Biogeography and the evolution of coral reef fish species

Hodge, Jennifer Reneé (2014) Biogeography and the evolution of coral reef fish species. PhD thesis, James Cook University.

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This thesis examines the evolution of coral reef fish species, specifically the chronology and geography of extant species divergence, and the evolutionary processes that have shaped contemporary patterns of biodiversity. The evolutionary histories of species belonging to multiple genera from four common coral reef fish families: the Chaetodontidae (butterflyfishes), Labridae (wrasses), Pomacanthidae (angelfishes), and Epinephelidae (groupers) were reconstructed based on molecular data. Resultant phylogenies were temporally calibrated using palaeontological data. The reconstructed chronograms were combined with detailed distributional data to determine how closely related species are geographically distributed, and to explore the processes responsible for contemporary patterns of reef fish diversity. First, the diversification of endemic species was explored by considering a case study of the wrasse genus Anampses. A second case study assessed the evolution of sympatric species within the angelfish genus Pomacanthus. Finally, a multi-family phylogenetic hypothesis was constructed to broaden the generality of conclusions drawn from the case studies. This expanded phylogenetic hypothesis was used to critically evaluate traditional methods of phylogenetic age estimation; to compare the ages of species from different biogeographical areas; and to evaluate the role of geography in the speciation of coral reef fishes. Together, these studies have identified common evolutionary and biogeographical patterns among reef fish species, and begun to unravel potential processes involved in species divergence and maintenance.

A chronogram of the genus Anampses identified diversification of extant species from the mid-Miocene onward. Evolutionarily, this resulted in a high proportion of endemic species with varied divergence times and distributions largely restricted to the range edges of Indo-Pacific coral reefs. Evolutionary relationships within the genus, combined with limited spatial and temporal concordance among endemics, suggest that successive peripheral speciation, or peripheral budding, may have generated substantial species diversity within this genus. The findings highlight the importance of peripherally isolated locations in creating and maintaining endemic species.

Extant species in the genus Pomacanthus showed similar timing in their divergence, from the mid-Miocene onward. In contrast to Anampses, this genus consists of species that are largely sympatric, where 80% of sister-species demonstrated complete or substantial (> 85%) distributional overlap. Splits between lineages within the phylogeny corroborated key biogeographical events including the Terminal Tethyan Event and the rise of the Isthmus of Panama, suggesting that allopatric speciation impacted the early evolutionary history of the genus. Age-range correlation analyses revealed no significant relationship between the degree of distributional overlap and divergence time, demonstrating that exceptional sympatry is not restricted to evolutionarily older species. This work emphasizes the need to disentangle process from pattern by demonstrating that a number of speciation modes, including sympatry and peripatry, likely led to the divergence of species with exceptionally high distributional overlap.

Commonly, divergence time estimates from the nodes of a temporally-calibrated phylogeny are used as indicators of extant species' ages. However, this method can sometimes produce misleading age estimates, specifically in the presence of extinction and ancestral persistence. A method to minimize the impacts of extinction and ancestral persistence on divergence time estimation was established. The method focuses on recent divergences (using a sister-species approach) and involves the combination of minimum divergence time estimates (as indicators of species' ages) with the minimum geographical range area between two sister-species, for all sister-species pairs. When applied to coral reef fishes, this method revealed a general pattern of geographical range expansion with increasing evolutionary age. The differences in the trends recovered from excluding potential biases associated with ancestral persistence (i.e. maintaining a large geographic range over time) suggest that ancestral persistence may be prevalent among coral reef fishes, with successive peripheral speciation impacting age-area relationships. The described method may reveal the occurrence of successive peripheral speciation events across a broad range of taxa.

The multi-family phylogeny revealed similar temporal patterns of coral reef fish divergence among major marine realms and regions, despite differing geological histories. The evolutionary age of most coral reef fish species ranges from 1 to 5 Ma. Notable differences were recorded in the timing of divergence and spatial relationships of endemic species in the Red Sea and Hawaiian Islands. Red Sea endemics have diverged consistently throughout the past 16 Myr, whereas endemic species colonized the Hawaiian Islands in two distinct waves (0– 3 Ma and 8–12 Ma). These results suggest that markedly different processes have shaped patterns of diversification in two prominent, peripherally isolated locations.

Important areas of common overlap and vicariance were identified through the continued application of a sister-species approach using the multi-family phylogeny. Congruent vicariance was detected across six previously described biogeographical barriers: the Amazon and Orinoco barriers, Isthmus of Panama, Hawaiian Archipelago, Indo-Pacific, and a previously unnamed barrier I term the Mid-Indian Ocean Barrier (MIOB). The MIOB is hypothesized to be driven by the unusually high sediment content of the Ganges and Indus river systems and the resultant impacts on physical oceanography. A high concentration of distributional overlap was strikingly concordant with the Coral Triangle. This may suggest that the Coral Triangle harbours sufficiently complex environments to facilitate reproductive isolation through niche specialisation that permits closely related species to co-occur. However, the significantly lower than expected degree of distributional overlap among sister-species in this region indicates that it is, more frequently, an area of secondary contact between species that largely occupy adjacent ocean basins, supporting the Centre of Overlap hypothesis. This information helps to illuminate the roles various biogeographical regions and boundaries play in creating and maintaining extant species diversity. In summary, coral reef fish species have an intricate evolutionary history involving a combination of evolutionary processes that have led to the establishment of complex contemporary biogeographical patterns. Fluctuations in soft biogeographical barriers, founder events and potential divergence in sympatry appear to have driven present day biodiversity. The Coral Triangle not only harbours a unique richness of species but it also supports the coexistence of numerous sister-species. As a whole, this thesis provides a detailed description of the temporal evolution of coral reef fish species, their contemporary geographical distributions, and the evolutionary processes that have likely shaped their distinctive patterns of biodiversity.

Item ID: 42130
Item Type: Thesis (PhD)
Keywords: age estimation; age–range correlation; allopatry; biodiversity; coral reef fishes; Coral Triangle; divergence dating; endemism; evolutionary age; evolutionary history; fossil calibration; Hawaiian Islands; marine biogeography; molecular phylogeny; pan-tropical; peripatric speciation; peripheral budding; Red Sea; sister-species speciation mode; successive colonisation; successive division; sympatry
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Hodge, Jennifer R., Read, Charmaine I., Van Herwerden, Lynne, and Bellwood, David R. (2012) The role of peripheral endemism in species diversification: evidence from the coral reef fish genus Anampses (Family: Labridae). Molecular Phylogenetics and Evolution, 62 (2). pp. 653-663.

Hodge, Jennifer R., Read, Charmaine I., Bellwood, David R., and van Herwerden, Lynne (2013) Evolution of sympatric species: a case study of the coral reef fish genus Pomacanthus (Pomacanthidae). Journal of Biogeography, 40 (9). pp. 1676-1687.

Hodge, Jennifer R., Van Herwerden, Lynne , Bellwood, David R., and UNSPECIFIED (2014) Temporal evolution of coral reef fishes: global patterns and disparity in isolated locations. Journal of Biogeography, 41 (11). pp. 2115-2127.

Hodge, Jennifer, and Bellwood, David R. (2015) On the relationship between species age and geographical range in reef fishes: are widespread species older than they seem? Global Ecology and Biogeography , 24 (4). pp. 495-505.

Date Deposited: 23 Dec 2015 05:28
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060311 Speciation and Extinction @ 34%
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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