Katie Marshall
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Population variation in enzyme activity, metabolic rate
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Theses completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest theses.
The mechanisms behind freeze tolerance in intertidal invertebrates is poorly understood. Due to differences in habitat and physiology, many biochemical processes utilized by terrestrial freeze tolerant organisms are not possible for intertidal invertebrates. Here I investigate the potential role of ice-binding proteins (IBPs) in the freeze tolerance of intertidal invertebrates. I first used bioinformatics to determine if there is molecular evidence for IBPs in intertidal invertebrates. I found a significant overrepresentation of putative IBPs in intertidal invertebrates relative to invertebrates from other habitat types, with no taxonomic patterns. These putative IBPs had high sequential similarity to type II antifreeze proteins from fish and antifreeze glycoproteins from both fish and ticks. Using some basic gene mapping I was also able to investigate the potential evolutionary origin of one of these putative IBPs from a mussel species (Mytilus coruscus), finding that a duplication and neofunctionalization event likely occurred. Knowing this I investigated the role of IBPs in the freeze tolerance of the local mussel species M. trossulus, a species that is more freeze tolerant in individuals from high shore positions during the winter months. I predicted that IBP activity would be measured in the protein extract of the species and that said activity would be greatest in winter individuals from high shore heights. Using a series of freezing assays and chemical treatments, I was able to find ice nucleation activity in M. trossulus and show strong evidence the activity was mediated by a protein, which I interpreted as IBPs. IBP activity did not vary by season or by shore height. This means IBPs may play a role in the year-long freeze tolerance of the species, but other mechanisms must explain the seasonal and tidal patterns in their freeze tolerance. In all, this thesis expands on our knowledge of intertidal freeze tolerance and provides the groundwork for future research into IBPs in multiple intertidal species.
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Many intertidal invertebrates are freeze tolerant, meaning that they can survive ice formation within their bodies when exposed to freezing air temperatures during low tides. In my thesis I addressed two key questions regarding intertidal invertebrate freeze tolerance using the intertidal mussel Mytilus trossulus. First: What biochemical mechanisms enable freeze tolerance in intertidal invertebrates? Second: How do sublethal single and repeated freeze exposures negatively impact intertidal invertebrates? To address the first question, I investigated the role of osmolytes in mussel freeze tolerance, which may be cryoprotective by mitigating osmotic stress caused by freezing. I sought to determine if different osmolytes are interchangeable cryoprotectants (acting as colligative cryoprotectants), or if each osmolyte has unique a cryoprotective role, beyond just contributing to increased intracellular osmolarity (and thus act as non-colligative cryoprotectants). I did this by manipulating the composition of mussels’ intracellular osmolyte pools, and then testing how mussel freeze tolerance changed. I found that mussel freeze tolerance did not change after taurine and betaine increased in concentration, significantly decreased after alanine and glycine increased in concentration, and increased with increasing TMAO concentrations, indicating that TMAO may be cryoprotective. Overall, my findings indicate that osmolytes are non-colligative cryoprotectants. Next, I explored how mussels are impacted by sublethal freezing. I found that mussels do not filter feed for the first four hours post-freeze, but resume filter feeding 24 hours after freezing, which corresponds to my microscopic examinations of mussel gill tissues after freezing which reveal freeze-related damage. I also found that freezing decreased mussel posterior adductor strength, although this effect did not lead to an increase in mussel susceptibility to sea star predation. Finally, I found that mussels survived shorter, repeated freezes (where mussels received 1 day for recovery between freezes) better than prolonged freezes, when total time frozen is held constant. Thus, mussels are well-adapted to survive the short freezing events which they regularly encounter in their habitat, and one mechanism behind this survival could be TMAO accumulation. Further, the effects of sublethal freezing on mussel performance are limited, although how these effects scale up to entire mussel beds remains unknown.
