Évolution des tactiques alternatives chez l'omble de fontaine. Patrons de reproduction, héritabilité et pêche sélective

L’objectif principal de cette thèse était de déterminer les bases génétiques des tactiques alternatives de vie chez l’omble de fontaine, Salvelinus fontinalis. L’anadromie, la migration en eau salée et le retour vers l’eau douce pour la reproduction, ainsi que la résidence, la réalisation du cycle de vie entièrement en eau douce, sont deux formes de vie communes chez les salmonidés souvent retrouvées en sympatrie. Ces formes sont ici considérées comme des tactiques alternatives au sein d’une stratégie conditionnelle et étudiées sous le modèle de traits seuils. Tout d’abord, à l’aide de marqueurs moléculaires et d’analyses d’assignation parentale, la reproduction entre les deux formes, assurée par les mâles résidents, a été mise en évidence. De plus, le succès reproducteur individuel était lié à la taille chez les femelles, mais pas chez les mâles, suggérant l’emploi d’une tactique de reproduction furtive par ces derniers. Ensuite, des méthodes de reconstruction de groupes d’individus apparentés couplées à un « modèle animal » ont permis d’estimer l’héritabilité de la tactique (gamme variant entre 0.53 et 0.56) ainsi que la corrélation génétique entre la taille et la tactique (-0.52 ou -0.61), suggérant une évolution conjointe de ces deux traits. Finalement, à l’aide d’un modèle éco-génétique, les conséquences de la pêche sportive sur l’évolution de l’anadromie et la résidence ont été évaluées. Après 100 ans de pression de pêche, la norme de réaction de migration est déplacée, entrainant une diminution dans la probabilité de migrer avec une augmentation de l’intensité de pêche. Ce changement est accompagné par une augmentation dans l’âge à la migration. La proportion de poissons adoptant la tactique anadrome diminue dans la population à mesure que l’intensité de pêche augmente, tout comme le nombre absolu de poissons retrouvé en eau salée. Ces changements se traduisent en de plus bas âges et tailles à maturité. Cette thèse contribue à notre compréhension du déterminisme des phénotypes alternatifs et se distingue par sa réalisation complète sous conditions naturelles. En mettant en lumière les bases génétiques de l’anadromie et la résidence, ce travail suggère qu’une réponse évolutive est possible face à des pressions de sélection, anthropiques ou naturelles, et une telle réponse est démontrée grâce à une approche de modélisation innovatrice.The central objective of this thesis was to assess the genetic basis of alternative life-history tactics in brook charr, Salvelinus fontinalis. Anadromy, defined as migration to sea before returning to freshwater to spawn, and residency, the completion of the entire life-cycle in freshwater, are two tactics commonly found in sympatry in salmonids. These two life-history forms are considered here as alternative tactics within a conditional strategy and are studied according to the threshold model of quantitative genetics. First, molecular markers and parentage analysis revealed that reproduction frequently occurred between the two forms, and was mediated by the resident males. Moreover, individual reproductive success was linked to body size in females, but not in males, which suggest that smaller males make use of the alternative sneaker reproductive tactic. Second, sib-reconstruction methods coupled to an “animal model” allowed the estimation of a significant heritability for the life-history tactic (between 0.53 and 0.56) and a significant genetic correlation between body size and tactic (-0.52 and -0.61), suggesting a joint evolution of these two traits. Finally, the evolutionary consequences of sportfishery on the evolution of anadromy and residency were assessed with the use of an eco-genetic model. After a hundred years of fishing-induced selection directed toward anadromous fish, the migration reaction norms shifted, resulting in a decrease in the probability of migrating with increasing harvest rate. This change was accompanied by a higher mean age at migration. The proportion of fish adopting the anadromous tactic decreased in the population as harvest rate increased, as did the absolute number of fish found in saltwater. These changes resulted in a lower mean age and size at maturity. This thesis contributes to our understanding of the determinism of alternative phenotypes and stands out because of its realization under completely natural conditions. By highlighting the genetic basis of anadromy and residency, this work suggests that an evolutionary response is expected in face of anthropogenic or natural selective forces, and such consequences are presented through an innovative modeling approach

