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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins.

ABSTRACT: Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ?90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirect-developing euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell type-biased alterations.

SUBMITTER: Erkenbrack EM

PROVIDER: S-EPMC5135324 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins.

Erkenbrack Eric M EM

Proceedings of the National Academy of Sciences of the United States of America 20161103 46

Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea ur ...[more]

PMID: 27810959

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Project description:The massive die-off of the long-spined sea urchin, Diadema antillarum, a significant reef grazer, in the mid 1980s was followed by phase shifts from coral dominated to macroalgae dominated reefs in the Caribbean. While Diadema populations have recovered in some reefs with concomitant increases in coral cover, the additional threat of increasing temperatures due to global climate change has not been investigated in adult sea urchins. In this study, I measured acute thermal tolerance of D. antillarum and that of a sympatric sea urchin not associated with coral cover, Echinometra lucunter, over winter, spring, and summer, thus exposing them to substantial natural thermal variation. Animals were taken from the wild and placed in laboratory tanks in room temperature water (∼22 °C) that was then heated at 0.16-0.3 °C min(-1) and the righting behavior of individual sea urchins was recorded. I measured both the temperature at which the animal could no longer right itself (T LoR) and the righting time at temperatures below the T LoR. In all seasons, D. antillarum exhibited a higher mean T LoR than E. lucunter. The mean T LoR of each species increased with increasing environmental temperature revealing that both species acclimatize to seasonal changes in temperatures. The righting times of D. antillarum were much shorter than those of E. lucunter. The longer relative spine length of Diadema compared to that of Echinometra may contribute to their shorter righting times, but does not explain their higher T LoR. The thermal safety margin (the difference between the mean collection temperature and the mean T LoR) was between 3.07-3.66 °C for Echinometra and 3.79-5.67 °C for Diadema. While these thermal safety margins exceed present day temperatures, they are modest compared to those of temperate marine invertebrates. If sea temperatures increase more rapidly than can be accommodated by the sea urchins (either by genetic adaptation, phenotypic plasticity, or both), this will have important consequences for the structure of coral reefs.

Project description:BackgroundStrongylocentrotid sea urchins have a long tradition as model organisms for studying many fundamental processes in biology including fertilization, embryology, development and genome regulation but the phylogenetic relationships of the group remain largely unresolved. Although the differing isolating mechanisms of vicariance and rapidly evolving gamete recognition proteins have been proposed, a stable and robust phylogeny is unavailable.ResultsWe used a phylogenomic approach with mitochondrial and nuclear genes taking advantage of the whole-genome sequencing of nine species in the group to establish a stable (i.e. concordance in tree topology among multiple lies of evidence) and robust (i.e. high nodal support) phylogenetic hypothesis for the family Strongylocentrotidae. We generated eight draft mitochondrial genome assemblies and obtained 13 complete mitochondrial genes for each species. Consistent with previous studies, mitochondrial sequences failed to provide a reliable phylogeny. In contrast, we obtained a very well-supported phylogeny from 2301 nuclear genes without evidence of positive Darwinian selection both from the majority of most-likely gene trees and the concatenated fourfold degenerate sites: ((P. depressus, (M. nudus, M. franciscanus), (H. pulcherrimus, (S. purpuratus, (S. fragilis, (S. pallidus, (S. droebachiensis, S. intermedius)). This phylogeny was consistent with a single invasion of deep-water environments followed by a holarctic expansion by Strongylocentrotus. Divergence times for each species estimated with reference to the divergence times between the two major clades of the group suggest a correspondence in the timing with the opening of the Bering Strait and the invasion of the holarctic regions.ConclusionsNuclear genome data contains phylogenetic signal informative for understanding the evolutionary history of this group. However, mitochondrial genome data does not. Vicariance can explain major patterns observed in the phylogeny. Other isolating mechanisms are appropriate to explore in this system to help explain divergence patterns not well supported by vicariance, such as the effects of rapidly evolving gamete recognition proteins on isolating populations. Our findings of a stable and robust phylogeny, with the increase in mitochondrial and nuclear comparative genomic data, provide a system in which we can enhance our understanding of molecular evolution and adaptation in this group of sea urchins.

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins.

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins.

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