Evolution of sexual conflict in scorpionflies

  1. Agnieszka Soszyńska-Maj  Is a corresponding author
  2. Ewa Krzemińska  Is a corresponding author
  3. Ricardo Pérez-de la Fuente
  4. Ji-Shen Wang
  5. Krzysztof Szpila
  6. Kornelia Skibińska
  7. Katarzyna Kopeć
  8. Wieslaw Krzemiński
  1. University of Lodz, Poland
  2. Polish Academy of Sciences, Poland
  3. Oxford University, United Kingdom
  4. Dali University, China
  5. Nicolaus Copernicus University, Poland

Abstract

Sexual conflict - opposite reproductive/genetic interests between sexes - can be a significant driver of insect evolution. Scorpionflies (Insecta: Mecoptera) are models in sexual conflict research due to their large variety of mating practices, including coercive behaviour and nuptial gift provisioning. However, the role of palaeontology in sexual conflict studies remains negligible, namely due to the paucity of well-preserved fossils. Here we describe three male scorpionflies from Cretaceous and Eocene ambers. The structure of notal and postnotal organs is analysed in extant and extinct forms; a depression below the base of the notal organ in different panorpid species spatially matches the anterior fold of the female's wing. Based on disparate abdominal configurations and correlations in extant relatives, we posit that each new fossil taxon had a different mating approach along a nuptial gifting-coercive spectrum. The Eocene specimen possesses extreme female clamping abdominal armature, suggesting a degree of sexual coercion greater than in any other known scorpionfly, extinct or extant. The fossil record of abdominal modifications in male scorpionflies documents a relatively late evolution (Eocene) of long notal organs indicating oppressive behaviour toward a female during mating. Our findings reveal a wider array of mating-related morphological specialisations among extinct Panorpoidea, likely reflecting more diversified past mating strategies and behaviours in this group, and represent first steps towards gaining a deep-time perspective on the evolution of sexual conflict over mating among insects.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional information related to this paper may be requested from the authors. Investigated fossils are available in public institutions: at the Institutional Collection from the El Soplao Cave (Government of Cantabria), Celis, Cantabria, N Spain and at the collection from the Museum of the Institute of Systematics and Evolution of Animals (ISEA), Polish Academy of Sciences (PAS), Kraków, Poland.

Article and author information

Author details

  1. Agnieszka Soszyńska-Maj

    Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Lodz, Poland
    For correspondence
    agnieszka.soszynska@biol.uni.lodz.pl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2661-6685
  2. Ewa Krzemińska

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland
    For correspondence
    ekrzeminska9@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  3. Ricardo Pérez-de la Fuente

    Museum of Natural History, Oxford University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2830-2639
  4. Ji-Shen Wang

    College of Agriculture and Biological Sciences, Dali University, Dali, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0188-0228
  5. Krzysztof Szpila

    Department of Ecology and Biogeography, Nicolaus Copernicus University, Torun, Poland
    Competing interests
    The authors declare that no competing interests exist.
  6. Kornelia Skibińska

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland
    Competing interests
    The authors declare that no competing interests exist.
  7. Katarzyna Kopeć

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland
    Competing interests
    The authors declare that no competing interests exist.
  8. Wieslaw Krzemiński

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Center, Poland (2013/09/B/NZ8/03270)

  • Agnieszka Soszyńska-Maj
  • Katarzyna Kopeć
  • Wieslaw Krzemiński

National Science Center, Poland (2016/23/B/NZ8/00936)

  • Agnieszka Soszyńska-Maj
  • Ewa Krzemińska
  • Kornelia Skibińska
  • Katarzyna Kopeć
  • Wieslaw Krzemiński

AEI/FEDER, UE (CGL2017-84419)

  • Ricardo Pérez-de la Fuente

High-level Talents, Dali University (KY2096124040)

  • Ji-Shen Wang

National Science Center, Poland (2018/31/B/NZ8/02113)

  • Krzysztof Szpila

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2022, Soszyńska-Maj et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,432
    views
  • 259
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Agnieszka Soszyńska-Maj
  2. Ewa Krzemińska
  3. Ricardo Pérez-de la Fuente
  4. Ji-Shen Wang
  5. Krzysztof Szpila
  6. Kornelia Skibińska
  7. Katarzyna Kopeć
  8. Wieslaw Krzemiński
(2022)
Evolution of sexual conflict in scorpionflies
eLife 11:e70508.
https://doi.org/10.7554/eLife.70508

Share this article

https://doi.org/10.7554/eLife.70508

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.

    1. Developmental Biology
    2. Evolutionary Biology
    Hope M Healey, Hayden B Penn ... William A Cresko
    Research Article

    Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provided the opportunity for detailed genetic analyses. We created a single-cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined the spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting that derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how the novelties of these fish evolved.