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Journal Articles - UP - MSI

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  • Transcriptome analysis of growth variation in early juvenile stage sandfish Holothuria scabra
    Ordoñez, June Feliciano F.; Galindez, Gihanna Gaye S.T.; Gulay, Karina Therese; Ravago-Gotanco, Rachel (Elsevier, 2021-12)
    The sandfish Holothuria scabra is a high-value tropical sea cucumber species representing a major mariculture prospect across the Indo-Pacific. Advancements in culture technology, rearing, and processing present options for augmenting capture production, stock restoration, and sustainable livelihood activities from hatchery-produced sandfish. Further improvements in mariculture production may be gained from the application of genomic technologies to improve performance traits such as growth. In this study, we performed de novo transcriptome assembly and characterization of fast- and slow-growing juvenile H. scabra from three Philippine populations. Analyses revealed 66 unigenes that were consistently differentially regulated in fast-growing sandfish and found to be associated with immune response and metabolism. Further, we identified microsatellite and single nucleotide polymorphism markers potentially associated with fast growth. These findings provide insight on potential genomic determinants underlying growth regulation in early juvenile sandfish which will be useful for further functional studies.
    The authors are grateful to the following individuals and institutions for providing samples and facilitating their collection: D. Ticao of (Finfish Hatcheries, Inc.); Dr. M.A. Juinio-Menez, ˜ J.R. Gorospe, C. Edullantes, B. Rodriguez, A. Rioja, T. Catbagan, and G. Peralta of Bolinao Marine Laboratory, University of the Philippines Marine Science Institute; and E. Tech (Palawan Aquaculture Corp.).
  • Zooxanthellae diversity and coral-symbiont associations in the Philippine archipelago: specificity and adaptability across thermal gradients
    Torres, Andrew F.; Valino, Darryl Anthony M.; Ravago-Gotanco, Rachel (Frontiers Media SA, 2021-10-20)
    Prolonged thermal stress and high levels of solar irradiance can disrupt the coral-algal symbiosis and cause bleaching and lowered overall fitness that lead to the likely death of the cnidarian host. Adaptive bleaching and acclimatization of corals, which posits bleaching as an opportunity for the coral host to switch its currently susceptible endosymbionts to more stress-tolerant taxa, offers hope for survival of reefs amid rapidly warming oceans. In this study, we explored the diversity and distribution of coral-zooxanthellae associations in the context of geospatial patterns of sea surface temperature (SST) and thermal anomalies across the Philippine archipelago. Thermal clusters based on annual sea surface temperature means and each site’s frequency of exposure to heat stress were described using three-decade (1985–2018) remotely sensed data. Haphazard sampling of 628 coral fragments was conducted in 14 reef sites over 3 years (2015–2018). Using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) fingerprinting and sequencing of the zooxanthellae ITS2 region, we characterized endosymbiont diversity within four reef-building coral families across archipelagic thermal regimes. Consistency in dominant Symbiodiniaceae taxon was observed in Acropora spp., Porites spp., and Heliopora coerulea. In contrast, the family Pocilloporidae (Pocillopora spp., Seriatopora spp., and Stylophora pistillata) exhibited biogeographic variability in zooxanthellae composition, concordant with inferred occurrences of sustained thermal stress. Multivariate analyses identify two broad Pocilloporidae clusters that correspond with mean SST ranges and frequency of exposure to bleaching-level thermal stress which are largely supported by ANOSIM. Differences in zooxanthellae assemblages may reflect host-specific responses to ecological or environmental gradients across biogeographic regions. Such patterns of variability provide insight and support for the adaptability and potential resilience of coral communities in geographically and oceanographically complex regions, especially amidst the increasing severity of global and local-scale stressors.
    This paper is dedicated to the late Ronald D. Villanueva whose contribution to the project during its inception has been invaluable. The authors thank Patrick R. Pata and the reviewers LE and RC-T for their helpful comments and suggestions, and acknowledge Hazel O. Arceo, Cesar L. Villanoy, and Maria Lourdes San Diego-McGlone for their support of this study. Eileen Peñaflor and Mariana Soppa shared key knowledge in processing satellite products. Mikhael Tañedo, Romer Albino, Emmeline Jamodiong, David Siquioco, Lovely Heyres, Rhea Luciano, Joey Cabasan, Frederico Sabban, Geminne Manzano, Clairecynth Yu, Joyce Velos, Joseph Garcia, Robert Casauay, Maryjune Cabiguin, Macy A onuevo-Arcega, Ariel Loja, Jerome Genilan, Amabelle Go, Jamie Dichaves, Elaine Saniel, and Miledel Quibilan assisted with field collections. Supporting hard coral data were provided by the DOST-PCAARRD NACRE Program and the DENR-BMB WPS and SECURE Philippine Rise Projects. This is MSI contribution number 486.
