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What Makes a Ferox? the Drivers and Consequences of Alternative Life History Strategies in S

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What Makes a Ferox? the Drivers and Consequences of Alternative Life History Strategies in S Hughes, Martin Robert (2017) What makes a ferox? The drivers and consequences of alternative life history strategies in S. trutta. PhD thesis. https://theses.gla.ac.uk/8280/ Copyright and moral rights for this work are retained by the author A copy can be downloaded for personal non-commercial research or study, without prior permission or charge This work cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Enlighten: Theses https://theses.gla.ac.uk/ [email protected] WHAT MAKES A FEROX? THE DRIVERS & CONSEQUENCES OF ALTERNATIVE LIFE HISTORY STRATEGIES IN S. trutta MARTIN ROBERT HUGHES BSC, UNIVERSITY OF GLASGOW, 2012 SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY SCOTTISH CENTRE FOR ECOLOGY AND THE NATURAL ENVIRONMENT, INSTITUTE OF BIODIVERSITY, ANIMAL HEALTH AND COMPARATIVE MEDICINE, COLLEGE OF MEDICAL AND LIFE SCIENCES, UNIVERSITY OF GLASGOW January 2017 © MARTIN ROBERT HUGHES 2017 ABSTRACT Understanding the mechanisms involved in producing and maintaining variation in phenotype, behaviour and life history traits within a single species, is of fundamental importance to evolutionary biology. Such intraspecific variation is well observed in organisms inhabiting depauperate environments, exploiting uncontested trophic niches. Classic examples can be found in island communities such as Darwin’s Finches of the Galapagos Islands and the Anolis lizards of the Caribbean, where organisms derived from a single invading ancestor rapidly diversified into numerous ecologically distinct niches, forming distinct and often reproductively isolated populations. Such adaptive radiations are considered an essential prerequisite to species formation and is often referred to as ecological speciation. Freshwater lakes share characteristics similar to islands that enable ecological speciation to occur rapidly. The rapid proliferation of African cichlids species in the African Great lakes is perhaps the best example of ecological speciation found on Earth today. Thousands of species of African cichlids have been described within Lakes Malawi, Tanganyika and Victoria each adapted, often morphologically, to a particular ecological niche. Fish species inhabiting post-glacial lakes of the Northern hemisphere represent model organisms to study the early mechanism of ecological speciation. Species such as Arctic charr and Three-spine sticklebacks have diverged across ecological axes within a single lake in numerous systems. As post-glacial lakes were inaccessible to ancestral fish until the last glacial retreat, (approximately > 15 000 years ago) the observed divergences have occurred in an extremely short amount of time. Brown trout Salmo trutta can exhibit multiple life histories within a single lacustrine system, including benthic, pelagic and piscivorous forms. The piscivorous form, known colloquially as ferox trout, are a relatively rare, understudied form of the S. trutta species complex. Interestingly ferox trout not only exhibit discrete morphology and foraging behaviour they also have higher growth potential, delayed maturation and extended longevity compared with sympatric S. trutta. Indeed, ferox trout represent a genetically distinct ancestral lineage in some locations where they occur, however the ecological, physiological and behavioural mechanisms driving the production of ferox trout populations has yet to be investigated. Thus, the thesis presented here tests the importance of different drivers in ferox trout production to increase our understanding of species formation and ecological speciation. Furthermore, I also investigated the within lake movements (home range, core range, speed) of benthic and pelagic S. trutta occurring in sympatry to determine 2 differential habitat use. In the General Introduction (chapter 1) I extensively review the available literature on adaptive radiations and ecological speciation with a particular emphasis on fish in post-glacial lakes. I discuss the history of ferox trout to contextualise the current thinking and to highlight knowledge gaps within the research. To investigate the ecological drivers of ferox trout populations, fine scale environmental characteristics associated with known ferox trout populations were investigated. I found large, deep lakes with populations of S. alpinus were highly correlated with ferox trout populations. I found 192 lakes in Scotland have evidence of supporting ferox trout and 366 lakes in Scotland could theoretically support ferox trout based on lake area alone (chapter 