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Of all abiotic factors that drive range boundaries, temperature is the best studied because of its pervasive influence on biological processes. For populations at high-latitudes, extreme cold and the populations’ cold-hardiness set the range boundary. Phenotypic plasticity, where a single genotype results in differentiated phenotypes under differential environmental conditions, can assist populations in managing changing temperatures. Local adaptation in phenotypic plasticity, which results in different responses in different populations, can assist with the variability in temperature a species can experience across its range, especially at range boundaries. I used the eastern spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae) as a model system for exploring local adaptation and phenotypic plasticity of insect cold-hardiness. The species is one of the most destructive forest pests in North America, therefore accurately predicting its range and population growth is essential for management. In this thesis, I show that there is no transgenerational plasticity in cold-hardiness. However, I found a fitness cost associated with repeated cold exposures. Additionally, across the species’ range, I found both local adaptation of seasonal cold-hardiness and short-term plasticity of this trait. Therefore, the findings of this thesis provide evidence for including phenotypic plasticity and local adaptation when modelling species distributions under climate change.
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Publications
- Molecular evidence of intertidal habitats selecting for repeated ice-binding protein evolution in invertebrates (2022)
Journal of Experimental Biology, 225 (Array) - Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers (Mytilus sp.): a limit to poleward range shifts (2022)
- Proteostasis in ice: The role of heat shock proteins and ubiquitin in the freeze tolerance of the intertidal mussel, Mytilus trossulus (2022)
- Temperature–habitat interactions constrain seasonal activity in a continental array of pitfall traps (2022)
Ecology, - Allochronic isolation on a latitudinal gradient in the polyphagous moth Hyphantria cunea (2021)
- Do endotherms have thermal performance curves? (2021)
Journal of Experimental Biology, - Embracing imperfection: machine-assisted invertebrate classification in real-world datasets (2021)
- Plasticity of cold hardiness in the eastern spruce budworm, Choristoneura fumiferana (2021)
- Surviving in a Frozen Forest: the Physiology of Eastern Spruce Budworm Overwintering (2021)
Physiology, - The benefits of herbivory outweigh the costs of bioerosion in a eutrophic coral community (2021)
- Whole-organism responses to constant temperatures do not predict responses to variable temperatures in the ecosystem engineer Mytilus trossulus (2021)
Proceedings of the Royal Society B: Biological Sciences, - Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex (2020)
Journal of Experimental Biology, - Drivers of plasticity in freeze tolerance in the intertidal mussel, Mytilus trossulus (2020)
Journal of Experimental Biology, - Robust and simplified machine learning identification of pitfall trap‐collected ground beetles at the continental scale (2020)
Ecology and Evolution, - Repeated freezing induces a trade-off between cryoprotection and egg production in the goldenrod gall fly, Eurosta solidaginis (2018)
Journal of Experimental Biology, - Transcriptional dynamics following freezing stress reveal selection for mechanisms of freeze tolerance at the poleward range margin in the cold water intertidal barnacle Semibalanus balanoides (2018)
- Thermal sensitivity at constant temperatures does not predict responses under varying temperatures (2017)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 57, E337--E337 - Bacteria eat first at the dinner table (2016)
Journal of Experimental Biology, 219 (1), 4--4 - Biological impacts of thermal extremes: mechanisms and costs of functional responses matter (2016)
Integrative and comparative biology, 56 (1), 73--84 - Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? (2016)
Ecology Letters, 19 (11), 1372--1385 - Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome (2016)
Scientific Reports, 6 - Diving beetles that handle heat better have bigger backyard (2016)
Journal of Experimental Biology, 219 (19), 2970--2970 - Integrating the effects of repeated cold exposure from transcriptome to species distribution in the eastern spruce budworm (2016)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 56, E138--E138 - Life in the frequency domain: the biological impacts of changes in climate variability at multiple time scales (2016)
Integrative and comparative biology, , icw024 - Light-exposed moths can't find the flame (2016)
