Are coral reefs victims of their own past success?

Renema, Willem; Pandolfi, John M.; Kiessling, Wolfgang; Bosellini, Francesca; Klaus, James S.; Korpanty, Chelsea; Rosen, Brian; Santodomingo, Nadiezhda; Wallace, Carden C.; Webster, Jody M.; Johnson, Kenneth G.

doi:10.1126/sciadv.1500850

Cited by 52 publications

(49 citation statements)

References 61 publications

(84 reference statements)

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“…The diversification of these butterflyfishes occurred at a time when the coral assemblages of the world's reefs underwent a major change in coral composition and growth forms. The global proportion of staghorn coral occurrences in coral assemblages persisted throughout most of the Cenozoic but increased substantially during the Pliocene and especially the Quaternary (Renema et al ). Indeed, the rapidly growing branching acroporid corals offered different structural components in terms of shelter and feeding/foraging modes when compared to massive corals such as poritids that dominated Miocene reefs more than 5 Ma.…”

Section: Discussionmentioning

confidence: 99%

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot

DiBattista

Alfaro

Sorenson

et al. 2018

Ecology and Evolution

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For tropical marine species, hotspots of endemism occur in peripheral areas furthest from the center of diversity, but the evolutionary processes that lead to their origin remain elusive. We test several hypotheses related to the evolution of peripheral endemics by sequencing ultraconserved element (UCE) loci to produce a genome‐scale phylogeny of 47 butterflyfish species (family Chaetodontidae) that includes all shallow water butterflyfish from the coastal waters of the Arabian Peninsula (i.e., Red Sea to Arabian Gulf) and their close relatives. Bayesian tree building methods produced a well‐resolved phylogeny that elucidated the origins of butterflyfishes in this hotspots of endemism. We show that UCEs, often used to resolve deep evolutionary relationships, represent an important tool to assess the mechanisms underlying recently diverged taxa. Our analyses indicate that unique environmental conditions in the coastal waters of the Arabian Peninsula probably contributed to the formation of endemic butterflyfishes. Older endemic species are also associated with narrow versus broad depth ranges, suggesting that adaptation to deeper coral reefs in this region occurred only recently (<1.75 Ma). Even though deep reef environments were drastically reduced during the extreme low sea level stands of glacial ages, shallow reefs persisted, and as such there was no evidence supporting mass extirpation of fauna in this region.

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Section: Discussionmentioning

confidence: 99%

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot

DiBattista

Alfaro

Sorenson

et al. 2018

Ecology and Evolution

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“…Ancient WGD is considered as a significant evolutionary factor in the origin and diversification of evolutionary lineages [17,18,28,54], but much work remains to definitively identify WGD and to understand its consequences in different evolutionary lineages. Staghorn corals of the genus Acropora , which constitute the foundation of modern coral reef ecosystems, are hypothesized to have originated through polyploidization [2,11,15]. However, there is no genetic evidence to support this assertion.…”

Section: Discussionmentioning

confidence: 99%

“…Reef-building corals contribute to tropical marine ecosystems that support innumerable marine organisms, but reefs are increasingly threatened due to recent increases in seawater temperatures, pollution, and other stressors [1,2]. The Acroporidae is a family of reef-building corals in the phylum Cnidaria, one of the basal phyla of the animal clade [3-5].…”

Section: Introductionmentioning

confidence: 99%

An ancient genome duplication in the speciose reef-building coral genus, Acropora

