Dating the evolutionary origins of coral reef fishes

Cowman, Peter Francis (2011) Dating the evolutionary origins of coral reef fishes. PhD thesis, James Cook University.

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This thesis examines the origins and maintenance of the high diversity of coral reef fishes in the Indo-Australian Archipelago (IAA), the largest marine biodiversity hotspot. Bayesian age estimation techniques, combining molecular and palaeontological data, were used to reconstruct an evolutionary timeline for four conspicuous coral reef fish families: the Labridae (wrasses), Chaetodontidae (butterflyfishes), Pomacentridae (damselfishes) and Apogonidae (cardinalfishes). First, the evolutionary origins of trophic novelty and habitat preference were explored in the Labridae and Chaetodontidae. Then, to assess congruence in patterns of cladogenesis, rates of diversification and lineage accumulation were compared for the four families. Finally, to gain a biogeographic perspective, ancestral range reconstruction was used to compare global patterns of origination and dispersal. Specifically, the origins and progression of biodiversity in the IAA was compared to other marine provinces. Combined, these data provided an insight into the evolution of this complex association between fishes and coral reefs.

A chronogram of the Labridae identified molecular origins in the late Cretaceous, with both major lineages (hypsigenyine and julidine) present shortly after the K/T boundary (~63 MY). All major lineages were in place by the beginning of the Miocene (23 MY) with most diversification in extant lineages occurring within the Miocene. Multiple origins of novel feeding modes were revealed with two distinct pulses. The Palaeocene/Eocene saw the origins of feeding modes that are well represented in other families: gastropod feeders, piscivores and browsing herbivores. A second wave of innovation in the Oligocene/Miocene resulted in more specialised feeding modes: coral feeding, foraminifera feeding and fish cleaning.

There is little evidence of a general relationship between trophic specialisation and species diversity. All major feeding modes on present day reefs were probably already in place 7.5 million years ago.

The Chaetodontidae stem lineage has origins in the Eocene and by the early Oligocene the two major lineages have diverged: bannerfishes and butterflyfishes. Optimisation of recent ecological data reveal that corallivory has arisen at least five times over a period of 12 MY, from 15.7 to 3 MY. Significantly higher diversity was recorded in lineages of the genus Chaetodon, in which the greatest number of corallivores are found. However, it was the move onto coral reefs in the Miocene, not corallivory that foreshadowed rapid cladogenesis within Chaetodon. This coincides with a global reorganisation of coral reefs and the expansion of fast-growing corals. This historical association underpins the sensitivity of specific butterflyfish clades to global coral decline.

Previous chronologies of the Labridae and Chaetodontidae were reassessed with increased taxon sampling, and added fossil data. For the first time, the timing of diversification within the Pomacentridae and Apogonidae were estimated using Bayesian inference. Lineage through time plots for these four families revealed a possible late Eocene/early Oligocene cryptic extinction event coinciding with the collapse of the ancestral Tethyan/Arabian hotspot. Rates of diversification analysis revealed elevated cladogenesis in all four families in the Oligocene/Miocene. In this rebound, lineages with a high percentage of coral reef associated taxa display significantly higher diversities and higher net diversification rates than expected, throughout the Miocene epoch. Similar patterns were found in other reef associated fish and gastropod groups. The development of a complex mosaic of reef habitats in the IAA during the Oligocene/Miocene period appears to have been a significant driver of cladogenesis at this time. Patterns of diversification among taxa suggest that coral reefs also acted as a refuge from high extinction, as reef taxa are able to sustain significant diversity at higher extinction rates than their non-reef counterparts. As such, the IAA appears to support both cladogenesis and survival in associated lineages, laying the foundation for the Recent IAA marine biodiversity hotspot.

Ancestral range reconstruction of the Chaetodontidae, Pomacentridae and Labridae revealed temporal patterns of origination and dispersal between the East Pacific, Atlantic, Indian Ocean, IAA and Central Pacific. The IAA acts as both a centre of origination and as a source of diversity to the Indian Ocean and Central Pacific, for all three families. The Atlantic and East Pacific both show high relative rates of origination, however, on a global scale these regions support significantly lower origination than the IAA. Inferred palaeodiversity of ancestral lineages is masked by the extinction of lineages following the closure of the Tethys seaway and decline of ancestral biodiversity hotspots. Lineages of Eocene and Oligocene origin that appear restricted to the IAA would have been peripheral at the time to the Tethyan hotspot. However, it was the proliferation and expansion of these restricted lineages throughout the Miocene that underpins the diversity in the IAA hotspot and across the entire Indo-Pacific. The distribution of vicariance events across known historical barriers highlights the lack of temporal congruence among taxa in the Isthmus of Panama, the East Pacific Barrier and the Terminal Tethyan Event, but much greater congruence between the IAA, Indian and Pacific Oceans.

In summary, for three of the four families, initial divergences following the K/T boundary represent the origins of generalised feeding strategies. During this time there was the potential for panmixia between all ocean regions. The apparent slowdown in net speciation rate throughout the Eocene may reflect a late Eocene/Oligocene cryptic extinction event. The survival and subsequent proliferation of Eocene lineages restricted to the IAA during the Miocene underpins much of the current biodiversity on coral reefs and laid the foundation for a wave of trophic innovation in the Labridae and Chaetodontidae. In all four families, Recent patterns are a result of evolutionary, geological and ecological factors spanning over 40 to 60 MY. Today's hotspot is the product of long history of division, decline and diversification.

Item ID: 23789
Item Type: Thesis (PhD)
Keywords: coral reef fishes, age estimation, lineage diversification, trophic novelty, ancestral biogeography, molecular phylogenetics, Indo-Australian Archipelago (IAA), refuges, centre of survival, cladogenesis, evolutionary origins
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Cowman, Peter F., Bellwood, David R., and van Herwerden, Lynne (2009) Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs. Molecular Phylogenetics and Evolution, 52 (3). pp. 621-631.

Chapter 3: Bellwood, D.R., Klanten, S., Cowman, P.F., Pratchett, M.S., Konow, N., and Van Herwerden, L. (2010) Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. Journal of Evolutionary Biology, 23 (2). pp. 335-349.

Chapter 4: Cowman, P.F., and Bellwood, D.R. (2011) Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. Journal of Evolutionary Biology, 24 (12). pp. 2543-2562.

Date Deposited: 31 Oct 2012 01:18
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060311 Speciation and Extinction @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 34%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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