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"Combosch, David"
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Population Genetics of an Ecosystem-Defining Reef Coral Pocillopora damicornis in the Tropical Eastern Pacific
2011
Coral reefs in the Tropical Eastern Pacific (TEP) are amongst the most peripheral and geographically isolated in the world. This isolation has shaped the biology of TEP organisms and lead to the formation of numerous endemic species. For example, the coral Pocillopora damicornis is a minor reef-builder elsewhere in the Indo-West Pacific, but is the dominant reef-building coral in the TEP, where it forms large, mono-specific stands, covering many hectares of reef. Moreover, TEP P. damicornis reproduces by broadcast spawning, while it broods mostly parthenogenetic larvae throughout the rest of the Indo-West Pacific. Population genetic surveys for P. damicornis from across its Indo-Pacific range indicate that gene flow (i.e. larval dispersal) is generally limited over hundreds of kilometers or less. Little is known about the population genetic structure and the dispersal potential of P. damicornis in the TEP.
Using multilocus microsatellite data, we analyzed the population structure of TEP P. damicornis among and within nine reefs and test for significant genetic structure across three geographically and ecologically distinct regions in Panama.
We detected significant levels of population genetic structure (global R(ST) = 0.162), indicating restricted gene flow (i.e. larvae dispersal), both among the three regions (R(RT) = 0.081) as well as within regions (R(SR) = 0.089). Limited gene flow across a distinct environmental cline, like the regional upwelling gradient in Panama, indicates a significant potential for differential adaptation and population differentiation. Individual reefs were characterized by unexpectedly high genet diversity (avg. 94%), relatively high inbreeding coefficients (global F(IS) = 0.183), and localized spatial genetic structure among individuals (i.e. unique genets) over 10 m intervals. These findings suggest that gene flow is limited in TEP P. damicornis populations, particularly among regions, but even over meter scales within populations.
Journal Article
Barcoding and mitochondrial phylogenetics of Porites corals
2024
Coral reefs are the most diverse ecosystem on the planet based on the abundance and diversity of phyla and higher taxa. However, it is still difficult to assess the diversity of lower taxa, especially at the species level. One tool for improving the identification of lower taxa are genetic markers that can distinguish cryptic species and assess species boundaries. Here, we present one such approach for an important and challenging group of reef-building corals. Porites corals are the main reef-builders of many coral reefs in the Indo-Pacific, owing to the massive growth forms of some species. The current number of valid Porites species is controversial, inflated with many synonymies, and often based on gross colony morphology although several morphospecies believed to be widespread and common can only be distinguished based on detailed microstructure analyses by taxonomic experts. Here, we test the suitability of multiple regions of mtDNA as genetic barcodes to identify suitable markers for species differentiation and unambiguous identification. Resulting sequencing data was further used for the first phylogenetic analysis of Guam’s Porites species. We tested eight different mitochondrial markers and analyzed four in detail for 135 Porites specimens: mtDNA markers were amplified for 67 Porites specimens from Guam, representing 12 nominal Porites species, and combined with 69 mitochondrial genomes, mostly from Hawaii. The combination of all 4 markers distinguished 10 common and 7 uncommon Central-West Pacific Porites species. Most clades separate species along taxonomic boundaries, which is uncommon for Porites corals and testifies to the suitability of our multi-marker approach, and a combination of the two most promising barcodes distinguished 8/10 common species. These barcodes are thus suitable to distinguish virtually cryptic species in one of the most important and challenging coral genera. They offer a cheap, fast and reliable way to identify Porites species for species-level research, monitoring and conservation.
Journal Article
Genomic data reveals habitat partitioning in massive Porites on Guam, Micronesia
2024
Corals in marginal reef habitats generally exhibit less bleaching and associated mortality compared to nearby corals in more pristine reef environments. It is unclear, however, if these differences are due to environmental differences, including turbidity, or genomic differences between the coral hosts in these different environments. One particularly interesting case is in the coral genus
Porites
, which contains numerous morphologically similar massive
Porites
species inhabiting a wide range of reef habitats, from turbid river deltas and stagnant back reefs to high-energy fore reefs. Here, we generate ddRAD data for 172
Porites
corals from river delta and adjacent (<0.5 km) fore reef populations on Guam to assess the extent of genetic differentiation among massive
Porites
corals in these two contrasting environments and throughout the island. Phylogenetic and population genomic analyses consistently identify seven different clades of massive
Porites
, with the two largest clades predominantly inhabiting either river deltas or fore reefs, respectively. No population structure was detected in the two largest clades, and
Cladocopium
was the dominant symbiont genus in all clades and environments. The perceived bleaching resilience of corals in marginal reefs may therefore be attributed to interspecific differences between morphologically similar species, in addition to potentially mediating environmental differences. Marginal reef environments may therefore not provide a suitable refuge for many reef corals in a heating world, but instead host additional cryptic coral diversity.
