Origin and evolution of animal eyes and light-guided behaviours

Nencki Open Lab Academy of Neuroscience – Faculty of Physics of the University of Warsaw
July 12, 2024

Gáspár Jékely

Centre for Organismal Studies, Heidelberg University

Charles Darwin set us a problem…


  • “To suppose that the eye, with all its inimitable contrivances […] could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree.”





  • “Yet reason tells me …”

… and gave us the solution




  • Gradual evolution by natural selection


  • Variation

  • Inheritance

  • Differential survival

Darwin’s ‘proto-eye’



“We can commence a series with an optic nerve merely coated with pigment”
Charles Darwin

Natural selection for a gradual increase in resolution



?

?









Lamprey

Human

Eagle

A pessimistic estimate of the time required for an eye to evolve

Proto-eyes still exist in marine plankton

Platynereis dumerilii









  • breeding culture
  • microinjection, transgenesis
  • neuron-specific promoters and antibodies
  • knock-out lines
  • neuronal connectome
  • neuronal activity imaging 😎

Platynereis dumerilii















Spawning
movie by Albrecht Fischer


Synchronously developing larvae

Proto-eyes still exist in marine plankton

trochophora larva

Direct sensory-motor coupling of eyes to cilia

pigment cup of eye

photoreceptor cell

The eyespots mediate phototaxis

Helical swimming, sensing and turning are tightly linked

Visual phototaxis with 2-pixel eyes

Whole-body volume EM of an entire Platynereis larva

The nervous system of the larva


~2,000 neurons

Synaptic connectome

Neural circuit of the visual eyes

Diversity of larval eyes

In quest of the origin of eyes

Ciliated zooplankton larvae

Coral larvae

In collaboration with Kirsty Wan (LSI Exeter) and Jamie Craggs (Horniman Museum)

Coral larvae

Emelie Brodrick


Hannah Laeverenz



Rebecca Poon & Kirsty Wan

Coral larvae react to light

Light-off induces contraction and ciliary arrest

A coral larval nerve net - simplest nervous system?

Hydrozoan larval phototaxis

Jeff Goddard, iNaturalist

GJ & Jürgen Berger

Clava multicornis

Field trips to explore marine plankton

Ischia, Sorgeto, 2024

Field trips lead to unexpected discoveries

with Alexandra Kerbl, Ischia May 31, 2024

What is this??

with Alexandra Kerbl, Ischia May 31, 2024

OMG

Egg plates and Müller’s larvae of polyclad flatworms

-> brought them back to Heidelberg

Planocera ceratommata

But are we sure…?

Müller’s larvae are phototactic and have three eyespots

Rhabdomeric and ciliary photoreceptors

Platynereis

Müller’s larva

Natural selection for a gradual increase in resolution


coral larvae, helical phototaxis
2-pixel eyes










Lamprey

Human

Eagle

Acknowledgements

  • Emelie Brodrick
  • Cyrielle Kaltenrieder
  • Réza Shahidi
  • Milena Marinkovic
  • Daniel Thiel
  • Sanja Jasek
  • Cameron Hird
  • Rebecca Turner
  • Luis A. Bezares-Calderón
  • Kei Jokura
  • Luis Yanez Guerra
  • Alexandra Kerbl

Former lab members

  • Albina Asadulina
  • James Beard
  • Markus Conzelmann
  • Nadine Randel
  • Philipp Bauknecht
  • Martin Gühmann
  • Cristina Pineiro-Lopez
  • Nobuo Ueda
  • Aurora Panzera
  • Csaba Verasztó
  • Elizabeth Williams