School of BioSciences - Research Publications

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    Bio-ORACLE v2.0: Extending marine data layers for bioclimatic modelling
    Assis, J ; Tyberghein, L ; Bosch, S ; Verbruggen, H ; Serrao, EA ; De Clerck, O (WILEY, 2018-03)
    Abstract Motivation The availability of user‐friendly, high‐resolution global environmental datasets is crucial for bioclimatic modelling. For terrestrial environments, WorldClim has served this purpose since 2005, but equivalent marine data only became available in 2012, with pioneer initiatives like Bio‐ORACLE providing data layers for several ecologically relevant variables. Currently, the available marine data packages have not yet been updated to the most recent Intergovernmental Panel on Climate Change (IPCC) predictions nor to present times, and are mostly restricted to the top surface layer of the oceans, precluding the modelling of a large fraction of the benthic diversity that inhabits deeper habitats. To address this gap, we present a significant update of Bio‐ORACLE for new future climate scenarios, present‐day conditions and benthic layers (near sea bottom). The reliability of data layers was assessed using a cross‐validation framework against in situ quality‐controlled data. This test showed a generally good agreement between our data layers and the global climatic patterns. We also provide a package of functions in the R software environment (sdmpredictors) to facilitate listing, extraction and management of data layers and allow easy integration with the available pipelines for bioclimatic modelling. Main types of variable contained Surface and benthic layers for water temperature, salinity, nutrients, chlorophyll, sea ice, current velocity, phytoplankton, primary productivity, iron and light at bottom. Spatial location and grain Global at 5 arcmin (c. 0.08° or 9.2 km at the equator). Time period and grain Present (2000–2014) and future (2040–2050 and 2090–2100) environmental conditions based on monthly averages. Major taxa and level of measurement Marine biodiversity associated with sea surface and epibenthic habitats. Software format ASCII and TIFF grid formats for geographical information systems and a package of functions developed for R software.
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    Diversity and stability of coral endolithic microbial communities at a naturally high pCO2 reef
    Marcelino, VR ; Morrow, KM ; van Oppen, MJH ; Bourne, DG ; Verbruggen, H (WILEY, 2017-10)
    The health and functioning of reef-building corals is dependent on a balanced association with prokaryotic and eukaryotic microbes. The coral skeleton harbours numerous endolithic microbes, but their diversity, ecological roles and responses to environmental stress, including ocean acidification (OA), are not well characterized. This study tests whether pH affects the diversity and structure of prokaryotic and eukaryotic algal communities associated with skeletons of Porites spp. using targeted amplicon (16S rRNA gene, UPA and tufA) sequencing. We found that the composition of endolithic communities in the massive coral Porites spp. inhabiting a naturally high pCO2 reef (avg. pCO2 811 μatm) is not significantly different from corals inhabiting reference sites (avg. pCO2 357 μatm), suggesting that these microbiomes are less disturbed by OA than previously thought. Possible explanations may be that the endolithic microhabitat is highly homeostatic or that the endolithic micro-organisms are well adapted to a wide pH range. Some of the microbial taxa identified include nitrogen-fixing bacteria (Rhizobiales and cyanobacteria), algicidal bacteria in the phylum Bacteroidetes, symbiotic bacteria in the family Endozoicomoniaceae, and endolithic green algae, considered the major microbial agent of reef bioerosion. Additionally, we test whether host species has an effect on the endolithic community structure. We show that the endolithic community of massive Porites spp. is substantially different and more diverse than that found in skeletons of the branching species Seriatopora hystrix and Pocillopora damicornis. This study reveals highly diverse and structured microbial communities in Porites spp. skeletons that are possibly resilient to OA.