Journal Article
Population Genomics for Coral Reef Restoration—A Case Study of Staghorn Corals in Micronesia
2025
Staghorn Acropora corals are ecological keystone species in shallow lagoons and back reef habitats throughout the tropics. Their widespread decline coupled with their amenability for asexual propagation propelled them to the forefront of global coral restoration efforts—albeit frequently without much scientific input. To guide these efforts and as a blueprint for similar projects, we conducted a comprehensive population genomic study of Acropora cf. pulchra, a major restoration target species in the Indo‐West Pacific. Our results revealed that A. cf. pulchra populations in the Mariana Islands are characterized by large clonal clusters and extremely low levels of genetic diversity. Differentiation among populations followed a significant isolation‐by‐distance pattern and delineated two distinct metapopulations on Guam. Our investigation identified critical population genetic parameters, necessitating targeted management strategies, and provides actionable guidelines for effective conservation efforts. For management and conservation, two populations emerged as pivotal connectivity hubs with elevated genetic diversity. For restoration, we show that A. cf. pulchra populations demonstrated a suitability for extensive asexual propagation and provide guidelines on how to best apply that. To preserve and augment genetic diversity, strategies to mitigate inbreeding are crucial until sexual reproduction can be fully integrated into restoration protocols. Critical sites for restoration include local connectivity hubs, fringing lagoons that connect metapopulations, and back reefs around a particularly isolated population. These findings offer crucial insights into the genetic landscape of a keystone coral species and provide actionable recommendations for coral conservation and restoration. By advocating for the preservation of population connectivity and the promotion of genotypic, genetic, and symbiont diversity in coral restoration, our study serves as a blueprint for leveraging population genomic studies to enhance the efficacy and resilience of restoration projects on remote islands.
Journal Article
ENSO Drove 2500-Year Collapse of Eastern Pacific Coral Reefs
by
Urrego, Dunia H.
,
Combosch, David J.
,
Enochs, Ian C.
in
Acidification
,
Animal, plant and microbial ecology
,
Animals
2012
Cores of coral reef frameworks along an upwelling gradient in Panamá show that reef ecosystems in the tropical eastern Pacific collapsed for 2500 years, representing as much as 40% of their history, beginning about 4000 years ago. The principal cause of this millennial-scale hiatus in reef growth was increased variability of the El Niño-Southern Oscillation (ENSO) and its coupling with the Intertropical Convergence Zone. The hiatus was a Pacific-wide phenomenon with an underlying climatology similar to probable scenarios for the next century. Global climate change is probably driving eastern Pacific reefs toward another regional collapse.
Journal Article
Mixed asexual and sexual reproduction in the Indo‐Pacific reef coral Pocillopora damicornis
2013
Pocillopora damicornis is one of the best studied reef‐building corals, yet it's somewhat unique reproductive strategy remains poorly understood. Genetic studies indicate that P. damicornis larvae are produced almost exclusively parthenogenetically, and yet population genetic surveys suggest frequent sexual reproduction. Using microsatellite data from over 580 larvae from 13 colonies, we demonstrate that P. damicornis displays a mixed reproductive strategy where sexual and asexual larvae are produced simultaneously within the same colony. The majority of larvae were parthenogenetic (94%), but most colonies (10 of the 13) produced a subset of their larvae sexually. Logistic regression indicates that the proportion of sexual larvae varied significantly with colony size, cycle day, and calendar day. In particular, the decrease in sexual larvae with colony size suggests that the mixed reproductive strategy changes across the life of the coral. This unique shift in reproductive strategy leads to increasingly asexual replications of successful genotypes, which (in contrast to exclusive parthenogens) have already contributed to the recombinant gene pool. This study provides the first detailed genetic analyses of the unusual, simultaneously mixed reproductive strategy in the important reef‐building coral Pocillopora damicornis. The proportion of sexual larvae varied with colony size, reproductive cycle day and general calendar day. In particular, the decrease in the production of sexually produced larvae with increasing colony size, suggests that the mixed reproductive strategy changes across the life of the coral, which has important ecological and evolutionary consequences.
