Evolutionary genetics of rainbowfish : phylogeny, adaptation and constraint

McGuigan, Katrina Louise. (2001). Evolutionary genetics of rainbowfish : phylogeny, adaptation and constraint PhD Thesis, School of Biological Sciences, The University of Queensland.

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Author McGuigan, Katrina Louise.
Thesis Title Evolutionary genetics of rainbowfish : phylogeny, adaptation and constraint
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2001
Thesis type PhD Thesis
Supervisor Mark Blows
Craig Franklin
Craig Moritz
Total pages 117
Collection year 2002
Language eng
Subjects L
270205 Genetic Development (incl. Sex Determination)
780105 Biological sciences
Formatted abstract
Freshwater fish are ideal models for evolutionary studies because of their discrete habitat associations and predictable paths for dispersal among populations. Rainbowfish (Melanotaeniidae) are one of the most common and widespread Australo-Papuan freshwater fish families. In this study I characterised rainbowfish genotype and phenotype at inter- and intra-specific levels to determine the processes of evolution responsible for generating the observed patterns of variation in genes, morphology, physiology and behaviour.

Neutral (mtDNA cytochrome b and control region) sequence variation was used to assess the role of major biogeographic barriers, the Central Highlands of New Guinea and the Torres Strait/Arafura Sea, in structuring diversity within Melanotaeniidae. Species within the family exhibited a pattern of sequence variation consistent with allopatric speciation influenced by biogeographic barriers. The Central Highlands of New Guinea underwent a period of major uplift approximately 5 myr ago. Mutual divergences between monophyletic clades of rainbowfish in northern, western and southern New Guinea were concordant with disruption of gene flow 5 myr ago, supporting the role of the Highlands in this divergence. Rainbowfish from southern New Guinea and Australia were polyphyletic. Variation in the age of divergence was consistent with episodic connection of the two landmasses, via the freshwater Lake Carpentaria, during periods of low sea level in the Pleistocene. Despite inconsistencies with current morphology-based taxonomy, the six major clades identified through the mtDNA phylogeny were supported by discriminant functions analysis of morphological variation. Identification of strong phylogenetic signal in morphological traits indicated that they had evolved through random genetic drift.

Three species of Melanotaenia inhabit the Atherton Tablelands of north Queensland and there has been extensive confusion over the taxonomic status of rainbowfish populations in the region. This study identified a cryptic, previously undescribed species, M. utcheensis. Although not sister species, M. utcheensis and M. eachamensis were both relatively ancient products of in situ speciation from an ancestral species that was distributed throughout east and west coast drainages. The third Atherton Tableland species, M. splendida splendida, was considerably younger and a recent colonist of the region. Within M. utcheensis there were two geographically segregated, morphologically distinct, divergent mtDNA lineages. Generally, all species exhibited extensive intraspecific variation in morphology such that the use of single populations to represent species-wide morphological variation probably contributed to past taxonomic confusion.

The cause of extensive intraspecific variation in rainbowfish was investigated by specifically considering the role of water velocity, which can influence morphology through demands on locomotion. Replicate natural populations of both M. eachamensis and M. duboulayi, allopatric species from east coast Austraha, were examined for morphology, sustained and burst swimming performance and red muscle area. This study revealed that the pattern of variation in these traits was similar in both species. Inter-habitat variation was greater than intra-habitat variation in both morphology and swimming performance. A common garden experiment identified a genetic basis to the variation. Morphological differences between lake and stream fish were consistent with hydromechanical predictions of reduced recoil (and maximised efficiency) during sustained body-caudal fin swimming in streams. Additionally, relative to lake conspecifics, M. duboulayi from streams had faster sustained, but slower burst swimming speeds, more red muscle and relied less on burst-coast swimming to achieve their fast sustained speeds. In M. eachamensis, stream fish likewise showed a reduced reliance on burst-coast swimming and had more red muscle. However, in contrast to both M. duboulayi and to their own locomotor morphology and behaviour, M. eachamensis from streams had faster burst, but slower sustained swimming speeds than fish from lakes. Evolution of the same, hydromechanically predictable, suites of traits in replicate lake and stream habitats indicated that natural selection repeatedly found the same morphological and physiological solutions to the challenge posed by water velocity.

The role of genetic constraint in determining the direction of morphological divergence between species (neutral divergence) and between water velocity habitats (adaptive divergence) was investigated using M. eachamensis and M. duboulayi. The heritability of morphological traits ranged from 11 % to 79%. Neutral divergence between species was strongly biased in the direction of maximum additive genetic variance, gmax- This indicated that drift-driven evolution was tightly genetically constrained. The direction of adaptive divergence between water velocity habitats was also biased in the direction of gmax- This bias was less than for neutral divergence, probably indicating the dissipation of the genetic constrait as populations approached their selective optimum. These results represent the first empirical evidence that, although both neutral and adaptive divergence occur in the direction of maximum genetic variance, genetic constraint is stronger, or more persistant, for divergence resulting from drift than for selection driven divergence.

Document type: Thesis
Collection: UQ Theses (RHD) - UQ staff and students only
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Created: Fri, 24 Aug 2007, 17:51:02 EST