RESILIENCE ACROSS GENERATIONS: EXPLORING TRANSGENERATIONAL AND LARVAL ACCLIMATION TO THERMAL STRESS IN THE MARINE ANNELID HYDROIDES ELEGANS

Ph.D

Inter- and Intra-specific variation in egg size among reef fishes across the Isthmus of Panama

Effects of planktonic food supplies and temperature on pelagic fish larvae are thought to be the primary environmental determinants of adaptive variation in egg size. Differences between the Atlantic and Pacific coasts of Panama in primary production (higher in the Pacific due to upwelling) and temperature (less seasonal in the non-upwelling Caribbean) allow testing such ideas. We compared the volumes, dry weights and energy content of eggs of 24 species of reef fishes from the two sides of the isthmus during the cool and warm seasons. Both egg volume and egg dry weight were good predictors of egg energy content among species, although not within species. Caribbean species produced larger eggs than their close relatives in the Pacific. In the Pacific, eggs were significantly larger during the cool upwelling season than during the warm, non-upwelling period, with a similar but weaker seasonal pattern evident in the Caribbean. The production of larger eggs in the low-productivity Caribbean is consistent with the hypothesis that species produce larger eggs and offspring when larval food supplies are lower. Parallel patterns of seasonal variation in eggs size and the greater strength of that relationship in the Pacific indicate that temperature drives seasonal variation in egg size within species. The decline in egg size with increasing temperature, a general pattern among ectotherms, may be a physiological side-effect, due to differing effects of temperature on various metabolic processes during oogenesis or on hormones that influence growth and reproduction. Alternatively, the seasonal pattern may be adaptive in these fishes, by affecting larval performance or maintaining a particular timeline of major events during embryonic development

Serpulidae (Annelida: Polychaeta) from the Suez Canal: from a Lessepsian migration perspective (a monograph).

Data on Serpulidae collected in the Suez Canal were assembled and analyzed. Five serpulid taxa are reported from the canal for the first time bringing the number of serpulids to at least 16. The Systematic Section compiles revised literature records, confirmed synonymies of the taxa, redescriptions where necessary, photographic studies of taxa and remarks on the populations studied. The possible Indo-West-Pacific or Mediterranean origins of the taxa in the Suez Canal are considered and their chronological records and distributions tracked within the Red Sea, the Gulfs of Aqaba and Suez, the Suez Canal and the Levant Basin based on the compiled literature and our extensive databases. Two Lessepsian migrants, Hydroides heterocerus and H. homoceros, show evidence of morphological variability along their migration route; the last also provides an example of a founder effect. Problems of identifying Protula and Salmacina taxa are addressed, along with remarks on the "cosmopolitan" designations of some taxa. Various hypotheses concerning Lessepsian migration are discussed, and attributes making Lessepsian migrant serpulid tubeworms successful invasive species are evaluated

Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification?

Human-assisted, trans-generational exposure to ocean warming and acidification has been proposed as a conservation and/or restoration tool to produce resilient offspring. To improve our understanding of the need for and the efficacy of this approach, we characterized life-history and physiological responses in offspring of the marine polychaete Ophryotrocha labronica exposed to predicted ocean warming (OW: + 3 degrees C), ocean acidification (OA: pH -0.5) and their combination (OWA: + 3 degrees C, pH -0.5), following the exposure of their parents to either control conditions (within-generational exposure) or the same conditions (trans-generational exposure). Trans-generational exposure to OW fully alleviated the negative effects of within-generational exposure to OW on fecundity and egg volume and was accompanied by increased metabolic activity. While within-generational exposure to OA reduced juvenile growth rates and egg volume, trans-generational exposure alleviated the former but could not restore the latter. Surprisingly, exposure to OWA had no negative impacts within-or trans-generationally. Our results highlight the potential for trans-generational laboratory experiments in producing offspring that are resilient to OW and OA. However, trans-generational exposure does not always appear to improve traits and therefore may not be a universally useful tool for all species in the face of global change

Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus

Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin (Strongylocentrotus purpuratus) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting

Environmental Impacts and Carry-over Effects in Complex Life Cycles: The Role of Different Life History Stages

