Patterns and processes of diversification in groupers (family: Epinephelidae)

Ma, Ka Yan (2014) Patterns and processes of diversification in groupers (family: Epinephelidae). PhD thesis, James Cook University.

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Abstract

This thesis examines the patterns and processes whereby coral reef fish biodiversity is generated and distributed. Molecular, fossil, ecological and geographical data were used to reconstruct the spatial-temporal diversification pattern of groupers (Family: Epinephelidae), a diverse, species-rich reef fish family, at three hierarchical levels. First, I used a comprehensive time-calibrated molecular phylogeny coupled with ancestral range reconstruction of groupers to examine the impact of Cenozoic geological and climatic change on the evolution of groupers. The historical processes that generated and maintained contemporary marine biodiversity hotspots in the Indo-Pacific and The tropical Atlantic + East Pacific (TAEP) biogeographic realms were also investigated. Then, recently developed Bayesian coalescence modeling was used to reconstruct the species phylogeny of the grouper genus Plectropomus. Combined with ancestral range reconstruction and ecological information, I explored the modes of speciation within this genus. Finally, I investigated the effect of Pleistocene climatic fluctuations on the intra-specific evolutionary history of a commercially important, widespread grouper species in the Indo-Pacific, Plectropomus areolatus, as a model. Population genetic structure, demographic history, and gene flow patterns were assessed using mitochondrial control region sequences and microsatellite loci.

At the family level, a comprehensive time-calibrated phylogeny of Epinephelidae identified a mid-Eocene origin of the family. Groupers diverged sequentially to form six strongly supported main clades. The clade containing Variola, Gonioplectrus, Saloptia and Plectropomus occupied the basal position, while the crown group harboured Epinephelus, Cromileptes and Anyperodon. My results questioned the monophyly of Cephalopholis, Hyporthodus, Mycteroperca, Epinephelus and the reticulated-grouper complex. In general, episodes of global cooling and oceanographic changes during the late Eocene and mid-Miocene were associated with the origins and rapid radiation in grouper clades, while tectonic movements such as the terminal Tethyan event during the early to mid-Miocene and the rise of the Isthmus of Panama during the Pleistocene instigated vicariant grouper divergences. However, the six clades exhibit substantial differences in age, geographic origins and temporal-spatial diversification patterns.

Considering spatial context, a history of connectivity is found in Indo-Pacific epinephelids, where regional origination contributed significantly to generating grouper biodiversity. In contrast, a history of isolation was evident in the TAEP epinephelids, with a stronger influence of vicariant events (mostly due to the Isthmus of Panama Barrier) in cladogenesis. The regional epinephelid biodiversity hotspots - the Indo-Australian Archipelago (IAA) and the Caribbean - were only in place from the Pliocene. Both hotspots supported minor regional origination and acted predominantly as biodiversity sinks throughout epinephelid history. The results suggested that the extensive coral reefs in the biodiversity hotspots supported abundant immigrants, rendering the hotspots the centres of survival throughout grouper evolutionary history. Hence, the cradles of grouper origination were in less coral-rich, peripheral regions. This finding prompted further investigations of grouper speciation mechanisms, especially in peripheral regions.

At the genus level, species tree analysis identified a late Miocene origin of Plectropomus. A variety of speciation processes were evident from ancestral range reconstruction, including potentially sympatric divergences in the IAA associated with sister species habitat preference differences, and successive peripheral budding by peripatric and/or vicariant speciation. The findings suggested crucial roles of geography and ecology in Plectropomus diversification. The results also call for taxonomic revision, as monophyly was refuted in P. pessuliferus. Coral groupers, like many other reef fishes, underwent recent diversification and colonized the Indo-Pacific and Red Sea biogeographic regions rapidly.

Climatic oscillations during the mid- to late Pleistocene were significant drivers of intra-specific lineage diversification and population bottlenecks as revealed by phylogeographic analyses, suggesting that sea level reductions associated with glacial cycles were implicated. Three regional P. areolatus populations were identified: Red Sea, Maldives and Pacific + Western Australia, with limited fine-scale population structure within regions. All three P. areolatus populations expanded following the late Pleistocene glacial retreat, but their demographic histories differed somewhat, possibly due to region-specific geological features. High self-replenishment was evident in all three regional populations and minimal migration was detected among regions, but within-region gene flow was substantial. These findings suggest it is crucial to manage P. areolatus in each region as a distinct stock.

In summary, major geological events and climatic oscillations during the past ~40 Myr were important drivers of grouper diversification. The origin of groupers in mid-Eocene and the diversification of major clades were both associated with global cooling and oceanographic changes, possibly prompting episodes of adaptive radiation. While within-region origination contributed significantly to grouper diversity, in later stages of grouper evolution, the formation of the Isthmus of Panama and glacial cycles during the Pleistocene instigated allopatric speciation and/or intra-specific lineage diversification at major biogeographic barriers. My study identified geographical and ecological factors driving reef fish diversification. Contemporary grouper biodiversity hotspots in the IAA and the Caribbean are both young and have acted as biodiversity sinks throughout grouper evolutionary history. Peripheral, less coral-rich region were identified as historical cradel of grouper diversity. Together, these results provide new insights into the multifarious relationship between reef fish evolution and geological/climatic history in the tropics.

Item ID: 41011
Item Type: Thesis (PhD)
Keywords: biodiversity; biogeography; climatic factors; coral grouper; diversification; epinephelidae; epinephelus; evolution; geographical distribution; groupers; marine biodiversity; phylogeny; phylogeography; plectropomus; populations; speciation; species
Date Deposited: 29 Oct 2015 02:29
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060301 Animal Systematics and Taxonomy @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 34%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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