Novel gene expression patterns in hybrid embryos between species with different modes of development.

Abstract

Cross-species hybrids between eggs of the direct-developing sea urchin, Heliocidaris erythrogramma, and sperm from its congeneric indirect-developing species, Heliocidaris tuberculata, show restoration of features of the paternal feeding pluteus larva, including the gut, and pluteus spicular skeleton. Unlike other reported sea urchin cross-species hybrids, Heliocidaris hybrids express genes derived from both maternal and paternal species at high levels. Ectodermal cell types, which differ radically between the two parental species, are of intermediate form in the hybrids. Gene expression patterns in hybrid embryo tissues represent a number of combinations of parental gene expression patterns: genes that are not expressed in one paternal species, but are expressed in hybrids as in the expressing parent; genes that show additive expression patterns plus novel sites of expression; a gene that is misexpressed in the hybrids; and genes expressed identically in both parents and in hybrids. The results indicate that both conserved and novel gene regulatory interactions are present. Only one gene, CyIII actin, has lost cell-type-specific regulation in the hybrids. Hybrids thus reveal that disparate parental genomes, each with its own genic regulatory system, can produce in combination a novel gene expression entity with a unique ontogeny. This outcome may derive from conserved gene regulatory regions in downstream genes of both parental species responding in conserved ways to higher-level regulators that determine modular gene expression territories.