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

  • 1,463
    views
  • 260
    downloads
  • 8
    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. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Evolutionary Biology
    Ljiljana Mihajlovic, Bharat Ravi Iyengar ... Yolanda Schaerli
    Research Article

    Gene duplication drives evolution by providing raw material for proteins with novel functions. An influential hypothesis by Ohno (1970) posits that gene duplication helps genes tolerate new mutations and thus facilitates the evolution of new phenotypes. Competing hypotheses argue that deleterious mutations will usually inactivate gene duplicates too rapidly for Ohno’s hypothesis to work. We experimentally tested Ohno’s hypothesis by evolving one or exactly two copies of a gene encoding a fluorescent protein in Escherichia coli through several rounds of mutation and selection. We analyzed the genotypic and phenotypic evolutionary dynamics of the evolving populations through high-throughput DNA sequencing, biochemical assays, and engineering of selected variants. In support of Ohno’s hypothesis, populations carrying two gene copies displayed higher mutational robustness than those carrying a single gene copy. Consequently, the double-copy populations experienced relaxed purifying selection, evolved higher phenotypic and genetic diversity, carried more mutations and accumulated combinations of key beneficial mutations earlier. However, their phenotypic evolution was not accelerated, possibly because one gene copy rapidly became inactivated by deleterious mutations. Our work provides an experimental platform to test models of evolution by gene duplication, and it supports alternatives to Ohno’s hypothesis that point to the importance of gene dosage.