Carry‐over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina
Abstract
The drastic shift from pelagic larvae to benthic adult form that occurs during marine invertebrate metamorphosis is often induced by intimate interactions between settling larvae and their benthic environment. Larval experience prior to and during metamorphosis can significantly affect adult fitness, but it is presently unknown whether the exact nature of the inductive cue is an experience that matters, or by what mechanism such carry‐over effects are mediated. Here we test for carry‐over effects of the specific nature of inductive cues on gene expression in metamorphosing postlarvae of the tropical abalone, Haliotis asinina. Postlarvae induced by three different species of coralline algae all successfully undergo metamorphosis, yet the expression profiles of 11 of 17 metamorphosis‐related genes differ according to which species of algae the larvae settled upon. Significantly, several genes continue to be differentially expressed for at least 40 h after removal of the algae from the postlarvae, clearly demonstrating a carry‐over effect of inductive cue on gene expression. We observe a carryover effect in several genes with varying functions and spatial expression patterns, indicating that each algal species impacts global gene expression in a unique manner. These data unexpectedly reveal that transcriptional modulation of metamorphosis‐related genes is contingent upon the precise composition of the benthic microenvironment experienced directly at induction of settlement, and highlight transcription as a mechanism that can mediate between larval and postlarval experiences. For new recruits into an abalone population, metamorphosis clearly does not represent a new transcriptional beginning.
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This environmental-cue-triggered metamorphosis pattern is seen across corals, annelids, molluscs, ascidians and others.
“This pattern is seen across corals, annelids, molluscs, ascidians and others [73-77].”
From An option space for early neural evolution (2015) · cites this paper as [74]
Cites
Pfaffl, M. W. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.9.e36 · Cited by 7,377 · see citing works
Developmental Plasticity and Evolution
West-Eberhard, M. J. (2003) · doi:10.1093/oso/9780195122343.001.0001 · Cited by 6,115 · see citing works
Ghalambor, C. K., McKay, J., Carroll, S. P., & Reznick, D. N. (2007) · Functional Ecology · doi:10.1111/j.1365-2435.2007.01283.x · Cited by 3,620 · see citing works
Nutritional Control of Reproductive Status in Honeybees via DNA Methylation
Kucharski, R., Maleszka, J., Forêt, S., & Maleszka, R. (2008) · Science · doi:10.1126/science.1153069 · Cited by 1,146 · see citing works
The segment polarity network is a robust developmental module
von Dassow, G., Meir, E., Munro, E. M., & Odell, G. M. (2000) · Nature · doi:10.1038/35018085 · Cited by 1,144 · see citing works
Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation
López-Maury, L., Marguerat, S., & Bähler, J. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2398 · Cited by 1,061 · see citing works
Wheeler, D. E., Buck, N. A., & Evans, J. D. (2006) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2006.00681.x · Cited by 708 · see citing works
Development and evolution of adaptive polyphenisms
Nijhout, H. F. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03003.x · Cited by 652 · see citing works
Settlement of benthic marine invertebrates
Rodriguez, S., Ojeda, F. P., & Inestrosa, N. (1993) · Marine Ecology Progress Series · doi:10.3354/meps097193 · Cited by 591 · see citing works
Larval experience and latent effects--metamorphosis is not a new beginning
Pechenik, J. A. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj028 · Cited by 591 · see citing works
Ecological developmental biology: integrating epigenetics, medicine, and evolution
(2009) · Choice Reviews Online · doi:10.5860/choice.46-5590 · Cited by 546 · see citing works
Sensory environments, larval abilities and local self-recruitment
Kingsford, M. J., Leis, J. M., Shanks, A. L., Lindeman, K. C., Morgan, S. G., & Pineda, J. (2002) · ResearchOnline - JCU (James Cook University) · Cited by 518 · see citing works
Metamorphosis Is Not a New Beginning
Pechenik, J. A., Wendt, D. E., & Jarrett, J. N. (1998) · BioScience · doi:10.2307/1313294 · Cited by 375 · see citing works
Rhythms of Gene Expression in a Fluctuating Intertidal Environment
Gracey, A. Y., Chaney, M. L., Boomhower, J. P., Tyburczy, W. R., Connor, K. M., & Somero, G. N. (2008) · Current Biology · doi:10.1016/j.cub.2008.08.049 · Cited by 256 · see citing works
