Molecular phylogeny, temporal patterns of lineage diversification and phylogeography of the surgeonfish genus Naso (Acanthuridae)

Klanten, Selma O. (2003) Molecular phylogeny, temporal patterns of lineage diversification and phylogeography of the surgeonfish genus Naso (Acanthuridae). PhD thesis, James Cook University.

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Abstract

A species-level phylogeny was constructed for all described (19) Naso species (Family: Acanthuridae) using three markers in combination, one nuclear (ETS2) and two mitochondrial (16S rRNA and cytochrome b). A number of taxa representing species from all acanthurid genera were included to generate a genus-level (total of 38 species) phylogeny of the order Acanthuroidei (surgeonfishes). Maximum likelihood, maximum parsimony and Bayesian inference analyses produced similar tree topologies, which confirmed the previously proposed genus-level relationships and resolved for the first time inter-specific relationships of all species of the monophyletic genus Naso. Species of the genus Naso segregated into four major sub-clades, with members of the subgenus Axinurus appearing basal. This molecular phylogeny was then used to examine hypotheses about the evolutionary relationships among species of Naso. This study demonstrates that distinct foraging modes and specialised body shapes arose independently at different times in the evolutionary history of the genus. Members of the subgenus Axinurus, characterised by a scombriform morphology, caudal fin structure and pelagic foraging mode, were consistently placed basal to the remaining Naso species, suggesting that pelagic foraging is plesiomorphic and benthic foraging derived in this genus. The genus-level phylogeny (nuclear marker, ETS2) was used to obtain a range of age estimates for the most recent common ancestor of the genus Naso. These age estimates (range of 52MY to 43.3MY) were then used to estimate divergence times (by nonparametric rate smoothing method) of the nodes, giving rise to extant Naso species using the combined sequence data (from all loci). The reconstruction of the pattern of divergence of extant species indicates two sequences of events. The basal species characterised by pelagic foraging modes arose during the Eocene and Oligocene. Most of the remaining Naso species, including those characterised by benthic foraging, arose over a period of 20MY during the Miocene. Diversification during this period was associated with major plate tectonic and glaciation events, resulting in changes in sea level, ocean temperature and productivity regimes. To examine further speciation events and the underlying processes, several comparative phylogeographic studies were undertaken. For this purpose, a Naso-specific fast evolving mitochondrial marker was designed from the control region (d-loop). Firstly, a widely distributed species N. vlamingii, was selected to examine genetic connectivity and diversity throughout its distribution in the Indo-Pacific Ocean. Although very weak (overall Fst 0.005) genetic differentiation was obtained for this species over its sampled range, suggesting gene flow, there was some evidence of isolation by distance at the largest spatial scale (between Seychelles and the Philippines). This however, may be due to lack of samples from the Indian Ocean. There was no subdivision into distinct geographic regions, hence no evidence of cryptic speciation across the range sampled in this study, despite the presence of the central Indian Ocean barrier in its distribution range. Diversity indices (haplotype, h and nucleotide, p) were extremely high (h = 1.0 and p = 15.1%), indicating that this species has had a long, but unstable evolutionary history, which has repeatedly allowed populations to diverge in isolation and to make secondary contact subsequently. A haplotype tree identified deep divergences for this species, suggesting that isolated populations diverged at times of low sea level. The lack of geographic partitioning in this species suggests that secondary contact was made between previously isolated and divergent populations at times of elevated sea level. The high dispersive capacity of the species is what allows secondary contact to occur between temporarily isolated populations. Additionally, two sister species pairs were selected for comparative phylogeographic studies. One pair (N. lituratus– N. elegans) spanned the same distribution range as N. vlamingii, but the species pair was partitioned by ocean basins across this range (Indian- /Pacific Ocean). The second pair (N. tuberosus – N. tonganus) has an even more restricted distribution range (west Indian-/west Pacific Ocean) and was also partitioned by ocean basins. The two sister species diverged allopatrically, and species of both sister pairs (N. lituratus– N. elegans and N. tuberosus – N. tonganus) segregated into distinct clades. There was no distinct geographic subdivision throughout the sampling range for any of these species. Instead, low levels of genetic differentiation were recorded among populations of each species (overall Fst values ranged from 0.005 to - 0.001) suggesting high levels of gene flow. Despite the presence of gene flow among populations there was some indication of reduced gene flow across the Indian Ocean (between Amirante of Seychelles and Cocos Keeling Island) for N. elegans. There was no indication of gene flow between species in either of the sister pairs (N. lituratus – N. elegans Fst =0.75 and N. tuberosus – N. tonganus Fst =0.71), despite the fact that each pair was considered a single species as recently as 2001 and 2002 respectively. This indicates reproductive isolation, despite the potential for extensive dispersal in these species. The diversity indices were high for all of the species (h = 0.90 – 1.00, p = 9.0 – 11.6%; h = 1.00, p = 4.2 – 6.4% respectively), indicating deep divergences between haplotypes, as was the case for N. vlamingii. Several factors probably contribute to the population genetic structure of all five species: certain life history traits such as an extensive pelagic larval duration (up to 3 months) in combination with the ability of larvae to swim actively for extended periods, their long evolutionary history, the longevity (reach 30 – 40 years) and relatively short time to reach reproductive maturity coupled with overlapping generations (offspring) reproducing. The dispersive capacities of N. vlamingii are clearly the greatest of the five species studied, and may be attributed to the semi-pelagic adult lifestyle combined with the pelagic larval duration and a generalist dietary habit of this species. This study has demonstrated that by applying a hierarchical approach (phylogenetic, temporal, and phylogeographic) in combination with biological, ecological and historical perspectives, it has been possible to elucidate the processes important in the diversification of the genus Naso.

Item ID: 82
Item Type: Thesis (PhD)
Keywords: Surgeonfish, Naso(Acanthuridae), Molecular phylogeny, Temporal patterns, Lineage diversification, Phylogeography
Date Deposited: 03 Aug 2006
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060409 Molecular Evolution @ 25%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 50%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 25%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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