A challenge faced by organisms with complex life cycles is how environmental factors experienced at an earlier life stage affect the fitness at that stage or are carried over to subsequent life stages. I used container-inhabiting mosquitoes: Aedes albopictus, Aedes aegypti, Aedes triseriatus and Culex quinquefasciatus to study the interactions and performance of life history stages under specific environmental factors. I investigated the effects of egg-desiccation tolerance on egg viability and larval performance in the Aedes mosquitoes. I found increase in egg hatch rate with relative humidity and interaction between relative humidity and egg storage period. Larval performance differed among species, but egg-desiccation tolerance did not lead to higher larval performance. I examined the effects of temperature on the outcome of larval intraspecific competition as well as interactions between temperatures for rearing and those for adult maintenance in Aedes albopictus. I found that increasing temperatures resulted in shorter development time and smaller adult sizes while increasing densities led to longer development time and smaller adult sizes for males and females. There was also an interaction between larval and adult temperatures; higher temperatures led to greater differences in female fecundity, and lower temperatures led to increased survival. I investigated the effects of female natal habitat on oviposition responses and larval performance in Ae. albopictus, Ae aegypti and Cx quinquefasciatus. I found that Ae aegypti showed no oviposition preference, Ae. albopictus significantly preferred animal:leaf detritus infusion and Cx quinquefasciatus did not oviposit in tap water. However, there were no overall carry-over effects of natal habitat on oviposition choices and population growth. I examined the relationships among female natal habitat, female size, egg number, and egg volume in Ae. albopictus and Cx. quinquefasciatus. For Ae. albopictus, I found strong positive relationships in animal detritus with female size and egg number, and in leaf detritus with egg volume. For Cx. quinquefasciatus, I found strong positive relationships in animal detritus with female size and egg number. My study provides more insight on the importance of habitat heterogeneity and environmental stochasticity, and the strength of their carry-over effects across life stages in complex life cycles

The biology of the evolution of viviparity in asterinid sea stars

Viviparous asterinids exhibit great diversity in reproductive and offspring provisioning strategies, which raises fascinating life-history questions. This thesis investigates the biology of parent-offspring size variation, offspring release, nutrient provisioning and morphological adaptions in three viviparous asterinid sea stars, Cryptasterina hystera, Parvulastra vivipara and P. parvivipara. These species have contrasting lecithotrophic and matrotrophic provisioning of developing offspring in the gonads. In C. hystera (lecithotrophic), the juveniles (655 µm diameter) develop from large eggs (440 µm diameter). In P. vivipara and P. parvivipara, juveniles vary greatly in diameter (500–5000 µm) and develop from small eggs (84–150 µm diameter) through sibling cannibalism (matrotrophy). In these species, larger parents had greater reproductive output and produced more, but not larger, offspring. The species with matrotrophic offspring provisioning had a higher reproductive output than the lecithotrophic species. Parvulastra parvivipara released juveniles in 1–5 cohorts and exhibits continuous reproduction. Cryptasterina hystera retained a few large offspring in the gonad after 30 days of synchronous release. The degree of parental investment measured as matrotrophy index (the ratio of juvenile to egg dry mass) ranged from 597–55082 (P. parvivipara) and 1.7–6.2 (C. hystera), indicating a continuum in offspring provisioning. Potential specializations for viviparity and provisioning of nutrients for offspring were investigated using confocal microscopy and histology. The early larvae were closely associated with the inner gonad wall, supported by thin processes from somatic cells. The arrangement of P. parvivipara progeny in the gonads was observed three-dimensionally using micro-computed tomography. The juveniles were orally opposite to each other, presumably as a defensive strategy to protect themselves from being eaten. Confocal microscopy revealed 2–6 developmental stages in each gonad. The size variation of offspring intensifies when siblings start cannibalism post-metamorphosis

