Author's School

Graduate School of Arts & Sciences

Author's Department/Program

Biology and Biomedical Sciences: Evolution, Ecology and Population Biology


English (en)

Date of Award

January 2010

Degree Type


Degree Name

Doctor of Philosophy (PhD)

Chair and Committee

Allan Larson


This dissertation describes the evolutionary history of Moray eels: Muraenidae). Moray eels are apex predators on coral reefs around the world, but they are not well studied because of their cryptic habitats and occasionally aggressive behaviors. I provide the first molecular phylogeny of moray eels with widespread taxonomic and geographic coverage, including 44 species representing two subfamilies, eight genera, and all tropical ocean basins. Phylogenetic relationships among these taxa are estimated from portions of mitochondrial loci cytochrome b and cytochrome oxidase subunit 1, and portions of the nuclear loci RAG-1 and RAG-2. I test four sets of contrasting phylogenetic hypotheses using standard topological tests. First, my phylogeny statistically supports the taxonomic distinction between true morays: Muraeninae) and snakemorays: Uropterygiinae). Second, I demonstrate that the durophagous characters: shell crushing jaws) of the genera Gymnomuraena and Echidna are not homologous. Third, I demonstrate that durophagous morphological characters have evolved in parallel in an ancestor of Gymnomuraena and at least three additional times within the genus Echidna. Finally, the tree topology indicates multiple invasions of the Atlantic from the Indo-Pacific, one of these occurring immediately prior to formation of the Isthmus of Panama approximately 2.8 MY ago and one or two others occurring in the early to mid Miocene. Cladogenesis occurring within the Atlantic during the mid Miocene and Pliocene also contributed to moray species diversity. These data include a pair of sister species separated by the Isthmus of Panama, allowing a time-calibrated tree with an estimated crown age for Muraenidae at between 41 and 60 MY ago, consistent with fossil evidence. Most lineage accumulation within morays occurred from the late Pliocene: ~25 MY ago) through the Miocene: 5-23 MY ago). This dissertation also examines phylogeographic patterns of diversification within morays. Reef fishes disperse primarily as oceanic "pelagic" larvae, and debate continues over the extent of this dispersal, with recent evidence for geographically restricted: closed) populations in some species. In contrast, moray eels have the longest pelagic larval stages among reef fishes, possibly providing opportunities to disperse over great distances. I test this prediction by measuring mtDNA and nuclear DNA variation in two species of moray eels, Gymnothorax undulatus: N = 165) and Gymnothorax flavimarginatus: N = 124), sampled at 14-15 locations across the Indo-Pacific. The mtDNA data comprise 632 bp of cytochrome b and 596 bp of cytochrome oxidase I. Nuclear markers include two recombination-activating loci: 421 bp of RAG-1 and 754 bp of RAG-2). Analyses of molecular variance: AMOVA) and Mantel tests indicate little or no genetic differentiation, and no isolation by distance, across 22,000 km of the Indo-Pacific. I estimate that mitochondrial genetic variation coalesces within the past ~2.3 million years for G. flavimarginatus and within the past ~5.9 million years for G. undulatus. Permutation tests of geographic distance on the mitochondrial haplotype networks indicate recent range expansions for some younger haplotypes: estimated within ~600,000 years) and episodic fragmentation of populations at times of low sea level. My results support the predictions that the extended larval durations of moray eels enable ocean-wide genetic continuity of populations. This is the first phylogeographic survey of the moray eels, and morays are the first reef fishes known to be genetically homogeneous across the entire Indo-Pacific. Finally, this dissertation uses comparative phylogeography to examine the effects of niche breadth on population genetic structure. The effects of niche breadth on range size, rarity, and extinction risk have been well explored. However, the ability of niche breadth to affect population structure within species has never been examined in a comparative framework, possibly due to the unique set of conditions necessary for such a test. Population structure is often a result of differential gene flow among populations, and gene flow can be affected by both the vagility of an organism or its gametes: dispersal capability), or by the variety of habitats that an organism can occupy within its dispersal capabilities: niche breadth). While niche breadth has been shown to affect range size and rarity more than dispersal capability, it is unclear if this pattern extends to population genetic structure within species. I make use of a unique characteristic of moray eel: Muraenidae) biogeography. Moray eels are cosmopolitan species with the lowest level of endemism among the 4000+ species of reef fishes, and while many species exist in a variety of habitats throughout their range, other species with identical ranges occupy only a small subset of those habitats, and have a diet that is also a specialized subset of the habitat generalists' diet. I compare measures of population genetic structure in two broad-niche species of moray eels: Gymnothorax flavimarginatus, G. undulatus) with two co-distributed but more specialized narrow-niche species of moray eels: Echidna nebulosa and Gymnomuraena zebra) throughout the Indo-Pacific. I report molecular genetic data for E. nebulosa and G. zebra using molecular markers orthologous to those used for G. flavimarginatus and G. undulatus for geographically overlapping sampling localities. I estimate geographic distributions of the four moray species using geographic information systems to delimit the distributions of habitats favorable for each species. Despite an 80% reduction in available habitat within the narrow-niche species and comparable dispersal capabilities, each of the four species shows high levels of connectivity throughout their respective ranges. These results indicate that in broadly-distributed species with high dispersal capabilities, niche breadth may have little to no effect on population structure.


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