Search for: All records

Changes in developmental gene regulatory networks (dGRNs) underlie much of the diversity of life, but the evolutionary mechanisms that operate on interactions with these networks remain poorly understood. Closely related species with extreme phenotypic divergence provide a valuable window into the genetic and molecular basis for changes in dGRNs and their relationship to adaptive changes in organismal traits. Here we analyze genomes, epigenomes, and transcriptomes during early development in two sea urchin species in the genus Heliocidaris that exhibit highly divergent life histories and in an outgroup species. Signatures of positive selection and changes in chromatin status within putative gene regulatory elements are both enriched on the branch leading to the derived life history, and particularly so near core dGRN genes; in contrast, positive selection within protein-coding regions have at most a modest enrichment in branch and function. Single-cell transcriptomes reveal a dramatic delay in cell fate specification in the derived state, which also has far fewer open chromatin regions, especially near dGRN genes with conserved roles in cell fate specification. Experimentally perturbing the function of three key transcription factors reveals profound evolutionary changes in the earliest events that pattern the embryo, disrupting regulatory interactions previously conserved for ~225 million years. Together, these results demonstrate that natural selection can rapidly reshape developmental gene expression on a broad scale when selective regimes abruptly change and that even highly conserved dGRNs and patterning mechanisms in the early embryo remain evolvable under appropriate ecological circumstances. 

Animal gastrointestinal tracts harbor a microbiome that is integral to host function, yet species from diverse phyla have evolved a reduced digestive system or lost it completely. Whether such changes are associated with alterations in the diversity and/or abundance of the microbiome remains an untested hypothesis in evolutionary symbiosis. Here, using the life history transition from planktotrophy (feeding) to lecithotrophy (nonfeeding) in the sea urchinHeliocidaris, we demonstrate that the lack of a functional gut corresponds with a reduction in microbial community diversity and abundance as well as the association with a diet-specific microbiome. We also determine that the lecithotroph vertically transmits a Rickettsiales that may complement host nutrition through amino acid biosynthesis and influence host reproduction. Our results indicate that the evolutionary loss of a functional gut correlates with a reduction in the microbiome and the association with an endosymbiont. Symbiotic transitions can therefore accompany life history transitions in the evolution of developmental strategies.

 

Ocean acidification (OA) from seawater uptake of rising carbon dioxide emissions impairs development in marine invertebrates, particularly in calcifying species. Plasticity in gene expression is thought to mediate many of these physiological effects, but how these responses change across life history stages remains unclear. The abbreviated lecithotrophic development of the sea urchinHeliocidaris erythrogrammaprovides a valuable opportunity to analyse gene expression responses across a wide range of life history stages, including the benthic, post‐metamorphic juvenile. We measured the transcriptional response to OA inH. erythrogrammaat three stages of the life cycle (embryo, larva, and juvenile) in a controlled breeding design. The results reveal a broad range of strikingly stage‐specific impacts of OA on transcription, including changes in the number and identity of affected genes; the magnitude, sign, and variance of their expression response; and the developmental trajectory of expression. The impact of OA on transcription was notably modest in relation to gene expression changes during unperturbed development and much smaller than genetic contributions from parentage. The latter result suggests that natural populations may provide an extensive genetic reservoir of resilience to OA. Taken together, these results highlight the complexity of the molecular response to OA, its substantial life history stage specificity, and the importance of contextualizing the transcriptional response to pH stress in light of normal development and standing genetic variation to better understand the capacity for marine invertebrates to adapt to OA.