Genetic and environmental interplay during development: Variation at metamorphosis in a natural population of the tropical abalone, Haliotis asinina (Linnaeus)

Elizabeth Amy Williams (2009). Genetic and environmental interplay during development: Variation at metamorphosis in a natural population of the tropical abalone, Haliotis asinina (Linnaeus) PhD Thesis, School of Biological Sciences, The University of Queensland.

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Author Elizabeth Amy Williams
Thesis Title Genetic and environmental interplay during development: Variation at metamorphosis in a natural population of the tropical abalone, Haliotis asinina (Linnaeus)
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2009-06
Thesis type PhD Thesis
Supervisor Dr. Sandie M. Degnan
Prof. Bernard M. Degnan
Dr. Scott Cummins
Total pages 159
Total colour pages 13
Total black and white pages 146
Subjects 06 Biological Sciences
Abstract/Summary Regulation of transcription is an important molecular mechanism through which organisms can respond to environmental change. Environmentally-related transcriptional variation can play a significant role in evolution, potentially acting as a mechanism for the formation of new adaptive phenotypes. Organisms are most sensitive to the influence of external environmental variation during development, yet very few studies have explored environmentally-related transcriptional variation in early life history stages. Marine invertebrate metamorphosis, where intimate larval-environment interactions trigger settlement onto the benthos and a drastic morphological shift from larval to adult form, exemplifies the influence of environment on development. Variation in both the timing of metamorphosis and the form of specific metamorphic inductive cues, even at an intraspecific level, suggests that larvae have molecular mechanisms for surviving settlement and metamorphosis in a range of environmental conditions. The extent of transcriptional variation at metamorphosis remains largely unknown due to limited information on both the natural inductive cues and the molecular mechanisms directing metamorphosis in marine invertebrates. Contributing to current understanding of the interplay between genes, environment and phenotype during development, I explored molecular and ecological aspects of metamorphosis in a marine invertebrate, the tropical abalone Haliotis asinina. First, I employed cDNA microarray methods to identify candidate genes and document widespread transcriptional changes occurring in Haliotis asinina larvae during larval development and metamorphosis. Microarray results reveal that as the abalone veliger larva matures, it requires coordinated regulation of temporally different gene batteries involved in a wide range of physiological and developmental processes associated with the transition to a new, benthic habitat. All candidate genes showed changes in expression following exposure of larvae to coralline algae, an external inductive cue, demonstrating the remarkable effect of environment on transcription during marine invertebrate metamorphosis. 144 genes, ~40% of which are novel, were identified as candidates for a role in H. asinina metamorphosis. This high proportion of novel genes indicates that the conserved signaling pathways operating in marine invertebrate metamorphosis likely regulate the expression of taxon-specific genes. The relationship between abalone larvae and their natural inductive cue, coralline algae, is species-specific. To characterize the metamorphic cue preferences of Haliotis asinina larvae from Heron Island Reef, Australia, I documented larval induction response to a number of different coralline algae species commonly found in adult H. asinina habitat. H. asinina larvae exhibit highly specific responses to induction of metamorphosis by different coralline algae species, with 0 – 100% metamorphosis by 48 hours post induction depending on algae species. Unlike any other abalone species studied, the most effective inducers of Heron Island Reef H. asinina are articulated corallines of the genus Amphiroa. Comparing the response of different larval families to select species of coralline algae indicated that coralline algae community composition is likely to significantly impact H. asinina population structure. Additionally, I compared larval response to dead and live coralline algae to show that induction specificity is driven by chemical, not physical, properties. Characterization of the surface cell biomarkers of three different coralline algae species indicates that algal biomolecular composition relates to variations in H. asinina induction response. To explore the influence of variation in larval induction environment, I compared transcription patterns of 17 metamorphosis-related genes in Haliotis asinina larvae induced by three different species of coralline algae. H. asinina post-induction gene expression profiles vary according to the species of coralline algae inducer. This transcriptional variation occurs in genes with diverse functions and spatial expression patterns, highlighting the global nature of the impact of benthic microhabitat on gene expression. The environment-specific modulation of gene expression in H. asinina post-induction may be a means for marine invertebrates to cope with changes in their settlement environment at metamorphosis. Genes expressed in the larval sensory structures acting to detect external metamorphic cues may be particularly good candidates for studying environmentally-related transcriptional variation. I identified three novel genes expressed in putative sensory structures of Haliotis asinina larvae just prior to metamorphosis. The spatial and temporal expression patterns of these genes correlate with changes in larval ciliation patterns throughout metamorphosis, strongly suggestive of a role in metamorphic initiation. The three genes exhibit significant overlap in spatial expression profiles, indicative of genetic crosstalk between different sensory systems at metamorphosis. Transcriptional variation in gastropod sensory system genes may have assisted the evolution of different metamorphic inductive cues for different species. The results presented here establish an important role for transcriptional variation during marine invertebrate metamorphosis. Transcriptional variation underlies the morphological change from larval to adult body plan and also appears to assist larval recruitment in variable benthic habitats. Modulation of gene expression at metamorphosis in response to the environment may ultimately influence marine invertebrate species biogeography and evolution.
Keyword Abalone Haliotis-asinina
coralline algae
Ecological Genetics
gene expression
Larval Settlement
marine ecology
life history evolution
Additional Notes Colour pages: 19, 26, 35, 38, 75, 77, 86, 101, 102, 105-107, 151. Landscape pages: 48-52.

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Created: Wed, 20 Jan 2010, 14:17:45 EST by Elizabeth Williams on behalf of Library - Information Access Service