The evolutionary ecology of lampreys (Petromyzontiformes)

Hume, John B. (2013) The evolutionary ecology of lampreys (Petromyzontiformes). PhD thesis, University of Glasgow.

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Abstract

Lampreys (Petromyzontiformes) are an ancient vertebrate group, comprising 40 currently recognised species that range throughout the Northern and Southern Hemispheres. Despite a conserved morphology, lampreys nevertheless express a diverse range of life history strategies. Unusually for vertebrates larval lampreys are filter-feeding organisms prior to undergoing an extensive anatomical reorganisation, and the adoption of either a parasitic or a non-parasitic adult life. Parasitic lampreys consume the flesh and blood of actinopterygian fishes, either in marine or freshwater environments, while non-parasitic lampreys do not feed following their metamorphosis from the larval form. Morphological and genetic similarities between pairs of parasitic and non-parasitic lampreys have led to taxonomic confusion regarding the specific status of many non-parasitic forms, and the suggestion that the loss of the trophic adult phenotype is the result of a single species capable of producing alternative life history strategies. In this thesis it is argued that at least some paired species of lampreys do not comprise two distinct evolutionary lineages; rather, that non-parasitic lampreys represent one extreme in a continuum of life history variation expressed by a parasitic species. Some lamprey species, such as the European river lamprey Lampetra fluviatilis, are morphologically variable, exhibiting divergent phenotypes in response to ecological pressures, such as alternative foraging environments. Loch Lomond, Scotland contains a population of L. fluviatilis that feeds exclusively in the lake and exhibits a reduced body size and an overall morphology distinct from the typical anadromous form. Its foraging strategy indicates that it may be capable of switching hosts in the face of declining numbers of a presumed favoured and formerly abundant host, suggesting a certain amount of plasticity in its trophic ecology that may have ensured its survival in this freshwater lake. This freshwater-resident form, as well as anadromous L. fluviatilis and the non-parasitic species L. planeri, were found to spawn in a single river system within the Loch Lomond basin, and this site is crucial for the continued presence of this life history variant in Loch Lomond. The appearance of sexually mature specimens of three discrete phenotypes in this river, each representing an alternative life history strategy that may, or may not, belong to a single species, provides a crucial opportunity to test the strength of assortative mating between lamprey species pairs. Within this system the strength of assortative mating was found to be weak, and points to the possibility that freshwater-resident L. fluviatilis are mitigating gene flow between large anadromous parasitic L. fluviatilis, and small, non-parasitic L. planeri. As well as weak behavioural isolation, inter-specific sneak male mating tactics were documented among these populations, and represents the first time this phenomenon has been observed between paired lamprey species. Such behaviour indicates a lack of species-specific cues acting between L. fluviatilis and L. planeri, and suggests that hybrid offspring could be common in some systems. Testing hybrid viability (survivorship) between Loch Lomond’s two L. fluviatilis life history strategies and the sympatric L. planeri revealed no post-zygotic barriers to gene flow, at least in the form of gamete incompatibility. Perhaps more convincingly though, when comparing traditional morphometrics and body shape variation, as well as mitochondrial DNA sequences, between L. fluviatilis expressing different foraging strategies with populations of L. planeri, no robust species specific differentiation was observed. In fact, species delimitation between L. fluviatilis and L. planeri appears to be related solely to overall body size, which is itself a function of life history strategy. However, life history strategy was not correlated with current species designation as relationships among mtDNA haplotypes indicate non-parasitic populations have evolved independently multiple times throughout the geographic range of L. fluviatilis in Europe. Therefore, L. planeri should not be considered as a distinct species, either morphologically or genetically. Instead, L. fluviatilis appears capable of expressing a range of life history strategies; from parasitic anadromous populations through to non-parasitic stream-resident populations. The overall research approach employed in this thesis, i.e., the combination of ecological, behavioural, taxonomic and molecular studies, could be used to robustly examine the evolutionary ecology of parasitic and non-parasitic lampreys elsewhere.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Additional Information:
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ication in the Journal of Fish Biology [Hume, J. B., Adams, C. E., Bean, C. W. &
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l Heritage [Hume, J. B. (2011). Adult lamprey survey of the Endrick Water SSSI &
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blication in the Journal of Fish Biology [Hume, J. B., Adams, C. E., Mable, B. &
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iological Journal of the Linnean Society [Hume, J. B., Adams, C. E., Mable, B. &
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X 7.2 has been accepted for publication in The Glasgow Naturalist [Hume, J. B. &
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Keywords: Lamprey, evolution, speciation, freshwater, Loch Lomond, Endrick
Subjects: Q Science > QH Natural history
Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Funder's Name: UNSPECIFIED
Supervisor's Name: Adams, Prof. Colin E.
Date of Award: 2013
Depositing User: Dr John Breslin Hume
Unique ID: glathesis:2013-4125
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 16 Apr 2013 13:33
Last Modified: 16 Apr 2013 13:33
URI: http://theses.gla.ac.uk/id/eprint/4125

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