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    Analysis of chloroplast genomes and a supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta)
    Diaz-Tapia, P ; Maggs, CA ; West, JA ; Verbruggen, H ; Müller, K (WILEY, 2017-10-01)
    With over a thousand species, the Rhodomelaceae is the most species-rich family of red algae. While its genera have been assigned to 14 tribes, the high-level classification of the family has never been evaluated with a molecular phylogeny. Here, we reassess its classification by integrating genome-scale phylogenetic analysis with observations of the morphological characters of clades. In order to resolve relationships among the main lineages of the family we constructed a phylogeny with 55 chloroplast genomes (52 newly determined). The majority of branches were resolved with full bootstrap support. We then added 266 rbcL, 125 18S rRNA gene and 143 cox1 sequences to construct a comprehensive phylogeny containing nearly half of all known species in the family (407 species in 89 genera). These analyses suggest the same subdivision into higher-level lineages, but included many branches with moderate or poor support. The circumscription for nine of the 13 previously described tribes was supported, but the Lophothalieae, Polysiphonieae, Pterosiphonieae and Herposiphonieae required revision, and five new tribes and one resurrected tribe were segregated from them. Rhizoid anatomy is highlighted as a key diagnostic character for the morphological delineation of several lineages. This work provides the most extensive phylogenetic analysis of the Rhodomelaceae to date and successfully resolves the relationships among major clades of the family. Our data show that organellar genomes obtained through high-throughput sequencing produce well-resolved phylogenies of difficult groups, and their more general application in algal systematics will likely permit deciphering questions about classification at many taxonomic levels.
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    TAXONOMIC RESHUFFLING OF THE CLADOPHORACEAE
    Rindi, F ; Verbruggen, H (WILEY, 2016-12)
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    Multigene analyses resolve early diverging lineages in the Rhodymeniophycidae (Florideophyceae, Rhodophyta)
    Saunders, GW ; Filloramo, G ; Dixon, K ; Le Gall, L ; Maggs, CA ; Kraft, GT ; Verbruggen, H (WILEY-BLACKWELL, 2016-08)
    Multigene phylogenetic analyses were directed at resolving the earliest divergences in the red algal subclass Rhodymeniophycidae. The inclusion of key taxa (new to science and/or previously lacking molecular data), additional sequence data (SSU, LSU, EF2, rbcL, COI-5P), and phylogenetic analyses removing the most variable sites (site stripping) have provided resolution for the first time at these deep nodes. The earliest diverging lineage within the subclass was the enigmatic Catenellopsis oligarthra from New Zealand (Catenellopsidaceae), which is here placed in the Catenellopsidales ord. nov. In our analyses, Atractophora hypnoides was not allied with the other included Bonnemaisoniales, but resolved as sister to the Peyssonneliales, and is here assigned to Atractophoraceae fam. nov. in the Atractophorales ord. nov. Inclusion of Acrothesaurum gemellifilum gen. et sp. nov. from Tasmania has greatly improved our understanding of the Acrosymphytales, to which we assign three families, the Acrosymphytaceae, Acrothesauraceae fam. nov. and Schimmelmanniaceae fam. nov.
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    APPLICATION OF MULTIGENE PHYLOGENETICS AND SITE-STRIPPING TO RESOLVE INTRAORDINAL RELATIONSHIPS IN THE RHODYMENIALES (RHODOPHYTA)
    Filloramo, GV ; Saunders, GW ; Verbruggen, H (WILEY, 2016-06)
    Previous molecular assessments of the red algal order Rhodymeniales have confirmed its monophyly and distinguished the six currently recognized families (viz. Champiaceae, Faucheaceae, Fryeellaceae, Hymenocladiaceae, Lomentariaceae, and Rhodymeniaceae); however, relationships among most of these families have remained unresolved possibly as a result of substitution saturation at deeper phylogenetic nodes. The objective of the current study was to improve rhodymenialean systematics by increasing taxonomic representation and using a more robust multigene dataset of mitochondrial (COB, COI/COI-5P), nuclear (LSU, EF2) and plastid markers (psbA, rbcL). Additionally, we aimed to prevent phylogenetic inference problems associated with substitution saturation (particularly at the interfamilial nodes) by removing fast-evolving sites and analyzing a series of progressively more conservative alignments. The Rhodymeniales was resolved as two major lineages: (i) the Fryeellaceae as sister to the Faucheaceae and Lomentariaceae; and (ii) the Rhodymeniaceae allied to the Champiaceae and Hymenocladiaceae. Support at the interfamilial nodes was highest when 20% of variable sites were removed. Inclusion of Binghamiopsis, Chamaebotrys, and Minium, which were absent in previous phylogenetic investigations, established their phylogenetic affinities while assessment of two genera consistently polyphyletic in phylogenetic analyses, Erythrymenia and Lomentaria, resulted in the proposition of the novel genera Perbella and Fushitsunagia. The taxonomic position of Drouetia was reinvestigated with re-examination of holotype material of D. coalescens to clarify tetrasporangial development in this genus. In addition, we added three novel Australian species to Drouetia as a result of ongoing DNA barcoding assessments-D. aggregata sp. nov., D. scutellata sp. nov., and D. viridescens sp. nov.
