Evolutionary and ecological genetic patterns of widespread unicornfishes: investigations of the non-geographic clades phenomenon

Horne, John Barton (2011) Evolutionary and ecological genetic patterns of widespread unicornfishes: investigations of the non-geographic clades phenomenon. PhD thesis, James Cook University.

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Abstract

The tropical Indo-Pacific is a very large biogeographic region stretching from the Red Sea to the central Pacific, yet in spite of its size nearly 500 species of shallow water teleost fishes are mostly cosmopolitan throughout this vast region. To date only a small number of these species have been phylogeographically studied across their entire species ranges and most show some genetic population structure, usually between ocean basins. However, some Indo-Pacific coral reef fishes have genetically homogenous populations across the Indo-Pacific suggesting high levels of gene flow. Among those fishes that lack spatial population partitions some possess nongeographic or temporal population structures in the mtDNA. This means that their populations are composed of genetically differentiated lineages that are sympatrically distributed. The biological significance of this pattern is unclear and only a small number of reef fish taxa have been reported to have non-geographic clades. The first species in which this pattern was detected was the big nose unicornfish, Naso vlamingii, which is a widespread Indo-Pacific Acanthurid with a long pelagic larval duration (Klanten et al. 2007). The explanation given by Klanten et al. for the nongeographic clades of this species was temporary periods of isolation, mediated by low-sea-level barriers and followed by secondary contact and admixture of lineages. Yet, while the conclusions of Klanten et al. (2007) seem plausible, further investigation into non-geographic genetic patterns was warranted.

In this thesis four additional Naso species were phylogeographically surveyed at a broad scale across the Indo-Pacific: Naso brevirostris, Naso unicornis, Naso hexacanthus and Naso caesius. Like N. vlamingii, all species showed little in the way of spatial population structuring using conventional phylogeographic fixation indexes (F(st)). Model-based phylogenetic analysis, maximum parsimony and Bayesian inference revealed non-geographic population patterns in the mitochondrial control region with N. brevirostris being the most similar to N. vlamingii. Curiously, the sister species N. hexacanthus and N. caesius were not reciprocally monophyletic suggesting that some horizontal gene transfer has occurred between them. Expansion time based on mismatch distributions was also calculated for each species and each clade. Mismatch coalescence suggests mid-late Miocene expansion times for all taxa (considering N. hexacanthus and N. caesisus as a single taxon) and pre-Pleistocene expansion for non-geographic clades.

Coalescence age of species and clades was also assessed in the program BEAST using a fossil calibrated molecular dating and a relaxed molecular clock. For this analysis all Naso species previously mentioned, including N. vlamingii, were arranged into an interspecific phylogeny of cytochrome oxidase subunit one DNA sequences, with many representatives of each species and clade. Mean ages from this anaylsis suggest mid-miocene coalescence ages for each taxa and pre-Pleistocene coalescence for all non-geographic clades, indicating that Pleistocene processes probably do not account for non-geographic patterns in the genus Naso. Otherwise, little congruence could be found between the ages of clades, seemingly refuting the notion that a barrier was involved in the formation of these genetic features. Fossil calibrated coalescence ages were used to reconstruct demographic history of each species using Bayesian skyline plots. In all taxa, skyline plots suggest accelerated demographic expansion during the Pleistocene, rather than the bottlenecks or demographic decline expected based on the pretext that reef fishes suffered bottlenecks during the upheavals on coral reefs during the Pleistocene glacial cycles.

Complimentary to evolutionary genetic patterns, this thesis also includes a genetic survey of recently settled N. unicornis juveniles in the Marianas archipelago, using 12 polymorphic microsatellite loci and sequences from the mitochondrial control region. This particular study reveals that post-settlement larval pools of N. unicornis have an elevated genetic diversity in both the nuDNA and mtDNA relative to the preexisting adult population. Recruitment events are genetically unstructured in space and time in this species within the Marianas and recruits seemed likely to have sibling relationships among sampling locations and between year classes. The genetic diversity of larval pools, as well as the likelihood of sibling pairs to be separated in space and time suggests demographically open populations. In light of the phylogeography of this species, N. unicornis and its congeners most likely experience high levels of gene flow on ecological as well as evolutionary time frames.

Non-geographic clades appear to be a genetic phenomenon observed in some widespread and highly dispersive coral reef fishes of the lndo-Pacific. There was little evidence to suggest that a low-sea-level barrier to gene flow was associated with these clades. Most likely non-geographic clades arise as a consequence of rapid range expansion across patchily distributed coral reef habitat in a large biogeographic region. The sheer size of the Indo-Pacific appears to be an important factor shaping the population patterns of widespread cosmopolitan coral reef fishes.

Item ID: 38033
Item Type: Thesis (PhD)
Keywords: Acanthurid; Acanthuridae; clades; coral reef fish; genetic patterns; genetics; Indo-Pacific; Naso; phylogenetics; populations; recruitment; unicorn fish; unicornfishes
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Horne, John B., McIlwain, Jennifer L., and Van Herwerden, Lynne (2009) Isolation of 15 new polymorphic microsatellite markers from the blue-spine unicornfish Naso unicornis. Conservation Genetics Resources, 2. pp. 1-4.

Chapters 3 & 4: Horne, John B., van Herwerden, Lynne, Choat, J. Howard, and Robertson, D.R. (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Molecular Phylogenetics and Evolution, 49 (2). pp. 629-638.

Date Deposited: 05 Aug 2015 05:51
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070405 Fish Physiology and Genetics @ 50%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 50%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 50%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
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