Predatory gastropods (Neogastropoda) feed with a proboscis (elongate snout) and complex foregut. The presence of developmental modules (semi-autonomous components) in foregut development may have facilitated emergence of predatory feeding. In species with indirect development (feeding larval stage) physical and temporal separation of developing foregut modules (dorsal=larval esophagus; ventral=juvenile feeding structures) allows larval feeding and rapid switch to carnivory. However, previous studies on neogastropods with direct development (no feeding larval stage) did not identify foregut developmental modules. Thus, I investigated foregut development in two predatory, direct developing neogastropods: Nucella lamellosa and N. ostrina (Muricoidea), using histological sectioning, 3D reconstructions, TEM, and SEM. In both species, I showed evidence for dissociable dorsal and ventral foregut developmental modules. In N. lamellosa, the two modules were physically separate, although they were not separate in N. ostrina. My results reconcile differences in previous descriptions of foregut development between neogastropods with indirect and direct development. / Graduate

京都大学 / 新制・課程博士 / 博士(理学) / 甲第23040号 / 理博第4717号 / 新制||理||1676(附属図書館) / 京都大学大学院理学研究科生物科学専攻 / (主査)准教授 渡辺 勝敏, 教授 曽田 貞滋, 教授 沼田 英治 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DGAM

Ecological communities along gradients of environmental stress are thought to be structured by trade-offs between resisting biotic interactions in physically benign habitats and successfully exploiting physically stressful habitats. However, these trade-offs are likely to be affected by the predictability of abiotic stressors, and variation in the strength of biotic interactions. I investigated community assembly and food web interactions in ponds across an unpredictable gradient of water inundation (pond permanence) in Canterbury, New Zealand. Pond community composition and species richness were strongly influenced by pond permanence. However, species in temporary ponds were a nested subset of generalists that were also found in permanent ponds, rather than a unique assemblage of temporary pond specialists. Subsequent experiments indicated predator impact decreased with pond permanence, partially due to the foraging suppression of predatory invertebrates in permanent ponds by fish. Weak predation in permanent ponds combined with unpredictable drying regimes likely selected for generalist traits, and resulted in community assembly being driven by a gradient of drying stress rather than trade-offs between biotic interactions and drying. Furthermore, predator impact increased over time in temporary ponds. In predictable snow-melt ponds in the Colorado Rocky Mountains, seasonal windows of weak predation were exploited by vulnerable species, leading to increased diversity within habitats. However in unpredictable systems like Canterbury, temporal increases in predation risk that depend on drying history are likely to increase variability in the spatial arrangement of suitable habitats for particular species. This should further favour the evolution of generalist traits and reduce the importance of trade-offs between predation and drying in the assembly of communities. Considering the predictability of disturbance regimes and the spatial and temporal variation in biotic interactions will greatly enhance understanding and management of communities in heterogeneous landscapes.

Understanding how organisms function is central to Biology. Assessing how animals respond to fluctuations in their environment and determining inter-individual variation in phenotypic plasticity is paramount to identifying the physiology of traits, the selective pressures which have shaped them, and how we can manipulate them to benefit human life. The over-arching goal of my thesis is to understand the effects of sex, diet and pathogen exposure on the physiology of the fruit fly to assess the versatility of their individual traits in response to these natural factors. Chapter 2 investigates how the sexes utilise nutrition towards their lifespan and reproduction, providing evidence that the reproduction of males and females requires different dietary components while lifespan does not. Chapter 3 reveals that the sexes also differ in how they utilise nutrients for pathogen resistance identifying that females are highly protein-limited and more susceptible to infection than males. Chapter 4 provides the first comprehensive study of how organisms alter their dietary intake in response to infection, finding that flies behaviourally ingest less and consume higher protein:carbohydrate ratio diets when exposed to live fungal spores. Chapter 5 explores the phenomenon of trait-enhnacing external stresses, a response often termed hormesis. This study reveals that the beneficial physiological response from inactive fungal spore exposure, a potential form of hormesis, incurs immune costs. The implications of my results to the field of physiology are discussed in Chapter 6 where I also highlight the limitations of my work and potential consequences for life history research. Overall it is determined that studies investigating the natural physiological response of organisms or potentially beneficial treatments for our own species, must consider sex-specific effects, physiological consequences in a variety of traits, and how organisms may utilise variation within their environment to alter their phenotypic condition.