Selective mortality on early life-history traits of a temperate reef fish

Variability in recruitment and early life-history traits is widespread in many marine organisms. Phenotypic variation is particularly prevalent in the early life-history stages (e.g., larvae and juveniles) of reef fish, and provides the basis for selective mortality on growth and size-related traits, with important ecological and evolutionary consequences. Recruitment variability can alter the effective densities experienced by these early life stages, raising additional questions about the interplay between selection and density-dependent processes. While many examples of growth- and size-selective mortality have been documented for young reef fish (typically caused by predators), few studies consider how the strength and/or direction of selective mortality changes with ontogeny, or how these patterns may be mediated by density. I explore spatio-temporal variability in early life-history traits of the common triplefin, Forsterygion lapillum, using metrics derived from otoliths (a re-analysis of two previously collected data sets). I evaluate patterns of variation in traits with respect to early life-history stage (either larvae or post-settlement juveniles) and document shifts in the distributions of traits that are consistent with selective mortality favouring slower growing individuals. I conclude that a cohort of juveniles (sampled after settlement) was comprised of individuals that were smaller at hatch and grew slowly throughout the pelagic larval period relative to a cohort of larvae (sampled prior to settlement). I then conducted an experiment using a set of mesocosms to evaluate whether selective mortality on early life-history traits in common triplefin could be caused by a natural predator, the variable triplefin, Forsterygion varium. Specifically, I exposed groups of fish of each stage to a pair of predators and I used otoliths to reconstruct the traits of fish that survived versus fish that were consumed (i.e., I recovered otoliths from the guts of predators). Selection trials were conducted across realistic density gradients for each developmental stage. Fish size was negatively correlated with relative fitness for larvae (indicating larger fish were consumed preferentially by predators) but not for juveniles (where no size-selective mortality was observed). These patterns were consistent across the range of densities evaluated. Both larvae and juveniles experienced significant selection against fast larval growth (estimated from growth increments in otoliths), and the strength of selection was inversely related to density (i.e., strongest at lower densities, weakest at higher densities). However, juveniles also experienced selective predation for fast growth at the larval-juvenile transition. As with larval growth, selection was strongest at lower densities and weakest at higher densities. Collectively, these results suggest that predators may preferentially target larger larvae, and faster growing individuals regardless of developmental stage. However, this effect may be mediated by density, such that the strongest selection occurs during low recruitment. Density-dependent selection could explain how faster growing individuals can survive this vulnerable stage. These results provide evidence for carry-over effects of larval growth on juvenile survival, and suggest conspecific density should be considered when evaluating patterns of selective mortality

Rareté et changements globaux : tolérance aux changements globaux et capacité pour la plasticité transgénérationnelle chez une espèce rare et une espèce commune de polychètes marins

