Maternal genetic effects in Astyanax cavefish development

Abstract

The role of maternal factors in the evolution of development is poorly understood. Here we describe the use of reciprocal hybridization between the surface dwelling (surface fish, SF) and cave dwelling (cavefish, CF) morphs of the teleost Astyanax mexicanus to investigate the roles of maternal genetic effects in cavefish development. Reciprocal hybridization, a procedure in which F1 hybrids are generated by fertilizing SF eggs with CF sperm (SF × CF hybrids) and CF eggs with SF sperm (CF × SF hybrids), revealed that the CF degenerative eye phenotype showed maternal genetic effects. The eyes of CF × SF hybrids resembled the degenerate eyes of CF in showing ventral reduction of the retina and corresponding displacement of the lens within the optic cup, a smaller lens and eyeball, more lens apoptosis, a smaller cartilaginous sclera, and lens-specific gene expression characteristics compared to SF × CF hybrids, which showed eye and lens gene expression phenotypes resembling SF. In contrast, reciprocal hybridization failed to support roles for maternal genetic effects in the CF regressive pigmentation phenotype or in CF constructive changes related to enhanced jaw development. Maternal transcripts encoded by the pou2f1b, runx2b, and axin1 genes, which are involved in determining ventral embryonic fates, were increased in unfertilized CF eggs. In contrast, maternal mRNAs encoded by the ß-catenin and syntabulin genes, which control dorsal embryonic fates, showed similar expression levels in unfertilized SF and CF eggs. Furthermore, maternal transcripts of a sonic hedgehog gene were detected in SF and CF eggs and early cleaving embryos. This study reveals that CF eye degeneration is controlled by changes in maternal factors produced during oogenesis and introduces A. mexicanus as a model system for studying the role of maternal changes in the evolution of development.

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

“…Regarding the eye phenotype, our results are 512 consistent with those of Ma et al, 2018 who examined maternal genetic effects in cavefish eye 513 development and degeneration: at embryonic stages (12-24hpf), eye size and shape do not seem to be 514 influenced by maternal factors. However, later larval lens apoptosis and eye regression appear to be under 515 maternal control (Ma et al, 2018). This fits with our finding that lens size at 24hpf differs between 516 reciprocal F1 hybrids.…”

“…Since early embryonic development is driven by maternal determinants present in the oocyte before 489 fecundation, the cross fertility in A. mexicanus species is a valuable tool to obtain information about the 490 18 contribution of maternal effect genes to phenotypic evolution (Ma et al, 2018). Our analyses in F1 491 reciprocal hybrids demonstrate that the modifications in cavefish gastrulation are fully dependent on 492 maternal factors.…”

“…However, overexpression of these two candidate genes by mRNA 500 injection in cavefish was not able to recapitulate the gastrulation phenotype observed in the surface fish. 501 Ma et al (2018) have also recently described increased pou2f1b, runx2b, and axin1 mRNA levels in 502 unfertilized cavefish eggs as compared to surface fish eggs. These genes also show differential expression 503 in our transcriptomic dataset.…”

“…The findings above showing earlier convergence, extension and internalization of mesodermal 264 cell populations in the cave morphs, together with differences in the spatio-temporal gene regulation in 265 tissues derived from the organizer, prompted the examination of precocious embryogenesis and the 266 investigation of maternal components. The inter-fertility between A. mexicanus morphotypes offers a 267 powerful system to study the potential contribution of these maternally-produced factors to phenotypic 268 evolution (Ma et al, 2018). We compared gastrulation progression in F1 hybrid embryos obtained from 269 fertilization of surface fish eggs with cavefish sperm (HybSF), and cavefish eggs with surface fish sperm 270 (HybCF) (Figure 6A).…”

Cavefish cope with environmental hypoxia by developing more erythrocytes and overexpression of hypoxia inducible genes

“…Therefore, increased erythropoiesis in the ALM suggests that a relative ventralization of hematopoietic development has evolved in cavefish compared to surface fish. This possibility is supported by the expansion of erythroid development in zebrafish by overexpression of the ventralizing factors bmp2b and bmp7 during the gastrula period (Lengerke et al, 2008) and is in line with evidence implicating evolutionary changes in dorsal-ventral axis determination based on modified Spemann organizer activity in cavefish embryos (Ren et al, 2018; Ma et al, 2018).…”