Life history theory assumes that correlations among fitness-related life history traits should be negative among individuals, reflecting resource allocation constraints among traits such as growth and reproduction. These traits trade off because they cannot be simultaneously maximized in individuals facing finite resource acquisition. Positive correlations among traits that are expected to be negative (e.g. between energetically costly traits) have been regularly observed, however, and have usually been ascribed to genetic or resource acquisition differences. In the freshwater zooplankton Cladoceran Daphnia, positive correlations have been particularly well documented even when genetic and environmental variation have been controlled. The sign of these correlations represent a problem for life history theory, which is underpinned by the notion of universal and unavoidable costs associated with investing in a given trait. It has been suggested, however, that costs vary with environment and thus can change the sign of a correlation. A change in correlation sign over an environmental gradient may indicate that the assumed universality of costs and constraints are not as universal as expected by life history theory. Few life history experiments have examined traits in multiple environments, and fewer have done so while controlling resource acquisition and genetic variation. Here I ask whether the positive genetic correlations among somatic growth rate, egg production rate, and longevity are present in the face of equal ingestion, clonal individuals, and a finely resolved gradient of food quality, an environmental factor that frequently affects Daphnia. I partition trait covariation into genetic and residual, or environmental, sources. All resulting genetic correlations were non-significant. Residual correlations trended from significantly positive to negative between longevity and growth rate and remained near zero between longevity and egg rate. The residual correlation between growth and reproduction, two expensive traits, displayed significantly positive residual correlations across the food quality gradient remained significantly positive. Given the experimental controls in place, I suggest that differences in individual ontogeny may give rise to differential resource utilization or assimilation efficiency. This may be a mechanism for differential resource acquisition in the absence of ingestion variation. Additionally, the different ways genetic and residual correlations change over an environmental gradient may provide insight on one manner by which genotypes might coexist and provide a candidate explanation for the second paradox of the plankton. / Thesis (Master, Biology) -- Queen's University, 2014-03-31 07:01:21.774

Ecological communities along gradients of environmental stress are thought to be structured by trade-offs between resisting biotic interactions in physically benign habitats and successfully exploiting physically stressful habitats. However, these trade-offs are likely to be affected by the predictability of abiotic stressors, and variation in the strength of biotic interactions. I investigated community assembly and food web interactions in ponds across an unpredictable gradient of water inundation (pond permanence) in Canterbury, New Zealand. Pond community composition and species richness were strongly influenced by pond permanence. However, species in temporary ponds were a nested subset of generalists that were also found in permanent ponds, rather than a unique assemblage of temporary pond specialists. Subsequent experiments indicated predator impact decreased with pond permanence, partially due to the foraging suppression of predatory invertebrates in permanent ponds by fish. Weak predation in permanent ponds combined with unpredictable drying regimes likely selected for generalist traits, and resulted in community assembly being driven by a gradient of drying stress rather than trade-offs between biotic interactions and drying. Furthermore, predator impact increased over time in temporary ponds. In predictable snow-melt ponds in the Colorado Rocky Mountains, seasonal windows of weak predation were exploited by vulnerable species, leading to increased diversity within habitats. However in unpredictable systems like Canterbury, temporal increases in predation risk that depend on drying history are likely to increase variability in the spatial arrangement of suitable habitats for particular species. This should further favour the evolution of generalist traits and reduce the importance of trade-offs between predation and drying in the assembly of communities. Considering the predictability of disturbance regimes and the spatial and temporal variation in biotic interactions will greatly enhance understanding and management of communities in heterogeneous landscapes.