Mao

Shinzato

Satoh

2018

Preprint

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16Whole-genome duplication (WGD) has been recognized as a significant evolutionary 17 force in the origin and diversification of vertebrates, plants, and other organisms. 18Acropora, one of the most speciose reef-building coral genera, responsible for 19 creating spectacular but increasingly threatened marine ecosystems, is suspected to 20 have originated by polyploidy, yet there is no genetic evidence to support this 21 hypothesis. Using comprehensive phylogenomic and comparative genomic 22 approaches, we analyzed five Acropora genomes and an Astreopora genome 23 (Scleractinia: Acroporidae) to show that a WGD event likely occurred between 27.9 24 and 35.7 Million years ago (Mya) in the most recent common ancestor of Acropora, 25 concurrent with a massive worldwide coral extinction. We found that duplicated 26 genes became highly enriched in gene regulation functions, some of which are 27 involved in stress responses. The different functional clusters of duplicated genes are 28 related to the divergence of gene expression patterns during development. Some gene 29 duplications of proteinaceous toxins were generated by WGD in Acropora compared 30 with other Cnidarian species. Collectively, this study provides evidence for an ancient 31 WGD event in corals and it helps to explain the origin and diversification of Acropora. 32 gene families [12,13]. Thus, based on their unique lifestyle, variable chromosome 48 numbers, and complicated reticular evolutionary history, Indo-Pacific Acropora likely 49 originated via polyploidy [10][11][12][13][14][15][16]. However, there is no direct molecular and genetic 50 evidence to support this hypothesis. 51 52Ancient whole (large-scale)-genome duplication (WGD), or paleopolyploidy, has 53 shaped in the genomes of vertebrates, green plants, and other organisms, and is 54 usually regarded as an evolutionary landmark in the origins and diversification of 55 organisms [17][18][19] (Supplementary Fig. 1). Two separate WGD events have been 56 documented in the common ancestors of vertebrates (two-rounds of WGD) [20] and 57 4 another major WGD has been reported in the last common ancestor of teleost fish 58 [21,22]. Meanwhile, living angiosperms share an ancient WGD event [23,24], and 59 many other WGD events have been reported in major clades of angiosperms [25,26]. 60In addition, two-rounds of WGDs in the vertebrates are suggested to have occurred 61 during the Cambrian Period, and some WGDs in plants are believed to have occurred 62during Cretaceous-Tertiary [17,25,27]. Thus, WGD is regarded as an important 63 evolutionary way to reduce the risk of extinction [17,18,25]. However, the study of 64 WGD in Cnidaria has received less attention [17,18,[28][29][30]. 65 66 Duplicated genes created by WGD have complex fates following the time of 67 diploidization [18,31]. Usually, one of the duplicated genes is silenced or lost due to 68 redundancy of gene functions, termed "nonfunctionalization". However, retained 69 duplicated genes provide important sources of biological complexity and ev...

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“…We used small colonies of Acropora muricata (Linné, 1758) as an experimental model for coral development and behaviour. Corals of the genus Acropora are fast-growing, ecologically crucial key architects of coral reef ecosystems, greatly contributing to their complex three-dimensional structure (Renema et al, 2016). They can also recover rapidly from environmental disturbances, making them important re-colonisers (Sweatman et al, 2011).…”

Section: Fig 1 A) Size Of Commonly Used Samples and Of A Small Colonmentioning

confidence: 99%

Light-induced polyp retraction and tissue rupture in the photosensitive, reef-building coral Acropora muricata

Laissue

Qian

et al. 2019

Preprint

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Coral reefs are in alarming decline due to climate emergency, pollution and other man-made disturbances. The numerous ecosystem services derived from coral reefs are underpinned by the growth and physical complexity of reef-forming corals. Our knowledge of their fundamental biology is limited by available technology. We need a better understanding of larval settlement and development, skeletogenesis, interactions with pathogens and symbionts, and how this biology interacts with environmental factors such as light exposure, temperature, and ocean acidification. We here focus on a fast-growing key coloniser, Acropora muricata. To enable dynamic imaging of the photosensitive organism at different scales, we developed light-sheet illumination for fluorescence microscopy of small coral colonies. Our approach reveals live polyps in previously unseen detail. An imaging range for Acropora muricata with no measurable photodamage is defined based upon polyp expansion, coral tissue reaction, and photobleaching. We quantify polyp retraction as a photosensitive behavioural response and show sparse zooxanthellar expulsion and coral tissue rupture at higher intensities of blue light. The simple and flexible technique enables non-invasive continuous dynamic imaging of highly photosensitive organisms with sizes between 1 mm 3 and 5 cm 3 , for eight hours, at high temporal resolution, on a scale from multiple polyps down to cellular resolution. This live imaging tool opens a new window into the dynamics of reef-building corals. KEYWORDSLive imaging; coral development; phototoxicity; widefield fluorescence microscopy; confocal laser scanning microscopy; selective plane illumination microscopy; large selective plane illuminator.

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Are coral reefs victims of their own past success?

Abstract: Pleistocene sea-level change transformed staghorn corals into prolific reef builders that are sensitive to anthropogenic stressors.

Cited by 52 publications

References 61 publications

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot

An ancient genome duplication in the speciose reef-building coral genus, Acropora

Light-induced polyp retraction and tissue rupture in the photosensitive, reef-building coral Acropora muricata

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