996) ‘Copying mate choice’: which phenomena deserve this term? Behav Process 36:99–102. https://doi.org/10.1016/0376-6357(95)00020-8

  31. Lee JSF, Bass AH (2004) Does exaggerated morphology preclude plasticity to cuckoldry in the midshipman fish (Porichthys notatus)? Naturwissenschaften 91:338–341. https://doi.org/10.1007/s00114-004-0531-y

  32. Manica A (2004) Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care. Anim Behav 67:1015–1021. https://doi.org/10.1016/j.anbehav.2003.09.011

  33. Mank JE, Avise JC (2006) Comparative phylogenetic analysis of male alternative reproductive tactics in ray-finned fishes. Evolution 60:1311–1316. https://doi.org/10.1554/06-042.1.sl

  34. Miller DJ, Lea RN (1972) Fish bulletin 157: guide to the coastal marine fishes of California. Scripps Institution of Oceanography, UC San Diego, pp 72–73

  35. Miller JS, Bose APH, Fitzpatrick JL, Balshine S (2019a) Sperm maturation and male tactic-specific differences in ejaculates in plainfin midshipman fish Porichthys notatus. J Fish Biol 94:434–445. https://doi.org/10.1111/jfb.13912

  36. Miller JS, Mazzoldi C, Rasotto MB, Balshine S (2019b) Differential investment in male accessory glands: lessons from a marine fish with alternative reproductive tactics. Mar Biol 166:1–12. https://doi.org/10.1007/s00227-019-3474-8

  37. Neff BD (2003) Decisions about parental care in response to perceived paternity. Nature 422:716–719. https://doi.org/10.1038/nature01547.1

  38. Neff BD, Sherman PW (2002) Decision making and recognition mechanisms. Proc R Soc Lond B 269:1435–1441. https://doi.org/10.1098/rspb.2002.2028

  39. Neff BD, Sherman PW (2003) Nestling recognition via direct cues by parental male bluegill sunfish (Lepomis macrochirus). Anim Cogn 6:87–92. https://doi.org/10.1007/s10071-003-0166-y

  40. Parker GA (1990) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Lond B 242:127–133. https://doi.org/10.1098/rspb.1990.0115

  41. Parker GA, Ball MA, Stockley P, Gage MJG (1996) Sperm competition games: individual assessment of sperm competition intensity by group spawners. Proc R Soc Lond B 263:1291–1297. https://doi.org/10.1098/rspb.1996.0189

  42. Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934. https://doi.org/10.1111/j.1469-185X.2010.00140.x

  43. Pärt T, Doligez B (2003) Gathering public information for habitat selection: prospecting birds cue on parental activity. Proc R Soc Lond B 270:1809–1813. https://doi.org/10.1098/rspb.2003.2419

  44. Development Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://cran.r-project.org/

  45. Sheldon BC (2002) Relating paternity to paternal care. Phil Trans R Soc B 357:341–350. https://doi.org/10.1098/rstb.2001.0931

  46. Sherman PW, Neff BD (2003) Father knows best. Nature 425:136–137. https://doi.org/10.1038/425136a

  47. Sisneros JA, Alderks PW, Leon K, Sniffen B (2009) Morphometric changes associated with the reproductive cycle and behaviour of the intertidal-nesting, male plainfin midshipman Porichthys notatus. J Fish Biol 74:18–36. https://doi.org/10.1111/j.1095-8649.2008.02104.x

  48. Sisneros JA, Forlano PM, Knapp R, Bass AH (2004) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocr 136:101–116. https://doi.org/10.1016/j.ygcen.2003.12.007

  49. Svensson O, Kvarnemo C (2007) Parasitic spawning in sand gobies: an experimental assessment of nest-opening size, sneaker male cues, paternity, and filial cannibalism. Behav Ecol 18:410–419. https://doi.org/10.1093/beheco/arl098

  50. Svensson O, Magnhagen C, Forsgren E, Kvarnemo C (1998) Parental behaviour in relation to the occurrence of sneaking in the common goby. Anim Behav 56:175–179. https://doi.org/10.1006/anbe.1998.0769

  51. Taborsky M (2008) Alternative reproductive tactics in fish. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 251–299

  52. Walker HJ, Rosenblatt RH (1988) Species pacific toadfishes of the genus Porichthys (Batrachoididae) with descriptions of three new species. Copeia 1988:887–904. https://doi.org/10.2307/1445712

  53. Warner JA, Case JF (1980) The zoogeography and dietary induction of bioluminescence in the midshipman fish, Porichthys notatus. Biol Bull 159:231–246. https://doi.org/10.2307/1541021

  54. Westneat DF, Sherman PW (1993) Parentage and the evolution of paternal care. Behav Ecol 4:66–77. https://doi.org/10.1093/beheco/4.1.66

Download references

Acknowledgements

We thank Pamela Walker, Ross Shepard, Captain Bill, Rubie Cogswell, and the Stz’uminus First Nation for their hospitality and for providing access to field sites. We also thank the anonymous reviewers for their helpful comments on this paper.

Data accessibility

Analyses reported in this article can be reproduced using the data provided in the supplementary materials.

Funding

This work was funded by a Natural Sciences and Engineering Research Council of Canada grant to SB. Additional funding was provided to AB and JM by the Department of Psychology, Neuroscience and Behaviour at McMaster University and to AB by the McMaster University Graduate Students’ Association, as well as the PADI Foundation.

Author information

Correspondence to Aneesh P. H. Bose.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The plainfin midshipman is a common intertidal species and is not considered threatened or endangered (Collette et al. 2010). This work was done in accordance with Fisheries and Oceans Canada scientific collections permits (XR 812015, XR 582017). The procedures used in this study were approved by the McMaster University Animal Research Ethics Board (AUP 13-12-52) and the University of Victoria Animal Care Committee (AUP 2017-003(1)), and are in line with the guidelines set by the Canadian Council on Animal Care (CCAC) and ASAB/ABS (2018) regarding the treatment of animals in research and teaching. Furthermore, these fish were also used in a number of additional experiments (e.g. Bose et al. 2018; Miller et al. 2019a, b).

Additional information

Publisher’s note

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

Communicated by K. Lindström

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bose, A.P.H., Houpt, N., Rawlins, M. et al. Indirect cue of paternity uncertainty does not affect nest site selection or parental care in a Pacific toadfish. Behav Ecol Sociobiol 74, 24 (2020). https://doi.org/10.1007/s00265-020-2803-8

Download citation

Keywords

  • Parental investment
  • Nest choice
  • Intertidal zone
  • Cuckoldry
  • Midshipman fish