Genetic basis and fitness consequences of migration in facultatively anadromous brown trout Salmo trutta

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Wynne, Robert
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University College Cork
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Animal migration is a widespread, but complex phenomenon, that evolves in response to spatial, temporal or ontogenetic separation of optimal feeding and breeding habitats. Considerable diversity in migratory behaviours and associated physiological, morphological and life-history traits can occur even within a single species, making it challenging to understand the various evolutionary and ecological processes involved. This thesis focuses on brown trout (Salmo trutta) as an excellent model species to study the drivers and consequences of alternative migratory tactics, as they display a vast continuum of migratory life histories, even within one population. Until recently, relatively little was known about the genetic mechanisms and selective pressures shaping the huge variation in migratory life histories in brown trout and other salmonids. Advances in molecular biology (the ‘omics revolution’), coupled with increasingly sophisticated telemetry techniques for studying movement behaviours in the wild, are now facilitating improved understanding of how migratory phenotypes are shaped by complex interactions between genes and environment. This, in turn, informs conservation and management of facultatively anadromous species in rapidly changing environments. The overarching aims of this thesis are to provide a deeper understanding of the genetic/evolutionary basis of migration in brown trout, but also to use genetics as a tool to gain insights into basic aspects of brown trout biology. The first data chapter (Chapter Two of the thesis) involved a common garden experiment undertaken in the Burrishoole catchment (northwest Ireland), which tested for heritable differences in migratory life history among geographically proximate, partially reproductively isolated, brown trout populations. Six different types of genetic crosses were made using wild-sourced broodstock. The progeny were then released into an experimental section of the Srahrevagh River (Burrishoole catchment) and their subsequent fates and movements tracked across three years using electrofishing surveys, trapping facilities and passive integrated transponder (PIT) telemetry, coupled with genetic parentage assignment (microsatellite markers) to assign sampled juveniles back to genetic cross types. The key findings of this chapter were that early movement behaviours (emigration from the river) and smolting rates (emigration to sea) differed among cross types, consistent with there being a quantifiable genetic basis to alternative migratory tactics. The contemporary sea trout run in the Burrishoole system is a remnant of what it once was, yet the numbers of resident/potamodromous brown trout remain apparently healthy. The results of Chapter Two imply that rapid evolutionary responses to anthropogenic environmental change could partially explain this switch away from anadromy towards residency. Although it has long been known that migrants and residents can co-occur within the same trout population, the underlying molecular mechanisms driving alternative life histories has remained poorly understood. Therefore, in Chapter Three, I performed transcriptional profiling (RNA sequencing or “RNA-seq”) of brain and liver tissues collected from immature brown trout smolts (migrants) and mature residents, in the context of a tank-based laboratory experiment. The results stated in chapter three provide new insights into tissue - and sex-specific gene expression patterns and associated molecular processes (particularly metabolism-associated pathways within the liver) that underlie the production of alternate migratory life histories and physiologies. In Chapter Four I then examined a different but related aspect of phenotypic diversity in brown trout, namely the long-recognised yet poorly understood phenomenon of autumn versus spring outmigration (from the river into sea), using genetic identity analysis complemented with physical tagging (PIT telemetry) within a wild population of brown trout located in northwest Ireland (Burrishoole catchment). Both autumn and spring migrants exhibited a sex bias towards females, but was stronger in spring than in autumn outmigrants, implying that the fitness costs and benefits of adopting either strategy may differ between the sexes. Crucially, I also found that autumn outmigrants returned to freshwater at a similar rate and only slightly smaller size than spring outmigrants, despite the former category being much smaller on leaving freshwater and spending longer away overall than the latter category. These findings suggest that autumn outmigrants are not a demographic dead-end and may be key contributors to the overall gene pool. There is a brackish lagoon (Lough Furnace) at the freshwater-marine interface in this catchment that may support the maintenance of these evolutionarily important alternative migratory tactics. My results emphasise how autumn outmigrating trout, and the transitional habitats that support their existence, should not be overlooked in the context of evolutionarily enlightened fisheries management. Collectively, the body of work presented in this thesis has shed new light on the molecular mechanisms and ecological/evolutionary processes involved in facultative animal migration and the maintenance of intraspecific phenotypic diversity in a culturally and economically important fish species. It is increasingly apparent that a “one size fits all” approach to management and conservation is suboptimal for species exhibiting complex life history patterns where a single population may express multiple life histories concurrently including for example as observed here partial migration and run time variation. Future genomics, transcriptomics and epigenomic work, coupled with detailed behavioural and physiological investigations, will aid progress towards a more holistic understanding of the evolutionary ecology of migration.
Anadromy , Genetics , Life history variation , Salmonids , Migration
Wynne, R. 2023. Genetic basis and fitness consequences of migration in facultatively anadromous brown trout Salmo trutta. PhD Thesis, University College Cork.
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