2). The alternative growth strategies and life spans exhibited by ferox trout and sympatric benthivorous brown trout (benthivorous trout hereafter), were examined by comparing the growth trajectories and age structures of three sympatric populations (Loch Rannoch, Loch Awe and Loch na Sealga). In Loch Rannoch, the ferox population adhered to the conventional model of growth proposed for ferox trout, i.e. relatively slow growth followed by an acceleration of growth after a switch to piscivory, however the two other populations did not conform to this model of growth. In Loch Awe, ferox trout grew much faster than benthivorous trout, including early ontogeny, however in Loch na Sealga there were no measurable differences in growth. Interestingly, all ferox trout populations were older than benthivorous trout. These results demonstrate that there are multiple ontogenetic growth pathways to achieving piscivory in S. trutta and that the adoption of a piscivorous diet may be a major factor contributing to extension of life span in S. trutta (chapter 3). Physiological, morphological and behavioural drivers were investigated by rearing full-sibling families of sympatric ferox trout and benthivorous brown trout from eggs in the laboratory, under common garden conditions. I found offspring from ferox trout parents had higher survival rates, larger yolk sacs and decreased levels of mesenteric fat, compared with offspring from sympatric benthivorous trout. Offspring of ferox trout and benthivorous trout also had distinct head shape morphology, which converged over time under common garden conditions (chapter 4). Offspring from ferox trout were more dominant than size-matched offspring from sympatric benthivorous trout, by examining food acquisition ability, spatial position, flank colour index and aggressive interactions within a semi-natural stream system (chapter 5). Lastly, the within lake movement of sympatric benthic and pelagic S. trutta was investigated by acoustic telemetry. Acoustic tags were surgically implanted into S. trutta exhibiting distinct head morphologies associated with trophic position in an oligotrophic 3 post-glacial lake. Tagged S. trutta were tracked over a three-month period (July-September). No differences in home range or core area size (km2) between benthic and pelagic S. trutta were identified. However, both forms demonstrated clear diel cycles in movement and responded similarly to temporal change. There was extensive overlap in core use of the lake, however pelagic trout were found over deeper waters more often than benthic trout (chapter 6). In the general discussion (chapter 7), I summarise the results of these studies and discuss the evolutionary, conservation and economic importance of such research. I also discuss the limitations of this research and the potential future areas of study. 4 “It seems to me that the natural world is the greatest source of excitement; the greatest source of visual beauty; the greatest source of intellectual interest. It is the greatest source of so much in life that makes life worth living.” SIR DAVID ATTENBOROUGH “When you want to succeed as bad as you want to breathe, then you will be successful.” ERIC THOMAS 5 CONTENTS CHAPTER 1. GENERAL INTRODUCTION. 1.1. HISTORY OF EVOLUTIONARY THEORY ........................................... 20 1.2. ADAPTIVE RADIATION .............................................................. 21 1.3. ECOLOGICAL OPPORTUNITY ....................................................... 22 1.3.1. NEW RESOURCES ................................................................. 22 1.3.2. MASS EXTINCTION ................................................................ 23 1.3.3. EVOLUTION OF NOVEL TRAITS ................................................. 23 1.3.4. COLONISING NEW HABITAT ..................................................... 23 1.4. PHENOTYPIC PLASTICITY ......................................................... 24 1.5. TROPHIC NICHE SPECIALISATION ................................................. 25 1.6. REPLICATED ADAPTIVE RADIATION .............................................. 26 1.7. POST GLACIAL LAKES ............................................................... 28 1.7.1. THREE-SPINE STICKLEBACKS ................................................... 28 1.7.2. RAINBOW SMELT ................................................................. 29 1.7.3. LAKE WHITEFISH ................................................................. 30 1.7.4. ATLANTIC SALMON ............................................................... 31 1.7.5. ARCTIC CHARR ................................................................... 32 1.7.6. BROWN TROUT ..................................................................
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