Abstract
BackgroundThe evolution of novel genes is thought to be a critical component of morphological innovation but few studies have explicitly examined the contribution of novel genes to the evolution of novel tissues. Nematosomes, the free-floating cellular masses that circulate through the body cavity of the sea anemone Nematostella vectensis, are the defining apomorphy of the genus Nematostella and are a useful model for understanding the evolution of novel tissues. Although many hypotheses have been proposed, the function of nematosomes is unknown. To gain insight into their putative function and to test hypotheses about the role of lineage-specific genes in the evolution of novel structures, we have re-examined the cellular and molecular biology of nematosomes.ResultsUsing behavioral assays, we demonstrate that nematosomes are capable of immobilizing live brine shrimp (Artemia salina) by discharging their abundant cnidocytes. Additionally, the ability of nematosomes to engulf fluorescently labeled bacteria (E. coli) reveals the presence of phagocytes in this tissue. Using RNA-Seq, we show that the gene expression profile of nematosomes is distinct from that of the tentacles and the mesenteries (their tissue of origin) and, further, that nematosomes (a Nematostella-specific tissue) are enriched in Nematostella-specific genes.ConclusionsDespite the small number of cell types they contain, nematosomes are distinct among tissues, both functionally and molecularly. We provide the first evidence that nematosomes comprise part of the innate immune system in N. vectensis, and suggest that this tissue is potentially an important place to look for genes associated with pathogen stress. Finally, we demonstrate that Nematostella-specific genes comprise a significant proportion of the differentially expressed genes in all three of the tissues we examined and may play an important role in novel cell functions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0683-3) contains supplementary material, which is available to authorized users.
Highlights
The evolution of novel genes is thought to be a critical component of morphological innovation but few studies have explicitly examined the contribution of novel genes to the evolution of novel tissues
Nematosome development Nematosomes first appear in the body cavity of N. vectensis near the onset of reproductive maturity, after development of the ciliated tracts of the mesenteries
We demonstrate that nematosomes bud from regions of the mesenteries that are already rich in mature cnidocyte capsules (Fig. 2a, b) and the presence of cells in S-phase suggests that the process of budding involves proliferation of the cells around the mature cnidocytes
Summary
The evolution of novel genes is thought to be a critical component of morphological innovation but few studies have explicitly examined the contribution of novel genes to the evolution of novel tissues. To gain insight into their putative function and to test hypotheses about the role of lineage-specific genes in the evolution of novel structures, we have re-examined the cellular and molecular biology of nematosomes. Several additional studies provide support for novel/ taxonomically-restricted genes in generating lineagespecific morphological features (e.g., [9,10,11,12,13]) but surprisingly, most of these studies have identified only few novel genes to be contributing to the novel morphological trait of interest Despite their focus on the role of novel genes in the evolution of a novel trait, these studies reveal that the majority of the genes involved in evolutionary innovation are conserved. Only few studies have explicitly examined the abundance and distribution of novel genes across cell/ tissue types [12, 16, 17] and their results regarding the importance of novel genes have been conflicting
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