Divergent sensory investment mirrors potential speciation via niche partitioning across Drosophila

  1. Ian W Keesey  Is a corresponding author
  2. Veit Grabe
  3. Markus Knaden  Is a corresponding author
  4. Bill S Hansson  Is a corresponding author
  1. Max Planck Institute for Chemical Ecology, Germany

Abstract

The examination of phylogenetic and phenotypic characteristics of the nervous system, such as behavior and neuroanatomy, can be utilized as a means to assess speciation. Recent studies have proposed a fundamental tradeoff between two sensory organs, the eye and the antenna. However, the identification of ecological mechanisms for this observed tradeoff have not been firmly established. Our current study examines several monophyletic species within the obscura group, and asserts that despite their close relatedness and overlapping ecology, they deviate strongly in both visual and olfactory investment. We contend that both courtship and microhabitat preferences support the observed inverse variation in these sensory traits. Here, this variation in visual and olfactory investment seems to provide relaxed competition, a process by which similar species can use a shared environment differently and in ways that help them coexist. Moreover, that behavioral separation according to light gradients occurs first, and subsequently, courtship deviations arise.

Data availability

All data supporting the findings of this study, including methodology, display examples, raw confocal images and z-stack scans, statistical assessments, courtship videos, as well as other supplementary materials are all available with the online version of this publication. An additional, online data depository also contains raw data from this publication, and this material can be accessed via EDMOND, the Open Access Data Repository of the Max Planck Society (MPG):https://dx.doi.org/10.17617/3.3v

The following data sets were generated

Article and author information

Author details

  1. Ian W Keesey

    Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    ikeesey@ice.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3339-7249
  2. Veit Grabe

    Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0736-2771
  3. Markus Knaden

    Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    mknaden@ice.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6710-1071
  4. Bill S Hansson

    Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    hansson@ice.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4811-1223

Funding

Max-Planck-Gesellschaft (Open-access funding)

  • Ian W Keesey
  • Veit Grabe
  • Markus Knaden
  • Bill S Hansson

The funding organization had no role in the study design, data collection, interpretation, nor the decision to submit the work for publication. The authors declare no competing interests.

Reviewing Editor

  1. Virginie Courtier-Orgogozo, Université Paris-Diderot CNRS, France

Version history

  1. Received: March 17, 2020
  2. Accepted: June 30, 2020
  3. Accepted Manuscript published: June 30, 2020 (version 1)
  4. Version of Record published: August 4, 2020 (version 2)

Copyright

© 2020, Keesey 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

  • 2,685
    Page views
  • 455
    Downloads
  • 10
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Ian W Keesey
  2. Veit Grabe
  3. Markus Knaden
  4. Bill S Hansson
(2020)
Divergent sensory investment mirrors potential speciation via niche partitioning across Drosophila
eLife 9:e57008.
https://doi.org/10.7554/eLife.57008

Share this article

https://doi.org/10.7554/eLife.57008

Further reading

    1. Evolutionary Biology
    Alexei V Tkachenko, Sergei Maslov
    Research Article

    Life as we know it relies on the interplay between catalytic activity and information processing carried out by biological polymers. Here we present a plausible pathway by which a pool of prebiotic information-coding oligomers could acquire an early catalytic function, namely sequence-specific cleavage activity. Starting with a system capable of non-enzymatic templated replication, we demonstrate that even non-catalyzed spontaneous cleavage would promote proliferation by generating short fragments that act as primers. Furthermore, we show that catalytic cleavage function can naturally emerge and proliferate in this system. Specifically, a cooperative catalytic network with four subpopulations of oligomers is selected by the evolution in competition with chains lacking catalytic activity. The cooperative system emerges through the functional differentiation of oligomers into catalysts and their substrates. The model is inspired by the structure of the hammerhead RNA enzyme as well as other DNA- and RNA-based enzymes with cleavage activity that readily emerge through natural or artificial selection. We identify the conditions necessary for the emergence of the cooperative catalytic network. In particular, we show that it requires the catalytic rate enhancement over the spontaneous cleavage rate to be at least 102–103, a factor consistent with the existing experiments. The evolutionary pressure leads to a further increase in catalytic efficiency. The presented mechanism provides an escape route from a relatively simple pairwise replication of oligomers toward a more complex behavior involving catalytic function. This provides a bridge between the information-first origin of life scenarios and the paradigm of autocatalytic sets and hypercycles, albeit based on cleavage rather than synthesis of reactants.

    1. Cell Biology
    2. Evolutionary Biology
    Jonathan E Phillips, Duojia Pan
    Research Advance

    The genomes of close unicellular relatives of animals encode orthologs of many genes that regulate animal development. However, little is known about the function of such genes in unicellular organisms or the evolutionary process by which these genes came to function in multicellular development. The Hippo pathway, which regulates cell proliferation and tissue size in animals, is present in some of the closest unicellular relatives of animals, including the amoeboid organism Capsaspora owczarzaki. We previously showed that the Capsaspora ortholog of the Hippo pathway nuclear effector Yorkie/YAP/TAZ (coYki) regulates actin dynamics and the three-dimensional morphology of Capsaspora cell aggregates, but is dispensable for cell proliferation control (Phillips et al., 2022). However, the function of upstream Hippo pathway components, and whether and how they regulate coYki in Capsaspora, remained unknown. Here, we analyze the function of the upstream Hippo pathway kinases coHpo and coWts in Capsaspora by generating mutant lines for each gene. Loss of either kinase results in increased nuclear localization of coYki, indicating an ancient, premetazoan origin of this Hippo pathway regulatory mechanism. Strikingly, we find that loss of either kinase causes a contractile cell behavior and increased density of cell packing within Capsaspora aggregates. We further show that this increased cell density is not due to differences in proliferation, but rather actomyosin-dependent changes in the multicellular architecture of aggregates. Given its well-established role in cell density-regulated proliferation in animals, the increased density of cell packing in coHpo and coWts mutants suggests a shared and possibly ancient and conserved function of the Hippo pathway in cell density control. Together, these results implicate cytoskeletal regulation but not proliferation as an ancestral function of the Hippo pathway kinase cascade and uncover a novel role for Hippo signaling in regulating cell density in a proliferation-independent manner.