Cette thèse s'inscrit dans le vaste domaine des recherches sur l'évolution des traits d'histoire de vie. Les traits d'histoire de vie sont directement impliqués dans la reproduction et la survie, et donc dans la valeur sélective, des organismes. L'intérêt pour les traits d'histoire de vie est motivé par l'immense diversité de ces traits dans le monde vivant. En particulier, il existe une grande diversité de patrons de vieillissement dans la nature. Cette thèse traite de l'évolution du vieillissement dans les populations naturelles. Comme pour la plupart des traits d'histoire de vie, les recherches théoriques sur l'évolution du vieillissement ont été menées dans le contexte d'une unique population, stable, et vivant dans un environnement constant. L'objectif de cette thèse est de prédire comment évolue le vieillissement lorsque les populations sont structurées dans l'espace et lorsque l'environnement varie dans le temps et l'espace. Mon approche a été essentiellement théorique, mais j'ai pu explorer certaines questions avec des données récoltées dans des populations naturelles. En introduction, je présente les éléments nécessaires à prendre à compte lorsqu'on s'intéresse à l'évolution des traits d'histoire de vie dans les populations structurées en âge. Je fais le constat que ces populations sont soumises à des variations environnementales et structurées dans l'espace. Dans la première partie, je montre que les variations de l'environnement, dans le temps et dans l'espace, peuvent affecter les patrons de sénescence. J'utilise des méthodes de génétique quantitative où je fais l'hypothèse que les mutations ont un effet spécifique à l'environnement et à l'âge. Dans la deuxième partie, je m'intéresse aux conséquences des dynamiques d'extinction-recolonisation sur la stratégie de partage des ressources entre la survie et la reproduction des individus en fonction de leur âge. Je montre en particulier que la dispersion est une source de variabilité pour cette stratégie et examine comment dispersants et non-dispersants diffèrent pour leur traits d'histoire de vie dans 3 jeux de données. De façon générale, mes résultats montrent que la prise en compte des conditions écologiques et environnementales complexes où vivent les organismes permet de mieux comprendre la diversité des patrons de vieillissement dans la nature. En dernier lieu, je fais un court bilan de cette thèse puis donne des perspectives possibles à mes recherches et de façon plus générale aux recherches sur l'évolution du vieillissement. / This thesis belongs to the wide field of life history evolution. Life history traits are directly involved in reproduction and survival. The interest for life-history evolution arises because organisms have evolved so many different ways of combining these traits to affect fitness. In particular, there is an important diversity of aging patterns in the wild. Aging is defined as the variation of life-history traits, such as survival or fecundity, with age. Senescence describes more precisely the idea that survival or fecundity decline with age. This synthesis deals with the question of aging in natural populations. Like most life-history traits, the evolution of aging has often been studied in the context of a single undisturbed population in a constant environment. My thesis aims at investigating how relaxing this assumption affects the evolution aging. I investigated this question mostly theoretically, but I used data from the field to investigate related questions. In introduction, I first go through evolutionary characteristics of age-structured populations. I also make the observation that age-structured populations are structured in space and live in a varying environment. In the first part, I investigate how environmental variability in space and time influences aging through the key results of Hamilton (1966) that the strength of selection declines with age. I used a quantitative genetics framework where I assumed that mutations that affect survival or fecundity have an age and environment specific effect. In the second part, I examine the role of metapopulation dynamics on the evolution of aging. I used an adaptive dynamics framework where mutations affect how a resource is shared between reproduction and survival at a given age. I show how the optimal age-specific reproductive effort is different in a metapopulation and in a single population. I then investigate how dispersal can be a source of heterogeneity in optimal age-specific reproductive effort. In this part, I went further in testing my predictions (and more generally exploring aging patterns) with data. As a general result, this thesis shows that including environmental and ecological heterogeneities helps understanding variation in aging in the wild. I finally discuss my main findings and give some perspectives to this work.

