2018bioRxiv (Cold Spring Harbor Laboratory)Open access

High temperature limits on developmental canalization in the ascidian Ciona intestinalis

Steven Q. Irvine, Katherine B. McNulty, Evelyn M. Siler, Rose E. Jacobson

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Abstract

The normal embryogenesis of marine animals is typically confined to a species-specific range of temperatures. Within that temperature range development results in a consistent, or canalized, phenotype, whereas above and below the range abnormal phenotypes are produced. This study reveals an abrupt high temperature limit, occurring over a 1-2C range, for normal embryonic development in C. intestinalis. Above that threshold morphological abnormalities in the notochord and other organs are observed, beginning with cleavage and gastrula stages, and becoming more pronounced as embryogenesis proceeds. However, even in highly morphologically abnormal temperature disrupted (TD) embryos, cell type specification, including muscle, endoderm, notochord, and sensory pigment cells is accomplished. An explanation for this finding is that in C. intestinalis cell type specification occurs relatively early in embryogenesis, due to cleavage stage segregation of maternal cytoplasmic determinants and short-range cell interactions, which are largely intact in TD embryos. On the other hand, morphogenesis of the notochord and other structures is dependent on precise cell movement and shape changes after the gastrula stage, which appear to be disrupted above the high temperature threshold. These findings have implications for the relationship between ecology and reproduction in C. intestinalis. More broadly they point to mechanisms behind canalization in animals, such as ascidians, characterized by early, largely autonomous, cell type specification.

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What this paper is about

The normal embryogenesis of marine animals is typically confined to a species-specific range of temperatures. Within that temperature range development results in a consistent, or canalized, phenotype, whereas above and below the range abnormal phenotypes are produced. This study reveals an abrupt high temperature limit, occurring over a 1-2C range, for normal embryonic development in C. intestinalis. Above that threshold morphological abnormalities in the notochord and other organs are observed, beginning with cleavage and gastrula stages, and becoming more pronounced as embryogenesis proceeds. However, even in highly morphologically abnormal temperature disrupted (TD) embryos, cell type specification, including muscle, endoderm, notochord, and sensory pigment cells is accomplished. An explanation for this finding is that in C. intestinalis cell type specification occurs relatively early in embryogenesis, due to cleavage stage segregation of maternal cytoplasmic determinants and short-range cell interactions, which are largely intact in TD embryos. On the other hand, morphogenesis of the notochord and other structures is dependent on precise cell movement and shape changes after the gastrula stage, which appear to be disrupted above the high temperature threshold. These findings have implications for the relationship between ecology and reproduction in C. intestinalis. More broadly they point to mechanisms behind canalization in animals, such as ascidians, characterized by early, largely autonomous, cell type specification.

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Available abstract

The normal embryogenesis of marine animals is typically confined to a species-specific range of temperatures. Within that temperature range development results in a consistent, or canalized, phenotype, whereas above and below the range abnormal phenotypes are produced. This study reveals an abrupt high temperature limit, occurring over a 1-2C range, for normal embryonic development in C. intestinalis. Above that threshold morphological abnormalities in the notochord and other organs are observed, beginning with cleavage and gastrula stages, and becoming more pronounced as embryogenesis proceeds. However, even in highly morphologically abnormal temperature disrupted (TD) embryos, cell type specification, including muscle, endoderm, notochord, and sensory pigment cells is accomplished. An explanation for this finding is that in C. intestinalis cell type specification occurs relatively early in embryogenesis, due to cleavage stage segregation of maternal cytoplasmic determinants and short-range cell interactions, which are largely intact in TD embryos. On the other hand, morphogenesis of the notochord and other structures is dependent on precise cell movement and shape changes after the gastrula stage, which appear to be disrupted above the high temperature threshold. These findings have implications for the relationship between ecology and reproduction in C. intestinalis. More broadly they point to mechanisms behind canalization in animals, such as ascidians, characterized by early, largely autonomous, cell type specification.

Key concepts: Notochord, Ciona intestinalis, Biology, Embryogenesis, Gastrulation, Morphogenesis, Endoderm, Embryo

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