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    RHODENIGMA CONTORTUM, AN OBSCURE NEW GENUS AND SPECIES OF RHODOGORGONALES (RHODOPHYTA) FROM WESTERN AUSTRALIA
    West, JA ; Zuccarello, GC ; de Goer, SL ; Stavrias, LA ; Verbruggen, H ; Gabrielson, P (WILEY-BLACKWELL, 2016-06)
    An unknown microscopic, branched filamentous red alga was isolated into culture from coral fragments collected in Coral Bay, Western Australia. It grew well unattached or attached to glass with no reproduction other than fragmentation of filaments. Cells of some branch tips became slightly contorted and digitated, possibly as a substrate-contact-response seen at filament tips of various algae. Attached multicellular compact disks on glass had a very different cellular configuration and size than the free filaments. In culture the filaments did not grow on or in coral fragments. Molecular phylogenies based on four markers (rbcL, cox1, 18S, 28S) clearly showed it belongs to the order Rhodogorgonales, as a sister clade of Renouxia. Based on these results, the alga is described as the new genus and species Rhodenigma contortum in the Rhodogorgonaceae. It had no morphological similarity to either of the other genera in Rhodogorgonaceae and illustrates the unknown diversity in cryptic habitats such as tropical coral rubble.
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    Global biogeographic structuring of tropical shallow-water brittle stars
    Bribiesca-Contreras, G ; Verbruggen, H ; Hugall, AF ; O'Hara, TD (WILEY, 2019-07)
    AIM: Biogeographic barriers emerged in the tropical oceans as continental masses moved with plate tectonics, and as the tropics contracted to lower latitudes from the late Eocene. These barriers have shaped tropical marine biodiversity. We characterize large‐scale diversity patterns for tropical brittle stars and investigate the effect of biogeographic barriers on these in space and time. LOCATION: Shallow‐water (<200 m) tropical oceans. TAXON: Tropical shallow‐water brittle stars (class Ophiuroidea). METHODS: We integrate phylogenetic and biogeographic modelling to test and quantify the biogeographic structuring across the major ocean basins for five families of brittle stars. These are well‐sampled in our phylogenies (173 species) and represent an important component of the brittle star fauna of tropical shallow waters. We define major bioregions based on patterns of compositional and phylogenetic beta diversity. RESULTS: We find congruence between patterns of shared ancestry of regions and inferred biogeographic histories. Biogeographic reconstructions show that faunal patterns reflect the emergence of biogeographic barriers in the tropical world, with evidence of vicariant events driven by the opening of the Atlantic Ocean, the narrowing of the Tethyan Seaway and the rise of the Isthmus of Panama. MAIN CONCLUSIONS: Biogeographic barriers almost completely isolated regional faunas. However, divergence age estimates predate the onset of the different barriers, suggesting that changes associated with the gradual emergence of the barriers had a strong effect on the evolutionary history of tropical shallow‐water brittle stars. Limited, very recent, bi‐directional dispersal was detected across the East Pacific Barrier, which is otherwise an important barrier for dispersal of brittle stars.
