From light to darkness: evolutionary history of the photosensory system in planarians (Platyhelminthes, Tricladida)

Author(s)

Luiza de Oliveira Saad

• Document type: Doctoral Thesis
• Press: São Paulo.
• Institution: Universidade de São Paulo (USP). Instituto de Biociências (IBIOC/SB)
• Defense date: 2022-11-04

Examining board members

Federico David Brown Almeida; Patrícia Neiva Coelho Schneider; Mansi Srivastava; Chao Yun Irene Yan

• Advisor: Federico David Brown Almeida

Abstract

To understand the evolution of form and diversification in the photosensory systems it is necessary to study the function, development, cell morphology, and environment context of eyes in different animals. Comparative studies of flatworms in the order Tricladida represent a good animal group to address questions about how eye structures evolved and diversified because Tricladida can occupy different environments, and display visual characters associated with it, offering an opportunity to study adaptations to the different environmental conditions. Indeed, our comparative review studies demonstrate that species of the order Tricladida inhabit different environments, and display diverse eye phenotypes accommodated to their ecological demands. Several eye-related key innovations found in Tricladida can be used to study how the environment shapes the diversification and evolution of traits, such as the presence of lensed eyes only found in marine species, or trilobated eyes only present in terrestrial species. Furthermore, Tricladida eyes have been repeatedly lost in different cave species, and therefore allow comparative studies related with the evolution of convergent traits associated to living in the dark. In order to elucidate the developmental and molecular changes that took place during the evolution of the rudimentary eyes found in a cave planarian, we carried detailed analyses of eye development in the cave planarian Girardia multidiverticulata. We found that G. multidiverticulata, which were initially described to be an eyeless species, actually retain small and functional, rudimentary eyes. With some exceptions during late differentiation of eye cells, these cave planarians expressed orthologs of conserved transcription factors known to be important for eye formation in surface planarians. However, differential expression analyses revealed changes in expression levels of genes involved eye function and pigment formation when compared with surface species. We found that the reduction in eye-cell number in cave planarians is caused by a decreased rate of stem cell fate specification to eye progenitors. This led to a lower rate of new eye cell differentiation during homeostasis, and also during regeneration. By contrast, formation of other tissues, including other neurons in the brain, was comparable between the cave and surface species. Additionally, two different morphotypes within the cave population exist and show heritable differences in eyes: one has small, pigmented rudimentary eyes (discernible eyes) and the other has unpigmented small eyes that are non-discernible by light microscopy. Aside for the pigmentation differences between the two Girardia multidiverticulata morphotypes presented changes in expression levels of genes. The existence of two different stages of eye trait regression within the same population, combined with reduced but not absent stem cell fate specification into eye cells, and altered eye gene expression suggest this species represents an intermediate stage of trait adaptation to the subterranean environment. We conclude that Girardia multidiverticulata represents a novel mode of evolutionary trait loss, in which change to the rate of stem cell fate selection in an adult setting result in reduction in organ size. These results further our understanding of the different mechanisms responsible for trait loss, which are essential to understand the evolution of eye loss. (AU)

• FAPESP's process: 18/06418-0 - From light to darkness: evolutionary history of the photosensory system in planarians (Platyhelminthes, Tricladida)
• Grantee: Luiza de Oliveira Saad
• Support Opportunities: Scholarships in Brazil - Doctorate