Journal Article
Three new species of Nautilus Linnaeus, 1758 (Mollusca, Cephalopoda) from the Coral Sea and South Pacific
2023
Nautiloids are a charismatic group of marine molluscs best known for their rich fossil record, but today they are restricted to a handful of species in the family Nautilidae from around the Coral Triangle. Recent genetic work has shown a disconnect between traditional species, originally defined on shell characters, but now with new findings from genetic structure of various Nautilus populations. Here, three new species of Nautilus from the Coral Sea and South Pacific region are formally named using observations of shell and soft anatomical data augmented by genetic information: N. samoaensis sp. nov. (from American Samoa), N. vitiensis sp. nov. (from Fiji), and N. vanuatuensis sp. nov. (from Vanuatu). The formal naming of these three species is timely considering the new and recently published information on genetic structure, geographic occurrence, and new morphological characters, including color patterns of shell and soft part morphology of hood, and will aid in managing these possibly endangered animals. As recently proposed from genetic analyses, there is a strong geographic component affecting taxonomy, with the new species coming from larger island groups that are separated by at least 200 km of deep water (greater than 800 m) from other Nautilus populations and potential habitats. Nautilid shells implode at depths greater than 800 m and depth therefore acts as a biogeographical barrier separating these species. This isolation, coupled with the unique, endemic species in each locale, are important considerations for the conservation management of the extant Nautilus species and populations.
Journal Article
Unified methods in collecting, preserving, and archiving coral bleaching and restoration specimens to increase sample utility and interdisciplinary collaboration
by
Kuffner, Ilsa B.
,
Barshis, Daniel J.
,
Barott, Katie
in
Aldehydes
,
Animals
,
Anthozoa - microbiology
2022
Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at −80 °C to −20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses.
Journal Article
Consensus Guidelines for Advancing Coral Holobiont Genome and Specimen Voucher Deposition
by
Villela, Helena
,
Ziegler, Maren
,
Parkinson, John Everett
in
coral holobiont
,
coral reef
,
genome sequencing
2021
Coral research is being ushered into the genomic era. To fully capitalize on the potential discoveries from this genomic revolution, the rapidly increasing number of high-quality genomes requires effective pairing with rigorous taxonomic characterizations of specimens and the contextualization of their ecological relevance. However, to date there is no formal framework that genomicists, taxonomists, and coral scientists can collectively use to systematically acquire and link these data. Spurred by the recently announced “Coral symbiosis sensitivity to environmental change hub” under the “Aquatic Symbiosis Genomics Project” - a collaboration between the Wellcome Sanger Institute and the Gordon and Betty Moore Foundation to generate gold-standard genome sequences for coral animal hosts and their associated Symbiodiniaceae microalgae (among the sequencing of many other symbiotic aquatic species) - we outline consensus guidelines to reconcile different types of data. The metaorganism nature of the coral holobiont provides a particular challenge in this context and is a key factor to consider for developing a framework to consolidate genomic, taxonomic, and ecological (meta)data. Ideally, genomic data should be accompanied by taxonomic references, i.e., skeletal vouchers as formal morphological references for corals and strain specimens in the case of microalgal and bacterial symbionts (cultured isolates). However, exhaustive taxonomic characterization of all coral holobiont member species is currently not feasible simply because we do not have a comprehensive understanding of all the organisms that constitute the coral holobiont. Nevertheless, guidelines on minimal, recommended, and ideal-case descriptions for the major coral holobiont constituents (coral animal, Symbiodiniaceae microalgae, and prokaryotes) will undoubtedly help in future referencing and will facilitate comparative studies. We hope that the guidelines outlined here, which we will adhere to as part of the Aquatic Symbiosis Genomics Project sub-hub focused on coral symbioses, will be useful to a broader community and their implementation will facilitate cross- and meta-data comparisons and analyses.
Journal Article
Revisiting metazoan phylogeny with genomic sampling of all phyla
by
Combosch, David
,
Laumer, Christopher E.
,
Fernández, Rosa
in
Animals
,
Classification
,
Evolution
2019
Proper biological interpretation of a phylogeny can sometimes hinge on the placement of key taxa—or fail when such key taxa are not sampled. In this light, we here present the first attempt to investigate (though not conclusively resolve) animal relationships using genome-scale data from all phyla. Results from the site-heterogeneous CAT + GTR model recapitulate many established major clades, and strongly confirm some recent discoveries, such as a monophyletic Lophophorata, and a sister group relationship between Gnathifera and Chaetognatha, raising continued questions on the nature of the spiralian ancestor. We also explore matrix construction with an eye towards testing specific relationships; this approach uniquely recovers support for Panarthropoda, and shows that Lophotrochozoa (a subclade of Spiralia) can be constructed in strongly conflicting ways using different taxon- and/or orthologue sets. Dayhoff-6 recoding sacrifices information, but can also reveal surprising outcomes, e.g. full support for a clade of Lophophorata and Entoprocta + Cycliophora, a clade of Placozoa + Cnidaria, and raising support for Ctenophora as sister group to the remaining Metazoa, in a manner dependent on the gene and/or taxon sampling of the matrix in question. Future work should test the hypothesis that the few remaining uncertainties in animal phylogeny might reflect violations of the various stationarity assumptions used in contemporary inference methods.
Journal Article