Skip to main content
SpringerLink
Log in

The effect of nuptial gift number on fertilization success in a Hawaiian swordtail cricket

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

Abstract

In many insects, males transfer nuptial gifts to females prior to, during, or after copulation. Nuptial gifts comprise any form of non-gametic material transfer, such as glandular secretions, prey items, and spermatophores. These gifts can increase male fitness by facilitating copulation or sperm transfer or by promoting the female’s use of the focal male’s sperm. However, when a female mates with multiple males, the relationships between the relative size, number, or quality of nuptial gifts that each male donates and the proportion of offspring that each male sires are unknown in many cases. Here, we assessed these relationships in the Hawaiian swordtail cricket Laupala cerasina. We experimentally manipulated the number of gifts a female received from two male mating partners in sequence, with the first male giving either more, fewer, or an equal number of gifts relative to the second male. We found that there was a significant positive relationship between nuptial gift number and paternity share. In addition, we found considerable first-male sperm precedence, regardless of gift contribution. Finally, offspring from second males tended to be produced later and to be part of larger families. These results show that both nuptial gift number and mating order play important roles in sperm use patterns and fertilization success in this species.

Significance statement

In many insects, males transfer nuptial gifts (a token, often nutritional, gift) to females prior to, during, or after copulation. In the Hawaiian swordtail cricket Laupala cerasina, males transfer a series of nuptial gifts in the form of spermless spermatophores, to females during courtship. Moreover, males experience sperm competition as females of this species are known to mate multiply. By manipulating the number of gifts transferred, we tested the hypothesis that males who transfer more nuptial gifts achieve higher fitness by fathering more offspring. We found a significant positive relationship between gift number and the proportion of offspring a male sires. In addition, controlling for gift number, the first male to mate with a female achieves more paternity. These results show that both nuptial gift number and mating order affect sperm use patterns and fertilization success in this species.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Albo MJ, Costa FG (2010) Nuptial gift-giving behaviour and male mating effort in the Neotropical spider Paratrechalea ornata (Trechaleidae). Anim Behav 79:1031–1036

    Article  Google Scholar 

  • Alcock J (1979) Selective mate choice by females of Harpobittacus Australis (Mecoptera: Bittacidae). Psyche 86:213–217

    Article  Google Scholar 

  • Brown WD (1997) Courtship feeding in tree crickets increases insemination and female reproductive life span. Anim Behav 54:1369–1382

    Article  CAS  Google Scholar 

  • deCarvalho TN, Shaw KL (2010) Elaborate courtship enhances sperm transfer in the Hawaiian swordtail cricket, Laupala cerasina. Anim Behav 79:819–826

    Article  Google Scholar 

  • deCarvalho TN, Fergus DJ, Bell RC, Shaw KL (2012) Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina. Behav Ecol Sociobiol 66:1333–1340

    Article  Google Scholar 

  • DiRienzo N, Marshall JL (2013) Function of the hemolymph nuptial gift in the ground cricket, Allonemobius socius. Ethology 119:104–109

    Article  Google Scholar 

  • Dodson G, Morris G, Gwynne D (1983) Mating behavior of the primitive orthopteran genus Cyphoderris (Haglidae). Orthopteran mating systems: sexual competition in a diverse group of insects/edited by DT Gwynnw and GK Morris

  • Ellison CK, Shaw KL (2010) Mining non-model genomic libraries for microsatellites: BAC versus EST libraries and the generation of allelic richness. BMC Genomics 11:428

    Article  Google Scholar 

  • Engqvist L, Sauer KP (2001) Strategic male mating effort and cryptic male choice in a scorpionfly. P Roy Soc B-Biol Sci 268:729–735

    Article  CAS  Google Scholar 

  • Engqvist L, Sauer KP (2003) Determinants of sperm transfer in the scorpionfly Panorpa cognata: male variation, female condition and copulation duration. J Evolution Biol 16:1196–1204

    Article  CAS  Google Scholar 

  • Engqvist L, Dekomien G, Lippmann T, Epplen JT, Sauer KP (2007) Sperm transfer and paternity in the scorpionfly Panorpa cognata: large variance in traits favoured by post-copulatory episodes of sexual selection. Evol Ecol 21:801–816

    Article  Google Scholar 

  • Fedorka KM, Mousseau TA (2002a) Nuptial gifts and the evolution of male body size. Evolution 56:590–596

    Article  Google Scholar 

  • Fedorka KM, Mousseau TA (2002b) Tibial spur feeding in ground crickets: larger males contribute larger gifts (Orthoptera: Gryllidae). Fla Entomol 85:317–323

    Article  Google Scholar 

  • Gao QH, Hua BZ (2013) Co-evolution of the mating position and male genitalia in insects: a case study of a hangingfly. PLoS One 8:e80651

    Article  Google Scholar 

  • Gwynne DT (1984) Nuptial feeding behavior and female choice of mates in Harpobittacus similis (Mecoptera, Bittacidae). J Aust Entomol Soc 23:271–276

    Article  Google Scholar 

  • Gwynne DT (1986) Courtship feeding in katydids (Orthoptera, Tettigoniidae): investment in offspring or in obtaining fertilizations. Am Nat 128:342–352

    Article  Google Scholar 

  • Gwynne DT, Snedden AW (1995) Paternity and female remating in Requena verticalis (Orthoptera: Tettigoniidae). Ecol Entomol 20:191–194

    Article  Google Scholar 

  • Gwynne DT (1997) The evolution of edible ‘sperm sacs’ and other forms of courtship feeding in crickets, katydids and their kin (Orthoptera: Ensifera). The evolution of mating systems in insects and arachnids 110:129

  • Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101

    Article  CAS  Google Scholar 

  • Gwynne DT, Bowen BJ, Codd CG (1984) The function of the katydid spermatophore and its role in fecundity and insemination (Orthoptera, Tettigoniidae). Aust J Zool 32:15–22

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  Google Scholar 

  • Lehmann GUC, Lehmann AW (2016) Material benefit of mating: the bushcricket spermatophylax as a fast uptake nuptial gift. Anim Behav 112:267–271

    Article  Google Scholar 

  • Lemons PR, Marshall TC, McCloskey SE, Sethi SA, Schmutz JA, Sedinger JS (2015) A likelihood-based approach for assessment of extra-pair paternity and conspecific brood parasitism in natural populations. Mol Ecol Resour 15:107–116

    Article  CAS  Google Scholar 

  • Lewis S, South A (2012) The evolution of animal nuptial gifts. Adv Stud Behav 44:53–97

    Article  Google Scholar 

  • Lewis SM, Vahed K, Koene JM, Engqvist L, Bussiere LF, Perry JC, Gwynne D, Lehmann GUC (2014) Emerging issues in the evolution of animal nuptial gifts. Biol Lett 10:20140336

    Article  Google Scholar 

  • Maxwell MR, Prokop P (2018) Fitness effects of nuptial gifts in the spider Pisaura mirabilis: examination under an alternative feeding regime. J Arachnol 46:404–412

    Article  Google Scholar 

  • Sakaluk SK (1984) Male crickets feed females to ensure complete sperm transfer. Science 223:609–610

    Article  CAS  Google Scholar 

  • Sakaluk SK, Campbell MTH, Clark AP, Chadwick-Johnson J, Keorpes PA (2004) Hemolymph loss during nuptial feeding constrains male mating success in sagebrush crickets. Behav Ecol 15:845–849

    Article  Google Scholar 

  • Shaw KL, Khine AH (2004) Courtship behavior in the Hawaiian cricket Laupala cerasina: males provide spermless spermatophores as nuptial gifts. Ethology 110:81–95

    Article  Google Scholar 

  • Simmons LW, Achmann R (2000) Microsatellite analysis of sperm-use patterns in the bushcricket Requena verticalis. Evolution 54:942–952

    Article  CAS  Google Scholar 

  • Simmons LW, Parker GA (1989) Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81:332–343

    Article  Google Scholar 

  • South A, Lewis SM (2012) Determinants of reproductive success across sequential episodes of sexual selection in a firefly. P Roy Soc B-Biol Sci 279:3201–3208

    Article  CAS  Google Scholar 

  • Svensson BG, Petersson E, Frisk M (1990) Nuptial gift size prolongs copulation duration in the dance fly Empis borealis. Ecol Entomol 15:225–229

    Article  Google Scholar 

  • Team RC (2014) R: a language and environment for statistical computing

  • Thornhill R (1976) Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). Am Nat 110:529–548

    Article  Google Scholar 

  • Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788

    Article  Google Scholar 

  • Turnell BR, Shaw KL (2015a) High opportunity for postcopulatory sexual selection under field conditions. Evolution 69:2094–2104

    Article  Google Scholar 

  • Turnell BR, Shaw KL (2015b) Polyandry and postcopulatory sexual selection in a wild population. Mol Ecol 24:6278–6288

    Article  Google Scholar 

  • Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev 73:43–78

    Article  Google Scholar 

  • Vahed K (2007) All that glisters is not gold: sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology 113:105–127

    Article  Google Scholar 

  • Wedell N (1991) Sperm competition selects for nuptial feeding in a bushcricket. Evolution 45:1975–1978

    Article  Google Scholar 

Download references

Acknowledgments

We thank Nick Ratterman for valuable comments on the early draft of this manuscript. Special thanks go to Stephen Parry, Françoise Vermeylen, Ziyi Song, and Bo Xu for helping with statistical analyses. Thanks are also due to the members of Shaw lab and of the NBB Lunch Bunch for their feedback.

Funding

This work was supported by the National Science Foundation (IOS-0843528 to KLS) and the China Scholarship Council (fellowship to QG).

Author information

Authors and Affiliations

  1. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA

    Qionghua Gao, Biz R. Turnell & Kerry L. Shaw

  2. State Key Laboratory of Crop Stress Biology for Arid Areas, Entomological Museum, Northwest A&F University, Yangling, Shaanxi, China

    Qionghua Gao & Baozhen Hua

  3. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences (CAS), Kunming, Yunnan, China

    Qionghua Gao

  4. Applied Zoology, Faculty Biology, Technische Universität Dresden, Dresden, Germany

    Biz R. Turnell

Authors
  1. Qionghua Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Biz R. Turnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baozhen Hua
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kerry L. Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QG and KLS conceived and designed the study; QG conducted the experiments; QG and BRT performed the statistical analysis. All authors wrote the manuscript.

Corresponding author

Correspondence to Qionghua Gao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. Wedell

Publisher’s note

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

Electronic Supplementary Material

Supplementary Figure S1

Micro production interval and macro production time in matings where the experimental female replaced a non-experimental female, compared to matings where the experimental female was present for the entire courtship (A, B); micro production interval and macro production time in females’ first vs. second matings (C, D). Micro production interval was calculated as the average number of minutes a male took to produce each of the final three micros; macro production time was calculated as the number of minutes before lights off that the macro was produced. (PDF 394 kb)

ESM 2

(XLSX 142 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Q., Turnell, B.R., Hua, B. et al. The effect of nuptial gift number on fertilization success in a Hawaiian swordtail cricket. Behav Ecol Sociobiol 73, 92 (2019). https://doi.org/10.1007/s00265-019-2705-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-019-2705-9

Keywords

Search

Navigation