A rapidly evolving secretome builds and patterns a sea shell
Jackson, D. J., McDougall, C., Green, K., Simpson, F., Wörheide, G., & Degnan, B. M. (2006) · BMC Biology · doi:10.1186/1741-7007-4-40 · Cited by 219 · see citing works
Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus
Oleksiak, M. F., Roach, J. L., & Crawford, D. L. (2004) · Nature Genetics · doi:10.1038/ng1483 · Cited by 205 · see citing works
Complexity and simplification in understanding recruitment in benthic populations
Pineda, J., Reyns, N. B., & Starczak, V. R. (2008) · Population Ecology · doi:10.1007/s10144-008-0118-0 · Cited by 200 · see citing works
Robustness, Flexibility, and the Role of Lateral Inhibition in the Neurogenic Network
Meir, E., von Dassow, G., Munro, E., & Odell, G. M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00839-4 · Cited by 193 · see citing works
The Pim kinases control rapamycin-resistant T cell survival and activation
Fox, C. J., Hammerman, P. S., & Thompson, C. B. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20042020 · Cited by 186 · see citing works
Why and how marine-invertebrate larvae metamorphose so fast
Hadfield, M. G. . (2000) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0197 · Cited by 172 · see citing works
Metamorphic Competence, a Major Adaptive Convergence in Marine Invertebrate Larvae
Hadfield, M. G. ., Carpizo‐Ituarte, E., del Carmen, K. A., & Nedved, B. T. (2001) · American Zoologist · doi:10.1093/icb/41.5.1123 · Cited by 165 · see citing works
V - The development of Haliotis Tuberculata , with special reference to organogenesis during torsion
Crofts, D. R. (1937) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1937.0012 · Cited by 150 · see citing works
Gregory, S. L., & Brown, N. H. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.5.1271 · Cited by 141 · see citing works
Settlement requirements of molluscan larvae: New data on chemical and genetic roles
Hadfield, M. G. . (1984) · Aquaculture · doi:10.1016/0044-8486(84)90272-2 · Cited by 131 · see citing works
Johnson, C. R., Sutton, D. C., Olson, R., et al. (1991) · Marine Ecology Progress Series · doi:10.3354/meps071143 · Cited by 123 · see citing works
A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response
Davidson, B., & Swalla, B. J. (2002) · Development · doi:10.1242/dev.129.20.4739 · Cited by 122 · see citing works
Signaling mechanisms underlying metamorphic transitions in animals.
Heyland, A., & Moroz, L. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icl023 · Cited by 121 · see citing works
Tasiemski, A., Vandenbulcke, F., Mitta, G., Lemoine, J., Lefebvre, C., Sautière, P. E., & Salzet, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312156200 · Cited by 118 · see citing works
Pechenik, J. A., & Heyman, W. D. (1987) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/s0022-0981(87)80012-6 · Cited by 116 · see citing works
Myeloid leukemia factor 1 regulates p53 by suppressing COP1 via COP9 signalosome subunit 3
Yoneda‐Kato, N., Tomoda, K., Umehara, M., Arata, Y., & Kato, J. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600656 · Cited by 100 · see citing works
Barlow, L. A., & Truman, J. W. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230705 · Cited by 90 · see citing works
Counihan, R. T., McNamara, D., Souter, D., Jebreen, E. J., Preston, N. P., Johnson, C. R., & Degnan, B. M. (2001) · Marine Ecology Progress Series · doi:10.3354/meps213193 · Cited by 89 · see citing works
Krug, P. (2001) · Marine Ecology Progress Series · doi:10.3354/meps213177 · Cited by 86 · see citing works
Settlement, early growth and survival of Haliotis rubra in response to different algal species
Daume, S., Krsinich, A., Farrell, S., et al. (2000) · Journal of Applied Phycology · doi:10.1023/a:1008110828581 · Cited by 85 · see citing works
Pechenik, J. A., & Qian, P. (1998) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/s0022-0981(97)00237-2 · Cited by 74 · see citing works
Isolation and expression of a cDNA for human brain fatty acid-binding protein (B-FABP)
Shimizu, F., Watanabe, T., Shinomiya, H., et al. (1997) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(97)00115-2 · Cited by 69 · see citing works
Aubin‐Horth, N., Letcher, B. H., & Hofmann, H. A. (2005) · Journal of Heredity · doi:10.1093/jhered/esi030 · Cited by 66 · see citing works
A complement response may activate metamorphosis in the ascidian Boltenia villosa