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    Widely distributed red algae often represent hidden introductions, complexes of cryptic species or species with strong phylogeographic structure
    Diaz-Tapia, P ; Maggs, CA ; Macaya, EC ; Verbruggen, H ; Müller, K (WILEY, 2018-12)
    Despite studies suggesting that most seaweeds are poor dispersers, many red algal species are reported to have circumglobal distributions. Such distributions have mostly been based on morphological identifications, but molecular data have revealed a range of issues with morphologically defined species boundaries. Consequently, the real distribution of such reportedly circumglobal species must be questioned. In this study, we analyzed molecular data sets (rbcL gene) of nine species in the Rhodomelaceae for which samples were available from widely spaced geographical locations. Three overall patterns were identified: (i) species showing strong phylogeographic structure (i.e., phylogenetic similarity correlates with geographical provenance), often to the point that populations from different locations could be considered as different species (Lophosiphonia obscura, Ophidocladus simpliciusculus, Polysiphonia villum, and Xiphosiphonia pinnulata); (ii) species with a broad distribution that is explained, in part, by putative human-mediated transport (Symphyocladia dendroidea and Polysiphonia devoniensis); and (iii) non-monophyletic complexes of cryptic species, most with a more restricted distribution than previously thought (Herposiphonia tenella, Symphyocladia dendroidea, and the Xiphosiphonia pennata complex that includes the species Xiphosiphonia pinnulata and Symphyocladia spinifera). This study shows that widely distributed species are the exception in marine red algae, unless they have been spread by humans.
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    Patterns and drivers of species diversity in the Indo-Pacific red seaweed Portieria
    Leliaert, F ; Payo, DA ; Gurgel, CFD ; Schils, T ; Draisma, SGA ; Saunders, GW ; Kamiya, M ; Sherwood, AR ; Lin, S-M ; Huisman, JM ; Le Gall, L ; Anderson, RJ ; Bolton, JJ ; Mattio, L ; Zubia, M ; Spokes, T ; Vieira, C ; Payri, CE ; Coppejans, E ; D'hondt, S ; Verbruggen, H ; De Clerck, O (WILEY, 2018-10)
    AIM: Biogeographical processes underlying Indo‐Pacific biodiversity patterns have been relatively well studied in marine shallow water invertebrates and fishes, but have been explored much less extensively in seaweeds, despite these organisms often displaying markedly different patterns. Using the marine red alga Portieria as a model, we aim to gain understanding of the evolutionary processes generating seaweed biogeographical patterns. Our results will be evaluated and compared with known patterns and processes in animals. LOCATION: Indo‐Pacific marine region. METHODS: Species diversity estimates were inferred using DNA‐based species delimitation methods. Historical biogeographical patterns were inferred based on a six‐gene time‐calibrated phylogeny, distribution data of 802 specimens, and probabilistic modelling of geographical range evolution. The importance of geographical isolation for speciation was further evaluated by population genetic analyses at the intraspecific level. RESULTS: We delimited 92 candidate species, most with restricted distributions, suggesting low dispersal capacity. Highest species diversity was found in the Indo‐Malay Archipelago (IMA). Our phylogeny indicates that Portieria originated during the late Cretaceous in the area that is now the Central Indo‐Pacific. The biogeographical history of Portieria includes repeated dispersal events to peripheral regions, followed by long‐term persistence and diversification of lineages within those regions, and limited dispersal back to the IMA. MAIN CONCLUSIONS: Our results suggest that the long geological history of the IMA played an important role in shaping Portieria diversity. High species richness in the IMA resulted from a combination of speciation at small spatial scales, possibly as a result of increased regional habitat diversity from the Eocene onwards, and species accumulation via dispersal and/or island integration through tectonic movement. Our results are consistent with the biodiversity feedback model, in which biodiversity hotspots act as both “centres of origin” and “centres of accumulation,” and corroborate previous findings for invertebrates and fish that there is no single unifying model explaining the biological diversity within the IMA.