1. Evolutionary Biology
Download icon

Plasticity and evolutionary convergence in the locomotor skeleton of Greater Antillean Anolis lizards

  1. Nathalie Feiner  Is a corresponding author
  2. Illiam SC Jackson
  3. Kirke L Munch
  4. Reinder Radersma
  5. Tobias Uller
  1. Lund University, Sweden
  2. University of Tasmania, Australia
Research Article
  • Cited 4
  • Views 1,987
  • Annotations
Cite this article as: eLife 2020;9:e57468 doi: 10.7554/eLife.57468

Abstract

Plasticity can put evolution on repeat if development causes species to generate similar morphologies in similar environments. Anolis lizards offer the opportunity to put this role of developmental plasticity to the test. Following colonization of the four Greater Antillean islands, Anolis lizards independently and repeatedly evolved six ecomorphs adapted to manoeuvring different microhabitats. By quantifying the morphology of the locomotor skeleton of 95 species, we demonstrate that ecomorphs on different islands have diverged along similar trajectories. However, microhabitat-induced morphological plasticity differed between species and did not consistently improve individual locomotor performance. Consistent with this decoupling between morphological plasticity and locomotor performance, highly plastic features did not show greater evolvability, and plastic responses to microhabitat were poorly aligned with evolutionary divergence between ecomorphs. The locomotor skeleton of Anolis may have evolved within a subset of possible morphologies that are highly accessible through genetic change, enabling adaptive convergence independently of plasticity.

Data availability

Raw scans are available at Morphosource under the project ID P1059, title 'Anolis sp.' (see source data file 1 for individual DOIs). The morphological raw data is available in the source data file 2. Supplementary file 1 contains Extended Methods and supplementary tables.

The following data sets were generated

Article and author information

Author details

  1. Nathalie Feiner

    Biology, Lund University, Lund, Sweden
    For correspondence
    nathalie.feiner@biol.lu.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4648-6950
  2. Illiam SC Jackson

    Biology, Lund University, Lund, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7948-2860
  3. Kirke L Munch

    School of Biological Sciences, University of Tasmania, Hobart, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Reinder Radersma

    Biology, Lund University, Lund, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Tobias Uller

    Biology, Lund University, Lund, Sweden
    Competing interests
    The authors declare that no competing interests exist.

Funding

John Templeton Foundation (60501)

  • Tobias Uller

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

Ethics

Animal experimentation: The study was conducted according to the Lund University Local Ethical Review Process under the permit number Dnr M 31-16.

Reviewing Editor

  1. Diethard Tautz, Max-Planck Institute for Evolutionary Biology, Germany

Publication history

  1. Received: April 1, 2020
  2. Accepted: August 12, 2020
  3. Accepted Manuscript published: August 13, 2020 (version 1)
  4. Version of Record published: September 22, 2020 (version 2)

Copyright

© 2020, Feiner 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

  • 1,987
    Page views
  • 275
    Downloads
  • 4
    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)

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

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

Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Tetsuya Hisanaga et al.
    Research Article

    KNOX and BELL transcription factors regulate distinct steps of diploid development in plants. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrium patens and Arabidopsis thaliana, KNOX and BELL proteins function in meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here, we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that in C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.

    1. Developmental Biology
    2. Evolutionary Biology
    Tom Dierschke et al.
    Research Article Updated

    Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular chlorophyte alga Chlamydomonas, KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort Marchantia polymorpha, paternal (sperm) expression of three of five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of both MpKNOX1 and MpBELL34 mediate the haploid-to-diploid transition. Loss-of-function alleles of MpKNOX1 result in zygotic arrest, whereas a loss of either maternal or paternal MpBELL234 results in variable zygotic and early embryonic arrest. Expression of MpKNOX1 and MpBELL34 during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.