Roberts, B., Davidson, B., MacMaster, G., Lockhart, V., Ma, E., Wallace, S. S., & Swalla, B. J. (2007) · Development Genes and Evolution · doi:10.1007/s00427-007-0157-0 · Cited by 62 · see citing works
Williams, E. A., Degnan, B. M., Gunter, H. M., Jackson, D. J., Woodcroft, B. J., & Degnan, B. M. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.04078.x · Cited by 62 · see citing works
Self-citationJackson, D. J., Ellemor, N. J., & Degnan, B. M. (2005) · Marine Biology · doi:10.1007/s00227-005-1603-z · Cited by 61 · see citing works
Developmental and Morphogenetic Gene Regulation inHaliotis rufescensLarvae at Metamorphosis
Degnan, B. M., & Morse, D. E. (1995) · American Zoologist · doi:10.1093/icb/35.4.391 · Cited by 61 · see citing works
THE ROLES OF BACTERIA AND MICRO AND MACRO ALGAE IN ABALONE AQUACULTURE: A REVIEW
Daume, S. (2006) · Journal of Shellfish Research · doi:10.2983/0730-8000(2006)25[151:trobam]2.0.co;2 · Cited by 60 · see citing works
Metamorphic Competence, a Major Adaptive Convergence in Marine Invertebrate Larvae1
Hadfield, M. G. ., Carpizo‐Ituarte, E., del Carmen, K. A., & Nedved, B. T. (2001) · American Zoologist · doi:10.1668/0003-1569(2001)041[1123:mcamac]2.0.co;2 · Cited by 59 · see citing works
On the evolution of invertebrate defensins
RODRIGUEZDELAVEGA, R., & Possani, L. D. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.03.009 · Cited by 57 · see citing works
Settlement of larval blacklip abalone, Haliotis rubra, in response to green and red macroalgae
Huggett, M. J., de Nys, R., Williamson, J. E., et al. (2005) · Marine Biology · doi:10.1007/s00227-005-0005-6 · Cited by 49 · see citing works
Toonen, R. J., & Pawlik, J. R. (2001) · Marine Ecology Progress Series · doi:10.3354/meps224103 · Cited by 48 · see citing works
Williams, E. A., Craigie, A., Yeates, A., et al. (2008) · Biological Bulletin · doi:10.2307/25470687 · Cited by 48 · see citing works
Self-citationDegnan, B. M., Degnan, B. M., & Morse, D. E. (1997) · Development Genes and Evolution · doi:10.1007/s004270050076 · Cited by 41 · see citing works
FACTORS AFFECTING SETTLEMENT OF ABALONE (HALIOTIS IRIS) LARVAE ON BENTHIC DIATOM FILMS
Roberts, R. D., Kawamura, T., & HANDLEY, C. M. (2007) · Journal of Shellfish Research · doi:10.2983/0730-8000(2007)26[323:fasoah]2.0.co;2 · Cited by 32 · see citing works
Pawlik, J. R. (1989) · Marine Ecology Progress Series · doi:10.3354/meps051195 · Cited by 31 · see citing works
Degnan, B. M., Groppe, J. C., & Morse, D. E. (1995) · Development Genes and Evolution · doi:10.1007/bf00188848 · Cited by 28 · see citing works
Larval development in Haliotis asinina Linnaeus.
Sawatpeera, S., Upatham, E. S., Kruatrachue, M., et al. (2001) · Journal of Shellfish Research · Cited by 20 · see citing works
Jackson, D. J., & Degnan, B. M. (2006) · Journal of Shellfish Research · doi:10.2983/0730-8000(2006)25[225:estaog]2.0.co;2 · Cited by 18 · see citing works
Williams, E. A., Cummins, S. F., & Degnan, S. M. (2009) · Communicative & Integrative Biology · doi:10.4161/cib.2.4.8553 · Cited by 15 · see citing works
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An option space for early neural evolution
Jékely, G., Keijzer, F., & Godfrey-Smith, P. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0181 · Cited by 171 · see citing works
Degnan, S. M., & Degnan, B. M. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0248 · Cited by 71 · see citing works
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- Authors
- WILLIAMS, E. A., & DEGNAN, S. M.
- Affiliations
- The University of Queensland (AU)
- Corresponding author
- DEGNAN, SANDIE M.
- Venue
- Molecular Ecology
- Publisher
- Wiley
- Published
- 2009-10-14
- Volume
- 18
- Issue
- 21
- Pages
- 4434-4449
- ISSN
- 0962-1083 (ISSN-L)
- 1365-294X
- OpenAlex
- W2094374816
- Cited by
- 25
- References
- 54
- Citations by year
- 2023: 1 · 2018: 2 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 3 · 2012: 2
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Ecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Vedecká Grantová Agentúra MŠVVaŠ SR a SAV
- Australian Research Council
- Topics
- Physical Sciences › Environmental Science › Global and Planetary Change › Marine Bivalve and Aquaculture Studies
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- residual effects, larval settlement, metamorphosis, Haliotis asinina, abalone, coralline algae, settlement cues, transcriptional regulation
- MeSH terms
- Animals, Larva, Metamorphosis, Biological, Transcription, Genetic, DNA, Complementary, Gene Expression Regulation, Developmental, Gene Expression Profiling, Gastropoda, Eukaryota
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