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ATLAS Deliverable 4.4: Reproduction, dispersal and genetic connectivity in benthos and fishes

Carreiro-Silva, M; Fox, A; Carlsson, J; Carlsson, JEL; Orejas, C; Roterman, CNR; Rakka, M; Boavida, J; González- Irusta, J; Morato, T; Bilan, M; Movilla, J; Godinho, A; Arnaud-Haond, S


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    <dct:title>ATLAS Deliverable 4.4: Reproduction, dispersal and genetic connectivity in benthos and fishes</dct:title>
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    <dct:description>&lt;p&gt;In the marine realm, the management of fishery resources, the control and prevention of invasive species and the conservation plans for threatened species or vulnerable ecosystems (some already suffering well characterized declines such as coral reefs &amp;ndash;Aichi target 10-, seagrass, and mangroves) requires the knowledge of interconnection and interdependency of stocks, populations and communities constituting these ecosystems. A particular challenge in marine systems is that most marine organisms exhibit a complex life cycle with two phases, including an adult stage with limited or no movements and a larval dispersive stage. In addition, many fish species can have dispersive phases during the larval, juvenile and adult phases. The direct observation and study of migratory movements is almost impossible in the oceans due to i) the reduced potential to fully access the marine environment, ii) the often minute size of the dispersing stages, iii) the often extremely large population sizes sensu stricto, and iv) the generally substantial migration distances, at adult or larval stages, with no strict a priori relationship with life history traits suspected to influence dispersal potential (Riginos et al., 2011). All those technical challenges to direct observation are of course exacerbated in the deep-sea, making models of predictive connectivity and indirect inferences a strong need. Molecular data interpreted in the theoretical framework of population genetics (Hellberg et al., 2002), ideally integrated with modelling approaches, have thus a central role to play in the study of marine connectivity.&lt;br&gt; Both predictive modelling and indirect inferences based on population genomics (and in some cases on biochemical analysis of calcified structures such as otoliths or shells) need to be fed by a good knowledge of the biology and ecology of species being studied. More precisely, Lagrangian modelling of particles requires input from a diversity of fields to deliver the most accurate predictions. Mostly three fields of research are at stake that are all represented in ATLAS consortium. First, oceanographic data are needed to establish the way currents can act as conveying belt for the dispersal of particles or in some cases adult stages. Second, habitat mapping and modelling to feed the model with knowledge of the geographic locations where dispersing life stages can be emitted from and those they can viably settle because many marine, and in particular deep-sea species have a spatially fragmented distribution. Third, reproductive biology information including the nature, duration and behaviour of the dispersing life stage because most deep-sea species&amp;rsquo; dispersal relies on the pelagic larval stages (Cowen and Sponaugle 2009, Hil&amp;aacute;rio et al. 2015), is required to accurately choose the oceanographic data in terms of season when dispersal can take place and define a confidence interval for its duration, chose the&amp;nbsp;depth of currents to be considered at different time steps, and account for the ability to mitigate or enhance their influence through active dispersal.&lt;br&gt; Genomic data need to be interpreted with a good knowledge of historical habitat modifications (at evolutionary time scales) to understand the signature left on the genomic composition of species by past patterns of past connectivity and indirectly reconstruct their modification, as well as that of species distribution range under the effect of past environmental changes. These can be done through the analysis of sequence divergence, allelic frequency and modelling. Multi-locus genotype based analysis can then be used to infer more contemporary patterns of connectivity that would correspond to a similar time scale as the predictions issued from Lagrangian modelling. In all cases, a good knowledge of the reproductive biology of species (particularly their ability to reproduce and persist through sexual reproduction, but also to self-fertilize) is also required to accurately transform observations of the geographic distribution of genetic polymorphism into inferences as to the present or past patterns of connectivity.&amp;nbsp;However, deep-sea species are harder to manipulate than their coastal counterparts, making it extremely difficult to observe or keep them in aquaria facilities in order to obtain the relevant information required for sound modelling predictions. During the ATLAS project, we successfully induced spawning and reared larvae of the octocoral Viminella flagellum under aquaria conditions. This was the first time that the larvae biology of a deep-sea octocoral has been studied. In addition, we have characterized the reproductive biology and gametogenic cycle of four CWC species that form important Vulnerable Marine Ecosystems (VMEs) in the Mediterranean and the Azores.