Maternal effects are the non-genetic contributions of mothers (or fathers) towards the phenotype of their offspring. Maternal effects are now well recognised as a facilitator for evolutionary change in offspring phenotypes and life history strategies which can have effects on population dynamics, population divergence and even speciation. Furthermore, maternal effects have been shown to have a heritable genetic basis and that they are genetically variable, which suggests that they contribute to maintaining phenotypic variation. Maternal effects may impede or accelerate responses to selection which has implications for adaptive evolution and making predictions about their evolutionary potential. The importance of their contribution to phenotypic variation and life history evolution has made maternal effects an important consideration in fields such as conservation and population biology, evolutionary ecology and evolutionary genetics. The aim of this thesis is to investigate if maternal effects can influence offspring life history traits and fitness parameters through maternal resources via the egg. Main questions that are asked include: can maternal effects help facilitate transition to a novel host-diet (Chapter 2); does maternal diet influence egg composition and, if so, does this have an effect on offspring life-history parameters (Chapter 3); is there a genetic basis to egg composition and is there potential for egg composition to evolve (Chapter 4); and are defensive compounds from the diet transferred into the eggs, if so, are these uni- or biparentally transferred and does this offer protection against predation (Chapter 5)? To address these questions we used a specialist insect herbivore, the large milkweed bug Oncopeltus fasciatus (Hemiptera: Lygaeidae). In the wild, O. fasciatus feed on plants from the genus Asclepias (Apocynacea). However, O. fasciatus can be reared successfully in laboratories on sunflower seeds Helianthus annus. For our experiments we used two populations of O. fasciatus, one population has been maintained on dry seeds of A. syriaca while the other population has been reared and maintained on sunflower seeds. The results of Chapter 2 were suggestive of a maternal host-diet effect on egg mass and hatching success, but we did not find evidence that maternal host-diet was significant in influencing a transition to a novel host. In Chapter 3 we found that there was variation in the free amino acid profiles of the eggs between our treatments suggesting that amino acid profiles may be influenced by maternal diet. The results of our multivariate selection analysis to examine linear and nonlinear (quadratic) relationships between maternal diet and the free amino acid profiles of the eggs suggest that there may be population-specific responses which can influence specific amino acid profiles in relation to hatchling mass. In Chapter 4 we used only the milkweed-adapted population to determine if there was a genetic basis to amino acid profiles in the eggs. We constructed a genetic variance-covariance (G) matrix to determine the strength and direction of the relationships between amino acids and to assess the potential for amino acid profiles to evolve. While we found genetic variation for amino acids, and that there was evidence for positive moderate to strong genetic correlations between many of them, we also found evidence for constraints for the potential for amino acid profiles to evolve as evidenced by the calculation of gmax (which represents the linear combination of components that has the highest genetic variance and which is the most accessible to evolution). In Chapter 5 we found maternal, but not paternal, transmission of cardenolides into the eggs. However, this did not confer protection of all eggs against predation from larvae of the green lacewing Chrysoperla carnea. Overall, results suggest that for our populations of O. fasciatus, maternal effects are significant in influencing early life history traits such as egg mass and hatchling mass. However, we did not find any significant effects on other offspring life history or fitness parameters that we measured. This may be surprising as positive, and negative, effects of non-genetic contributions of females (and males) to their offspring has been widely reported in many taxa. The patterns and implications of maternal resource allocation and their effects on offspring life history evolution are explored and discussed, as are the limitations of our experimental designs. I hope that this research can be used to stimulate further investigations into maternal effects and the relationships between host-plant, maternal allocation strategies and life history evolution.

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.

A central goal of life history theory is to understand the selective factors that generate the diversity of reproductive patterns observed in nature. Within lifetime changes in reproductive investment will determine an organism's fitness; however, this area of life history theory has received less attention than comparisons among population that characterize life history traits as a single population mean. Reproductive allocation can be affected by multiple cues; the integration of these cues across an organism's lifetime generates the diversity in life history strategies observed in nature. Life history studies should examine the interacting effects of multiple cues on life history strategies to generate better predictions and generalizations of age-related changes in reproductive investment. An individual's life history strategy is inherently multivariate consisting of a coordinated suite of life history traits that, when combined across the organism's lifetime, determines its fitness. Life history strategies can therefore be described as a trajectory through multivariate space defined by life history traits. Here I describe life history trajectory analysis, a multivariate analytical approach for quantifying and comparing phenotypic change in life history strategies; this methodology is adapted from an analytical framework originally described for studies of morphological evolution. Life history trajectories have attributes (magnitude, direction, and shape) that can be quantified and statistically compared among taxa to determine if life history patterns are predictable. Using the life history trajectory analysis, I demonstrate the effect of prior experience on reproductive allocation in the burying beetle Nicrophorus orbicollis. The effect of prior experience resulted in a terminal investment or accentuated response to age-based cues, or resulted in a conservative investment strategy or reproductive restraint. In the livebearing fish Gambusia affinis, females adjust the level of reproductive investment to current reproduction based on age- or environment-based cues. Age-0 females decreased the level of reproductive investment to current reproduction in late summer prior to the onset of fall and winter months. Old females, on the other hand, increased the level of reproductive investment as the summer progressed. The reproductive restraint and terminal investment patterns exhibited by age-0 and age-1 females, respectively, were consistent with the predictions from the cost of reproduction hypothesis. These studies demonstrate how the life history trajectory analysis provides an analytical tool to test predictions of life history theory. Additionally, I provide evidence that organisms use multiple cues to determine the level of reproductive investment and that the strength of the effect of each cue will depend on the age of an individual.