RELATING METABOLIC PHENOTYPES TO MOVEMENT BEHAVIOR IN BROOK TROUT

Brook trout movement-related life history strategies vary considerably and range from individuals that stay within the same 100 meters their entire life to individuals that are potamodromous or anadromous. Potential drivers of movement life histories have been the subject of much research in fish, with genetic subpopulation explanations often failing to explain the phenomenon. Metabolic phenotypes have been suggested as a possible driver for expression of different movement life histories. I investigated if metabolic phenotypes are related to movement strategies within a population of brook trout (Salvelinus fontinalis) in Unnamed Creek, a tributary to the Rock River, Alger County, MI. Intermittent flow respirometry was used in the field using ambient stream water to determine metabolic phenotypes of wild trout. Individuals were then tagged with passive integrated transponders (PIT) and tracked with stationary readers and a backpack reader during the summer. Brook trout that moved over 250m displayed a significantly larger aerobic scope than individuals that moved less than 250m. Temperature effects on metabolic measures were not detected among the brook trout in this study, but this could be due to wild acclimation to a range of temperatures rather than a single value.. This study suggests that brook trout metabolic phenotypes are variable between individuals and likely relate to movement phenotype under natural field conditions

The effects of medieval dams on genetic divergence and demographic history in brown trout populations

BACKGROUND: Habitat fragmentation has accelerated within the last century, but may have been ongoing over longer time scales. We analyzed the timing and genetic consequences of fragmentation in two isolated lake-dwelling brown trout populations. They are from the same river system (the Gudenå River, Denmark) and have been isolated from downstream anadromous trout by dams established ca. 600–800 years ago. For reference, we included ten other anadromous populations and two hatchery strains. Based on analysis of 44 microsatellite loci we investigated if the lake populations have been naturally genetically differentiated from anadromous trout for thousands of years, or have diverged recently due to the establishment of dams. RESULTS: Divergence time estimates were based on 1) Approximate Bayesian Computation and 2) a coalescent-based isolation-with-gene-flow model. Both methods suggested divergence times ca. 600–800 years bp, providing strong evidence for establishment of dams in the Medieval as the factor causing divergence. Bayesian cluster analysis showed influence of stocked trout in several reference populations, but not in the focal lake and anadromous populations. Estimates of effective population size using a linkage disequilibrium method ranged from 244 to > 1,000 in all but one anadromous population, but were lower (153 and 252) in the lake populations. CONCLUSIONS: We show that genetic divergence of lake-dwelling trout in two Danish lakes reflects establishment of water mills and impassable dams ca. 600–800 years ago rather than a natural genetic population structure. Although effective population sizes of the two lake populations are not critically low they may ultimately limit response to selection and thereby future adaptation. Our results demonstrate that populations may have been affected by anthropogenic disturbance over longer time scales than normally assumed

Heritability of Morphology in Brook Trout with Variable Life Histories

Distinct morphological variation is often associated with variation in life histories within and among populations of both plants and animals. In this study, we examined the heritability of morphology in three hatchery strains of brook trout (Salvelinus fontinalis), which were historically or are currently used for stocking and supplementation of both migratory and resident ecotypes in the upper Great Lakes region. In a common garden experiment, significant variation in body morphology was observed within and across populations sampled at three time periods. The most notable differences among strains were differences in dorso-ventral body depth and the shape of the caudal peduncle, with some differences in the anterior-posterior placement of the dorsal and ventral fins. Variation with and among 70 half-sib families indicates that heritabilities of morphology and body size were significant at most developmental time points both within and across strains. Heritabilities for morphological characters within strains ranged from 0 to 0.95 across time points. Significant within-strain heritabilities for length ranged from 0 to 0.93 across time points and for weight ranged from 0 to 0.88. Significant additive genetic variation exists within and across hatchery brook trout strains for morphology and size, indicating that these traits are capable of responding to natural or artificial selection

The impact of fishing-induced mortality on the evolution of alternative life-history tactics in brook charr