RÉSUMÉ: La variation au sein de la répartition géographique des espèces est observée depuis longtemps, et il a été reconnu, qu'à l'intérieur d'un groupe taxonomique, la majorité des espèces ont une distribution géographique restreinte (espèce rare), alors que peu sont largement distribuée (espèce commune). L'explication la plus acceptée quant à la variation du niveau de biodiversité à travers le monde est la différence au niveau de la « niche » des espèces, qui ultimement définit l'amplitude de leur distribution géographique. La variation des traits physiologiques joue un rôle pivot dans la définition de la niche des espèces, et par le fait même leur distribution géographique. Ainsi les espèces rares auront de plus petites fenêtres de tolérance physiologique et des niveaux de plasticité plus faibles, faisant d'elles des espèces plus à risque à l'extinction locale dans le contexte des changements globaux. En considérant que les espèces rares sont les plus nombreuses, leurs réponses face aux changements rapides en cours dans leur environnement vont avoir des impacts sur la diversité taxonomique au sein du règne animal, ainsi que sur la structure et les fonctions des futurs écosystèmes. Le réchauffement et l'acidification des océans vont avoir des répercussions sur un grand nombre de processus cellulaires. Par les changements au niveau du métabolisme énergétique, puis l'altération des traits d'histoire de vie, c'est toute la structure et le fonctionnement des écosystèmes qui seront bouleversé. La plasticité phénotypique peu rapidement aider à rétablir et maximiser les performances des organismes à l'intérieur d'une (intra-générationnelle) ou plusieurs générations (transgénérationnelle) lors de changements dans leur environnement. Par conséquent, le but de notre étude était d'investiguer si des espèces rare et commune répondent différemment aux scénarios de changements globaux en environnement marin, et si leur tolérance et capacité pour la plasticité transgénérationnelle sont différentes. Pour répondre à ces questions, deux espèces de polychètes du genre Ophryotrocha, une rare (O. robusta) et une commune (O. japonica), ont été exposées à quatre scénarios de changements globaux prédits pour la fin du siècle sur deux générations, soit des conditions de contrôle (C), d'acidification des océans (AO), de réchauffement des océans (RO) et un scénario combiné (RAO)). Les traits d'histoire de vie (croissance, fécondité, volume des œufs) ont été mesurés sur une période de quatre mois, après quoi les profiles métabolomiques des individus ont été analysés pour mettre en évidence les métabolites liés aux changements des traits d'histoire de vie. En général, la température élevée a été le facteur principal affectant négativement les performances de l'espèce rare. L'augmentation de la température a eu un impact négatif sur le fitness et la survie de O. robusta. À l'opposé, le fitness de l'espèce commune, mesurés en termes de taux de survie et de capacité à contribuer à la prochaine génération, est demeuré plutôt élevé dans tous les scénarios et générations. L'espèce commune a été l'espèce la plus performante dans les différents scénarios, probablement par le bénéfice des mécanismes de plasticité intra et transgénérationnelle. Ce qui mène à la conclusion que l'espèce rare possède une fenêtre de tolérance plus étroite que l'espèce commune et qu'elle aura plus de difficulté à faire face aux futures conditions de changements climatiques. Ces résultats ont une portée importante au niveau de la conservation de la biodiversité marine, considérant que les espèces rares sont communes dans le règne animal et ont un rôle clé en ce qui a trait aux fonctions des écosystèmes. -- Mot(s) clé(s) en français : Distribution géographique, tolérance, changements globaux, plasticité transgénérationnelle, histoire de vie, métabolomique, biodiversité. -- ABSTRACT: Variation in the geographical range of species has long been observed, and it well established that most species have a restricted geographic distribution (rare species), whilst few are geographically widespread (common species). One explanation for the variation in biodiversity levels across the globe is that difference in species' 'niche' ultimately defines the breadth of their geographical distribution. Variation in physiological traits is considered to play a pivotal role in defining species niche, and thus their geographical distribution and local abundance, predicting that rare species will have smaller physiological tolerance windows and plasticity levels. Rare species' responses to rapid ongoing changes in their environment will then greatly define taxonomic diversity across the tree of life, as well as the functions of future ecosystems. Ocean warming and acidification will have impacts on a number of cellular processes. Through shifts in metabolic energy and alteration of life-history traits, all the ecosystem's structure and functions will be affected. Phenotypic plasticity can rapidly help re-establishing and maximising organisms' performances within and between generations when environmental changes occur. Consequently, the aim of our study was to determine if rare and common species respond differently to global changes scenarios in a marine environment, and if their tolerance and capacity for transgenerational plasticity are different. To answer this, two species of polychaete of the genus Ophryotrocha, one rare (O. robusta) and one common (O. japonica), were exposed to four different climate change scenarios predict to occur by the end of the century for two generations (control (C), ocean acidification (OA), ocean warming (OW) and a combined scenario (OAW)). Life history traits (growth, fecundity and eggs volume) were measured on a four months period, after which metabolomics profiles were analysed to highlight molecular pattern (energetic metabolism) linked to life history traits' changes. Overall, the high temperature was the main factor negatively affecting the rare species' performances. The increase in temperature impacted the physiology of O. robusta, ultimately affecting its reproduction and survival. On the other hand, the common species' reproduction, measured in terms of survival success and capacity to contribute to the next generation, remained quite high for all scenarios and generations. The common species was also the most tolerant species under global change scenarios, likely benefiting from both within- and transgenerational plasticity mechanisms. Hence the rare species appear to possess a narrower tolerance window than the common species, and might will have more difficulties to cope with future climatic conditions. These results will likely have important impacts on marine biodiversity levels and conservation, considering that rare species are common in the animal kingdom and have key role in ecosystem functions. -- Mot(s) clé(s) en anglais : Geographic distribution, tolerance, global changes, transgenerational plasticity, life history, metabolomics, biodiversity