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    Restriction site-associated DNA sequencing reveals local adaptation despite high levels of gene flow in Sardinella lemuru (Bleeker, 1853) along the northern coast of Mindanao, Philippines
    Labrador, Kevin; Palermo, Joseph Dominic; Agmata, Altair; Ravago-Gotanco, Rachel; Pante, Ma. Josefa (Frontiers Media SA, 2022-02-24)
    Stock identification and delineation are important in the management and conservation of marine resources. These were highlighted as priority research areas for Bali sardinella (Sardinella lemuru) which is among the most commercially important fishery resources in the Philippines. Previous studies have already assessed the stocks of S. lemuru between Northern Mindanao Region (NMR) and Northern Zamboanga Peninsula (NZP), yielding conflicting results. Phenotypic variation suggests distinct stocks between the two regions, while mitochondrial DNA did not detect evidence of genetic differentiation for this high gene flow species. This paper tested the hypothesis of regional structuring using genome-wide single nucleotide polymorphisms (SNPs) acquired through restriction site-associated DNA sequencing (RADseq). We examined patterns of population genomic structure using a full panel of 3,573 loci, which was then partitioned into a neutral panel of 3,348 loci and an outlier panel of 31 loci. Similar inferences were obtained from the full and neutral panels, which were contrary to the inferences from the outlier panel. While the full and neutral panels suggested a panmictic population (global FST ∼ 0, p > 0.05), the outlier panel revealed genetic differentiation between the two regions (global FST = 0.161, p = 0.001; FCT = 0.263, p < 0.05). This indicated that while gene flow is apparent, selective forces due to environmental heterogeneity between the two regions play a role in maintaining adaptive variation. Annotation of the outlier loci returned five genes that were mostly involved in organismal development. Meanwhile, three unannotated loci had allele frequencies that correlated with sea surface temperature. Overall, our results provided support for local adaptation despite high levels of gene flow in S. lemuru. Management therefore should not only focus on demographic parameters (e.g., stock size and catch volume), but also consider the preservation of adaptive variation.
    We would like to acknowledge the assistance provided by Ma. Rio Naguit, Asuncion De Guzman, Jerry Garcia, Jhunrey Follante, Joshep Mercene, and John Christopher Azcarraga in sample collection and initial processing. We also acknowledge the research staff of the Marine Molecular Ecology and Evolution Laboratory (MMEEL), as well as the Marine Genomics and Molecular Genetics Laboratory (MGMGL) and its head, Arturo Lluisma, for providing valuable input in the conduct of the experiment and analysis of the data. Finally, we extend our gratitude to Demian Willette, Laura David, and Jonas Quilang for their valuable feedback on the manuscript.
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    Individual and interactive effects of ocean warming and acidification on adult Favites colemani
    Tañedo, Mikhael Clotilde S.; Villanueva, Ronald D.; Torres, Andrew F.; Ravago-Gotanco, Rachel; San Diego-McGlone, Maria Lourdes (Frontiers Media SA, 2021-09-09)
    Tropical coral reefs are threatened by local-scale stressors that are exacerbated by global ocean warming and acidification from the post-industrial increase of atmospheric CO2 levels. Despite their observed decline in the past four decades, little is known on how Philippine coral reefs will respond to ocean warming and acidification. This study explored individual and synergistic effects of present-day (pH 8.0, 28°C) and near-future (pH 7.7, 32°C) scenarios of ocean temperature and pH on the adult Favites colemani, a common massive reef-building coral in Bolinao-Anda, Philippines. Changes in seawater temperature drive the physiological responses of F. colemani, whereas changes in pH create an additive effect on survival, growth, and photosynthetic efficiency. Under near-future scenarios, F. colemani showed sustained photosynthetic competency despite the decline in growth rate and zooxanthellae density. F. colemani exhibited specificity with the Cladocopium clade C3u. This coral experienced lower growth rates but survived projected near-future ocean warming and acidification scenarios. Its pH-thermal stress threshold is possibly a consequence of acclimation and adaptation to local environmental conditions and past bleaching events. This research highlights the importance of examining the susceptibility and resilience of Philippine corals to climate-driven stressors for future conservation and restoration efforts in the changing ocean.