Although contemporary trends indicative of evolutionary change have been detected in the life-history traits of exploited populations, it is not known to what extent fishing influences the evolution of alternative life-history tactics in migratory species such as salmonids. Here, we build a model to predict the evolution of anadromy and residency in an exploited population of brook charr, Salvelinus fontinalis. Our model allows for both phenotypic plasticity and genetic change in the age and size at migration by including migration reaction norms. Using this model, we predict that fishing of anadromous individuals over the course of 100 years causes evolution in the migration reaction norm, resulting in a decrease in average probabilities of migration with increasing harvest rate. Moreover, we show that differences in natural mortalities in freshwater greatly influence the magnitude and rate of evolutionary change. The fishing-induced changes in migration predicted by our model alter population abundances and reproductive output and should be accounted for in the sustainable management of salmonids

Effects of Body Condition on Facultative Anadromy in Brown Trout (Salmo trutta)

Fish behavior and life history is influenced by factors such as the environment, genetics, and their physiological state. One key life history stage in brown trout is decision to migrate to the sea or reside in the river. The energy status and body condition of the fish is thought to play a role in the timing and duration of migration to the sea. In this study, I examined the role of body condition in the initiation of this life history stage and determined the importance of feeding regimes in the physiological trade-off between migration and residency. I used four different feeding regimes in age one and age two cohorts of hatchery-reared brown trout to observe if starvation or feeding saturation induce behavioral changes in migration both in a controlled environment as well as a natural river system. I used both passive integrative transponder tags (PIT) as well as acoustic telemetry tags to analyze migration. I was successfully able to manipulate body condition using variable feeding regimes in both cohorts and I found that migration initiation and behavior was influenced by feeding regime. Feeding increased migration in both cohorts in the laboratory setting, but not in the natural setting. Laboratory migration in the age two cohort was primarily independent of feeding treatments as almost all age two fish migrated, but migration intensity was found to be greater with fed treatment groups. In contrast, age one fish were highly influenced by feeding regime, with fewer starved fish migrating and at a slower rate. Downstream migration in the wild was extremely low for both cohorts independent of feeding treatment. Overall, the findings indicate that age at release and feeding condition prior to release can impact migration initiation and duration. The results contribute to a better understanding of this complex life history stage and the mechanisms involved in the initiation, behavior, and survival of migrating brown trout

Effet de la sélection et du régime thermique subi par les géniteurs lors de la maturation sexuelle sur la croissance et la survie à l'éclosion et résorption du sac vitellin des alevins d'omble de fonataine (Salvelinus fontinalis). Contribution parentale dans la variance phénotypique