Journal of Experimental Biology, 219 (13), 1936--1936 - Primed to fight: mom's meals make baby stronger (2016)
Journal of Experimental Biology, 219 (7), 910--910 - Dateless bees wear better perfume (2015)
Journal of Experimental Biology, 218 (19), 2985--2985 - Decreased competitive interactions drive a reverse species richness latitudinal gradient in subarctic forests (2015)
Ecology, 96 (2), 461--470 - NEW FAT FUELS FROZEN FLIES (2015)
Journal of Student Science and Technology, 8 (1) - Seasonal swings match latitudinal shifts in shut down (2015)
Journal of Experimental Biology, 218 (7), 964--965 - Sunbathing helps senior flies keep active (2015)
Journal of Experimental Biology, 218 (13), 1978--1979 - The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect (2015)
Functional Ecology, 29 (3), 357--366 - UVB damages treefrog tadpole DNA (2015)
Journal of Experimental Biology, 218 (19), 2981--2982 - Yeast's beery smell attracts fruit flies (2015)
Journal of Experimental Biology, 218 (2), 164--164 - Acid defends ants against attack (2014)
- Bug buddy builds biotin (2014)
- Insect gears give great jumps (2014)
Journal of Experimental Biology, 217 (2), 160--161 - Seasonal accumulation of acetylated triacylglycerols by a freeze-tolerant insect (2014)
Journal of Experimental Biology, 217 (9), 1580--1587 - Stinky secretions for keeping clean (2014)
- AHEAD OF THE GAME: HOW KNOCKED INSECTS STICK (2013)
- ATTACK OF THE EXPLODING TERMITES (2013)
- MONOGAMOUS QUEENS MEAN LAZY WORKERS (2013)
- MUTANT MOSQUITOES REVEAL DEET'S DUAL ACTION (2013)
- Real-time measurement of metabolic rate during freezing and thawing of the wood frog, Rana sylvatica: implications for overwinter energy use (2013)
Journal of Experimental Biology, 216 (2), 292--302 - The goldenrod gall fly s liquid little secret: 3-acetyl-1, 2-diacyl-sn-glycerols are associated with natural survival of intracellular freezing in Eurosta solidaginis (2013)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 53, E137--E137 - The sub-lethal effects of repeated cold exposure in insects (2013)
- Awards, Scholarships and Grants Awarded at the SICB Meeting in January 2012 (2012)
Integrative and Comparative Biology, 52 (1), 1--2 - Differences in tissue concentrations of hydrogen peroxide in the roots and cotyledons of annual and perennial species of flax (Linum) (2012)
Botany, 90 (10), 1015--1027 - Ecologically-relevant stresses hurt differently: the response of Eurosta solidaginis to repeated freeze-thaw cycles (2012)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 52, E113--E113 - FRUIT FLIES ON ICE (2012)
- LIGHT AND CHEMICAL CUES TRIGGER BIBLICAL SWARMS (2012)
Journal of Experimental Biology, 215 (19), v--vi - Real-time measurements of metabolism during freezing and thawing in wood frogs, Rana sylvatica (2012)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 52, E160--E160 - The impacts of repeated cold exposure on insects (2012)
Journal of Experimental Biology, 215 (10), 1607--1613 - Thermal Variability Increases the Impact of Autumnal Warming and Drives Metabolic Depression in an Overwintering Butterfly (2012)
PLoS ONE, 7 (3), e34470 - Threshold temperatures mediate the impact of reduced snow cover on overwintering freeze-tolerant caterpillars (2012)
Naturwissenschaften, 99 (1), 33--41 - WATER STRESS DOWN SOUTH (2012)
- Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae) (2011)
Journal of evolutionary biology, 24 (9), 1927--1938 - Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster (2011)
Journal of Experimental Biology, 214 (23), 4021--4029 - The effects of CO2 and chronic cold exposure on fecundity of female Drosophila melanogaster (2011)
Journal of Insect Physiology, 57 (1), 35--37 - The Evolution of Cold Tolerance inDrosophilaLarvae (2011)
Physiological and Biochemical Zoology, 84 (1), 43--53 - The impacts of repeated cold exposure in insects (2011)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 51, E127--E127 - The sub-lethal effects of repeated freezing in the woolly bear caterpillar Pyrrharctia isabella (2011)
Journal of Experimental Biology, 214 (7), 1205--1212 - Triacylglyceride measurement in small quantities of homogenised insect tissue: comparisons and caveats (2011)
Journal of insect physiology, 57 (12), 1602--1613 - Rapid changes in desiccation resistance in Drosophila melanogaster are facilitated by changes in cuticular permeability (2010)
Journal of Insect Physiology, 56 (12), 2006--2012 - Repeated stress exposure results in a survival--reproduction trade-off in Drosophila melanogaster (2009)
Proceedings of the Royal Society of London B: Biological Sciences, , rspb20091807 - The sublethal effects of multiple acute cold exposure: lessons from Drosophila (2009)
INTEGRATIVE AND COMPARATIVE BIOLOGY, 49, E266--E266
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