    We are grateful to the Marine Biogeochemistry Laboratory and Bolinao Marine Laboratory of the Marine Science Institute, University of the Philippines for the valuable logistical and laboratory support provided. We would also like to thank Drs. Haruko Kurihara, Atsushi Watanabe, and Toshihiro Miyajima for the design of the mass flow controller used in the experiments. This is UP-MSI contribution number 484.
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    Two hidden mtDNA-clades of crown-of-thorns starfish in the Pacific Ocean
    Yasuda, Nina; Inoue, Jun; Hall, Michael R.; Nair, Manoj R.; Adjeroud, Mehdi; Fortes, Miguel D.; Nishida, Mutsumi; Tuivavalagi, Nat; Ravago-Gotanco, Rachel; Forsman, Zac H.; Soliman, Taha; Koyanagi, Ryo; Hisata, Kanako; Motti, Cherie A.; Satoh, Noriyuki (Frontiers Media SA, 2022-04-27)
    Recurring outbreaks of crown-of-thorns starfish (COTS) severely damage healthy corals, especially in the Western Pacific Ocean. To obtain a better understanding of population genetics of COTS and historical colonization across the Pacific Ocean, complete mitochondrial genomes were sequenced from 243 individuals collected in 11 reef regions. Our results indicate that Pacific COTS (Acanthaster cf. solaris) comprise two major clades, an East-Central Pacific (ECP) clade and a Pan-Pacific (PP) clade, separation of which was supported by high bootstrap value. The ECP clade consists of COTS from French Polynesia, Fiji, Vanuatu and the Great Barrier Reef (GBR). The Hawaii population is unique within this clade, while California COTS are included in EPC clade. On the other hand, the PP clade comprises multiple lineages that contain COTS from Vietnam, the Philippines, Japan, Papua New Guinea, Micronesia, the Marshall Islands, GBR, Vanuatu, Fiji and French Polynesia. For example, a lineage of the PP clade, which has the largest geographic distribution, includes COTS from all of these locations. These results suggest two alternative histories of current geographic distributions of COTS in the Pacific Ocean, an ECP clade ancestry or Western Pacific clade ancestry. Although further questions remain to be explored, this discovery provides an evolutionary context for the interpretation of COTS population structure which will aid future coral reef research in the Pacific Ocean, and ultimately improve reef management of COTS.
    We thank the following people for their help with sample collection: Dr. Hugh Sweatman and the AIMS Bioresources Library for GBR samples, Dr. Molly Timmers for Hawaiian samples, Geoff Jones and Jeff Kinch for Papua New Guinean samples, Monal Lal for Fijian samples, Christina Shaw for Vanuatu samples, Hoang Dinh Chieu for Vietnamese samples, and Hiromitsu Ueno for Japanese samples. The DNA Sequencing Section and IT section of OIST are acknowledged for its expert help with genome sequencing and bioinfomatic analysis. Last, but not least, we acknowledge the traditional owners of the lands and sea country on which this research took place.
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    Complex patterns of genetic structure in the sea cucumber Holothuria (Metriatyla) scabra from the Philippines: implications for aquaculture and fishery management
    Lal, Monal M.; Macahig, Deo A. S.; Juinio-Meñez, Marie A.; Altamirano, Jon P.; Noran-Baylon, Roselyn; de la Torre-de la Cruz, Margarita; Villamor, Janine L.; Gacura, Jonh Rey L.; Uy, Wilfredo H.; Mira-Honghong, Hanzel; Southgate, Paul C.; Ravago-Gotanco, Rachel (Frontiers Media SA, 2024-06-04)
    The sandfish Holothuria (Metriatyla) scabra, is a high-value tropical sea cucumber harvested from wild stocks for over four centuries in multi-species fisheries across its Indo-Pacific distribution, for the global bêche-de-mer (BDM) trade. Within Southeast Asia, the Philippines is an important centre of the BDM trade, however overharvesting and largely open fishery management have resulted in declining catch volumes. Sandfish mariculture has been developed to supplement BDM supply and assist restocking efforts; however, it is heavily reliant on wild populations for broodstock supply. Consequently, to inform fishery, mariculture, germplasm and translocation management policies for both wild and captive resources, a high-resolution genomic audit of 16 wild sandfish populations was conducted, employing a proven genotyping-by-sequencing approach for this species (DArTseq). Genomic data (8,266 selectively-neutral and 117 putatively-adaptive SNPs) were used to assess fine-scale genetic structure, diversity, relatedness, population connectivity and local adaptation at both broad (biogeographic region) and local (within-biogeographic region) scales. An independent hydrodynamic particle dispersal model was also used to assess population connectivity. The overall pattern of population differentiation at the country level for H. scabra in the Philippines is complex, with nine genetic stocks and respective management units delineated across 5 biogeographic regions: (1) Celebes Sea, (2) North and (3) South Philippine Seas, (4) South China and Internal Seas and (5) Sulu Sea. Genetic connectivity is highest within proximate marine biogeographic regions (mean Fst=0.016), with greater separation evident between geographically distant sites (Fst range=0.041–0.045). Signatures of local adaptation were detected among six biogeographic regions, with genetic bottlenecks at 5 sites, particularly within historically heavily-exploited locations in the western and central Philippines. Genetic structure is influenced by geographic distance, larval dispersal capacity, species-specific larval development and settlement attributes, variable ocean current-mediated gene flow, source and sink location geography and habitat heterogeneity across the archipelago. Data reported here will inform accurate and sustainable fishery regulation, conservation of genetic diversity, direct broodstock sourcing for mariculture and guide restocking interventions across the Philippines.