RÉSUMÉ: Dans le cadre du réchauffement climatique et de l'augmentation des connaissances sur l'épigénétique, cette étude fait partie d'un projet plus global visant à approfondir les connaissances sur la transmission intergénérationnelle d'informations liées aux conditions thermiques en période de maturation sexuelle chez l'omble de fontaine (Salvelinus fontinalis). Nous avons testé l'hypothèse que le régime thermique subi par les parents pendant la période de maturation sexuelle pourrait avoir des effets sur la survie, le volume du sac vitellin, le temps de développement et la croissance des alevins aux stades précoces de leur développement, soit à l'éclosion et à la résorption du sac vitellin. Nous avons également vérifié si la sélection génétique pour deux traits d'intérêt (maturation sexuelle tardive et croissance) a des effets, croisés ou non avec les effets de température, sur ces mêmes caractères. Pour ce faire, des croisements de géniteurs de la souche Laval, mais de deux lignées (sélection, contrôle), ont été maintenus soit à un régime thermique chaud, soit à un régime thermique froid (différence de 2°C) durant la période automnale. Suite aux croisements, les œufs et alevins de chaque famille ont été incubés, puis élevés séparément pour toute la durée du projet. Les alevins issus de parents ayant subi un régime thermique plus froid ont mis plus de temps à se développer entre l'éclosion et la résorption de leur sac vitellin. Mais, pour les traits de croissance et de survie, le régime thermique subi par les parents n'a pas induit de variations phénotypiques. Pour l'ensemble des traits, aucun effet d'interaction entre la lignée et le régime thermique subi par les géniteurs n'a été relevé. Dans l'ensemble, les effets parentaux sont significatifs sauf pour le temps de développement. Les effets maternels sont importants, mais diminuent à la résorption du sac vitellin. À ces deux stades de vie, les contributions paternelles sont très faibles, voire négligeables. -- Mot(s) clé(s) en français : régime thermique des parents, effet maternel, effet paternel, sélection, jeunes stades, croissance, survie, temps de développement. -- ABSTRACT: In the context of global warming and the growing interest on involvement of epigenetics in the adaptation processes, this study aimed to better understand the intergenerational transmission of information related to thermal conditions during sexual maturation in brook trout (Salvelinus fontinalis). We tested the hypothesis that the thermal regime experienced by breeders during sexual maturation may have effects on survival, yolk sac volume, developmental time and growth of fry at early developmental stages, both at hatching and at the yolk sac resorption stage. We also aimed to test whether directional genetic selection for two traits of interest (late sexual maturation and growth) for charr aquaculture significantly influenced whether or not crossed with temperature effects, the same traits. To do so, Laval strain breeders from two lines (selection, control) were submitted to either a cold water regime or a warm mater regime during the fall (2°C difference between the two). Crosses were done and incubation and fry rearing was done in a way that each family was kept separate for the whole duration of the project. Fry issued from breeders maintained at the coldest thermal regime showed a longer development time between hatching and yolk sac resorption. However, for growth and survival traits, the thermal regime experienced by the breeders did not induce phenotypic variations. For all the traits considered in this study, no interaction effect between the lineage and the thermal regime experienced by the breeders were found. Overall, parental effects were significant except for development time. Maternal effects were significant but decreased at the resorption of the yolk sac. At the two life stages considered, paternal contribution was very small to negligible. -- Mot(s) clé(s) en anglais : parental thermal regime, maternal effect, paternal effect, selection, young stages, growth, survival, development time

Description and prediction of broad-scale spatial variability in expression of anadromy in female Oncorhynchus mykiss in the John Day River, Oregon, USA

Partial migration is a common migratory behavior where some individuals in a population migrate and others do not. Patterns of partial migration can vary dramatically, especially for species that inhabit a wide range of environments. I described and predicted spatial variation in marine migration (anadromy) of female Oncorhynchus mykiss (steelhead and rainbow trout) in the John Day River catchment basin, Oregon. This large catchment (20,500 km2), where O. mykiss is known to exhibit partial migration, encompasses a broad range of environmental conditions. I collected 149 juvenile O. mykiss across 72 sites and identified locations used by anadromous females by assigning maternal origin (anadromous versus non-anadromous) to each juvenile. These assignments used comparisons of strontium to calcium ratios in otolith primordia and freshwater growth regions to indicate maternal origin. Individuals within sites were more likely to have the same maternal origin than expected at random (χ2 test, P < 0.001). I used logistic regression to predict probability of anadromy among sites in relation to stream size (as indicated by mean annual runoff). Stream size and maternal origin for single fish collected from 69 sites were used to construct a predictive model. I examined the ability of this model to predict new individuals at 47 of these sites (where a second fish was collected) using a variety of diagnostics, including kappa statistics and receiver operating characteristic curves. The model predicted anadromy in this second set of individuals with a moderate level of accuracy (e.g. 68% correctly predicted with a 0.5 classification threshold). Residuals from the models were not spatially autocorrelated, as indicated by Mantel tests. This result also suggested that remaining variability in the expression of anadromy was due to localized influences, as opposed to broad-scale gradients unrelated to stream size. The importance of stream size implies that occurrence of migratory females was related to environmental variability, but stream size is an indicator of many potential processes, and I was unable to identify a specific likely mechanism. However, I was able to demonstrate 1) that it is possible to predict the probability of anadromy across broad environmental gradients, and 2) the validity of a sampling approach that minimizes the need for sacrificial sampling of individuals. These results are important for the management of O. mykiss because anadromous individuals (steelhead) within the John Day River watershed are listed as a threatened species, and it is difficult to discern steelhead from non-anadromous individuals (rainbow trout). My results provide managers with the first broad-scale description and prediction of locations supporting anadromy, and provide a broad template that can guide future habitat restoration, monitoring, and research to better manage and understand the expression of anadromy in O. mykiss

