Maternally regulated gastrulation as a source of variation contributing to cavefish forebrain evolution

Abstract

Sequential developmental events, starting from the moment of fertilization, are crucial for the acquisition of animal body plan. Subtle modifications in such early events are likely to have major impacts in later morphogenesis, bringing along morphological diversification. Here, comparing the blind cave and the surface morphotypes of Astyanax mexicanus fish, we found heterochronies during gastrulation that produce organizer and axial mesoderm tissues with different properties (including differences in the expression of dkk1b) that may have contributed to cavefish brain evolution. These variations observed during gastrulation depend fully on maternal factors. The developmental evolution of retinal morphogenesis and hypothalamic patterning are among those traits that retained significant maternal influence at larval stages. Transcriptomic analysis of fertilized eggs from both morphotypes and reciprocal F1 hybrids showed a strong and specific maternal signature. Our work strongly suggests that maternal effect genes and developmental heterochronies that occur during gastrulation have impacted morphological brain change during cavefish evolution.

Astyanax surface and cave fish morphs

“…4 c)—the fertilization of cavefish eggs with surface fish sperm and vice versa—provides a novel way to distinguish between traits evolved under maternal or zygotic control [ 32 ]. While most trait changes have been considered to originate zygotically, degeneration of the lens and retina, temporal differences in gastrulation, and some changes in the brain are under direct maternal control, and thus have consequences extending into the larval period [ 32 , 33 ]. The trait changes that occur via maternal effects could define early control points that broadly impact many downstream events in cavefish development.…”

Pescoids and chimeras to probe early evo-devo in the fishAstyanax mexicanus

“…Intermorph grafting will shed light on the cell autonomy and the effect of the embryonic signaling environment on previously described heterochronies, heterotopies and differences of gene expression levels of during development of Astyanax morphs (Hinaux et al, 2016;Pottin et al, 2011;Torres-Paz et al, 2019;Yamamoto et al, 2004). The combination of these grafting methods with the use of transgenic reporter lines such as the cavefish and surface fish zic1:GFP lines (Devos et al, 2019), will allow the detailed investigation of intrinsic and extrinsic factors implicated in eye specification and degeneration.…”

“…Symmetry breaking, axis elongation and neural specification occur despite the absence of extraembryonic signaling (Fulton et al, 2020;Schauer et al, 2020). In fish, these events are controlled maternally (Marlow, 2020;Solnica-Krezel, 2020) and A. mexicanus with its two morphotypes has become an excellent model to challenge the role of maternal determinants in embryogenesis (Ma et al, 2020(Ma et al, , 2018Torres-Paz et al, 2019).…”

“…Most of the morphological differences observed in the nervous system of A. mexicanus morphotypes have an early embryonic origin (Hinaux et al, 2016;Pottin et al, 2011;Rétaux et al, 2016;Yamamoto & Jeffery, 2000). In fact, recent evidence has shown that maternal determinants, present in the oocyte before fertilization and before zygotic developmental programs are initiated, have an important contribution to later phenotypes (Ma et al, 2020, Ma et al, 2018Torres-Paz et al, 2019). Indeed, any differential composition of maternal determinants in the eggs is susceptible to lead to changes in early developmental events, such as activation of the zygotic genome, embryonic patterning and establishment of signaling centers, thus affecting later ontogenetic processes.…”

Pescoids and Chimeras to Probe Early Evo-Devo in the Fish Astyanax mexicanus

“…Most of the morphological differences observed in the nervous system of A. mexicanus morphotypes have an early embryonic origin (Yamamoto and Jeffery, 2000;Pottin et al, 2011;Hinaux et al, 2016;Rétaux et al, 2016). In fact, recent evidence has shown that maternal determinants, present in the oocyte before fertilization and before zygotic developmental programs are initiated, have an important contribution to later phenotypes (Ma et al, 2018(Ma et al, , 2020Torres-Paz et al, 2019). Indeed, any differential composition of maternal determinants in the eggs is susceptible to lead to changes in early developmental events, such as activation of the zygotic genome, embryonic patterning and establishment of signaling centers, thus affecting later ontogenetic processes.…”