  • Transcriptome-derived SNP markers for population assignment of sandfish, Holothuria (Metriatyla) scabra
    Ordoñez, June F.; Ravago-Gotanco, Rachel (Elsevier, 2024-01-30)
    The sandfish, Holothuria scabra is a commercially important fishery and aquaculture species contributing to the high-value sea cucumber industry. Overexploited across many areas throughout its distributional range, natural populations are considered in decline. Accurate genetic assignment to population of origin is becoming increasingly important for genetics-based marine fisheries management and monitoring, especially for species experiencing depletion of natural stocks and decline in fisheries productivity due to overfishing and illegal, unreported, and unregulated (IUU) fishing. Initiatives for genetics-based applications on economically important seafood such as H. scabra have been limited by the lack of comprehensive genome or transcriptome resources. The present study developed and evaluated the use of gene-associated single nucleotide polymorphism (SNP) markers to assign sandfish to three locations in the Philippines, in the proximity of existing and emerging hatchery production centers. In silico SNP discovery pipeline using pooled RNA-Seq libraries and medium-throughput genotyping approach generated a dataset comprising 115 individuals genotyped at 88 SNPs. Population assignment using machine-learning analysis and Bayesian approach revealed that the 88 transcriptome-derived SNPs allowed the assignment of sandfish individuals to population of origin, with an overall assignment accuracy of >80%. The novel SNPs developed could find their utility in facilitating the development of geographic traceability tools applicable in the context of sandfish aquaculture, fisheries management and conservation.
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    Pseudocryptic diversity and species boundaries in the sea cucumber Stichopus cf. horrens (Echinodermata: Stichopodidae) revealed by mitochondrial and microsatellite markers
    Lizano, Apollo Marco D.; Kim, Kenneth M.; Juinio-Meñez, Marie Antonette; Ravago-Gotanco, Rachel (Nature Research, 2024)
    Morphologically cryptic and pseudo-cryptic species pose a challenge to taxonomic identification and assessments of species diversity and distributions. Such is the case for the sea cucumber Stichopus horrens, commonly confused with Stichopus monotuberculatus. Here, we used mitochondrial cytochrome oxidase subunit I (COI) and microsatellite markers to examine genetic diversity in Stichopus cf. horrens throughout the Philippine archipelago, to aid species identification and clarify species boundaries. Phylogenetic analysis reveals two recently diverged COI lineages (Clade A and Clade B; c. 1.35–2.54 Mya) corresponding to sequence records for specimens identified as S. monotuberculatus and S. horrens, respectively. Microsatellite markers reveal two significantly differentiated genotype clusters broadly concordant with COI lineages (Cluster 1, Cluster 2). A small proportion of individuals were identified as later-generation hybrids indicating limited contemporary gene flow between genotype clusters, thus confirming species boundaries. Morphological differences in papillae distribution and form are observed for the two species, however tack-like spicules from the dorsal papillae are not a reliable diagnostic character. An additional putative cryptic species was detected within Clade B-Cluster 2 specimens warranting further examination. We propose that these lineages revealed by COI and genotype data be referred to as Stichopus cf. horrens species complex. © The Author(s) 2024.