Anadromy in brown trout (Salmo trutta): A review of the relative roles of genes and environmental factors and the implications for management and conservation

While many brown trout (Salmo trutta) populations spend their entire life cycle in freshwater, especially as river-lake migrants or river residents, others show facultative anadromy. That is, some trout migrate to sea while other individuals of the same population remain within their natal river. Sea trout can give rise to resident offspring and vice versa, although there is a strong tendency to track the parental life history. Anadromy delivers better feeding and thus larger size, which results in higher fecundity in females, enhanced mate choice, and other reproductive benefits. River residence, more prevalent in males as anadromy conveys fewer benefits, can give higher survival and avoids the energy expenditure required by anadromy. Overall, the costs and benefits of anadromy versus residency, measured in terms of survival and reproduction, are finely balanced and small changes to the cost-benefit equation can lead to evolutionary changes in life history. The decision to be anadromous or resident is a quantitative threshold trait, controlled by multiple genes and environmental factors. The dichotomous nature of the trait is postulated to be the result of the environmentally influenced physiological condition (e.g. energy status) relative to a genetically determined threshold. Anadromy ensues when an individual’s condition fails to meet the threshold level, which varies between sexes and among individuals and populations. Environmental factors and genetic architecture may also directly influence life history, e.g., by altering gene expression. A strong genetic influence on the anadromy decision means that facultative anadromy can be altered by natural selection driven by changes such as differential exploitation, stocking with farm-reared brown trout, partial barriers to migration, and changes in climate, and freshwater and marine productivity, together with parasite, pathogen and predator abundance resulting in reduced marine survival and growth. Further studies of the factors determining life history choice, together with multiple population estimates of heritability and differential reproductive success (fitness), are required to understand fully the impact of natural and anthropogenic environmental changes on sea trout dynamics

Early maturing males in a partially migratory population of anadromous and resident rainbow trout Oncorhynchus mykiss: influences of individual condition and stream temperature

Alternative male phenotypes in salmonine fishes arise from individuals that mature as either larger and older anadromous marine-migrants or as smaller and younger freshwater residents. Variability in age and size of males at maturity is hypothesized to be preceded by early differences in growth in size and lipid storage. Water temperature is one factor expected to influence growth and lipids. To better understand the processes influencing the expression of alternative male phenotypes, I examined the influence of growth in length (fork length) and whole body lipid content on freshwater maturing males in a mixed population of anadromous and resident rainbow trout (Oncorhynchus mykiss). I conducted this study in the John Day River basin in northeast Oregon where both anadromous and freshwater resident rainbow trout coexist. During the summer of 2007 I collected 168 age-1+ O. mykiss (80♀/88♂) nine months prior to the spawning season from thirty different streams. Water temperatures were recorded hourly in these streams from September 2007 through August 2008. Based on the temperature data I identified eight streams with contrasting thermal regimes and delineated those into two groups (warm and cold) to examine associations with growth and lipid storage. I determined sex and state of maturity visually and with the aid of microscopy. Length was measured in the field, age was estimated via otoliths and scales, and whole body lipid content was determined with the diethyl ether extraction method. Results indicated that larger males with higher lipid levels had a greater probability of maturing as a resident at age-1+ than smaller males with lower lipid levels. Among males, 40% were maturing and 80% of those fish had a length greater than 99 mm and whole body lipid content greater than 4% compared to only 19% of the immature males. Comparisons of streams with contrasting thermal regimes indicated that water temperature was associated with growth and lipid content in different ways. Growth was greater in the warm streams while whole body lipid content was higher in the cool streams. My results provide further support for the theoretical expectation that differences in individual condition precede male life history development and suggest that water temperature has a strong influence on the measures of condition commonly used to predict resident male maturity. However, my results also suggest that relationships between individual condition, maturation, and environmental variables (e.g., temperature) are complex and may represent influences of physiological, developmental, and evolutionary tradeoffs. This represents a first step towards understanding how individual condition and environment interact to influence the expression of alternative male phenotypes in rainbow trout