&lt;br&gt; Studies on coral reproduction revealed that all species studied were gonochoric (separate sexes), broadcast spawners (release of gametes into the water column) with continuous gametogenic cycles. The dendrophyllids Dendrophyllia cornigera and Dendrophyllia ramea from the Mediterranean come from relatively shallow depth ca. 50-100 m depth and their spawning seems to be coupled with seawater temperature. In contrast, spawning in the octocorals Dentomuricea meteor and V. flagellum collected from 200-500m deep the Azores seem to follow seasons with high primary productivity, in spring and autumn. Assexual reproduction was also studied for the octocorals Acanthogorgia armata and Acanella arbuscula based on aquaria observations. These octocorals displayed the ability of polyp bailout, with polyp dissociation from the mother colony resulting in free negatively buoyant polyps without any calcareous material. Polyp bailout is described as a stress response and an expression of reverse development, i.e. the ability of adult forms to develop into earlier developmental stages, which have higher probabilities of dispersal. It therefore may represent an important mechanism of dispersal under unfavourable conditions caused by increasing anthropogenic activities and climate change.&lt;br&gt; Larvae biology of the octocoral V. flagellum was studied under aquaria conditions, and the data produced used for the connectivity modelling studies in section 4. This is the first study on the larvae biology of a deep-sea octocoral, with results indicating a lower pelagic larvae duration (PDL) than the reef-bulding species Lophelia pertusa (12 days in V. flagellum compare with 3-5 weeks in L. pertusa).This influences the dispersal ability of this species, which seems to be much shorter that L. pertusa.&amp;nbsp;On the basis of this knowledge, and the one produced in WP3 for habitat mapping and modelling (for species for which enough data were available) and WP1 for water masses movements, the Lagrangian modelling could be adapted to fit several species studied in ATLAS, for which a benthic adult stage rendered coherent the hypothesis of a mainly larval driven dispersal. This included 2 invertebrates (the reef-building coral L. pertusa and the octocoral V. flagellum) and one fish species (Helicolenus dactylopterus) (section 5). Modelling of dispersal of the echinoid Cidaris cidaris was attempted but proved impossible due to the limited presence records of this species on public databases that could be used in habitat distribution models; likely erroneous records of presence derived from video and photographic data owing to morphological similarity with other taxa, and poor constraint in the population genetics of C. cidaris populations in the North Atlantic and Mediterranean. In order to account for uncertainties for many other species for which the reproductive biology could not be studied and information is lacking, nine &amp;lsquo;generic&amp;rsquo; models were produced at the scale of the North Atlantic. Those include lower, average and higher bounds for larval duration and movement in the water column. The aim of this exercise was to produce connectivity matrices that could be i) compared to inferences based on population genetics data in order to select the prediction that would best match the inference of connectivity and ii) be available for future studies as knowledge of the reproductive biology of species will inform the choice of one of the nine available scenarios that would best fit&amp;nbsp;the species being studied (available at Zenodo). These generic connectivity matrices clearly show the increased dispersal potential of increasing PLDs and drifting closer to the surface. They also highlight the regions of stronger currents as important sources of larvae, particularly currents along the continental slopes.&lt;br&gt; Individual species models for the corals L. pertusa, V. flagellum and the fish H. dactylopterus demonstrate how hydrodynamically-based modelled connectivity can be combined with species-specific habitat suitability models to suggest connectivity by species. Model outputs show how this predicted connectivity varies considerably with the assumptions made about larval behaviour. One common feature was that populations along the eastern boundary of the North Atlantic may be generally more strongly connected. However, as currents are generally weak here (compared to those on the western and northern boundaries of the basin) this conclusion is probably dependent on the existence of a near-continuous band of suitable habitat from the mouth of the Mediterranean northwards.&lt;br&gt; Connectivity models for L. pertusa under future climate scenarios suggest present day regions of high connectivity - important sources and sinks of larvae &amp;ndash; will have much reduced connectivity, with the best connectivity future sites found northwards along the coast of Greenland and Canada. In addition, in the south areas, the reduced population in the Azores, previously supplying larvae to the US and European coasts via intermediate seamounts, becomes connected only along the mid-Atlantic ridge, with some larvae still coming in from the US coast. Predictions of future distribution and connectivity for H. dactylopterus show expansion in the suitable habitat range to the north and west particularly into the Labrador Sea. However, predictions show that with the exception of the Azores and seamounts in the Mid-Atlantic Ridge, H. dactylopterus may become a single strongly connected component under future conditions, suggesting that H. dactylopterus population may become more robust and resilient under changed future conditions.&lt;br&gt; Finally, both sampling and genomic resources could be gathered to deliver inferences of connectivity at different time scales for two invertebrate VME indicator species (L. pertusa and Madrepora oculata), and their commensal polychaete Eunice norvegica, the associated invertebrate species to VMEs (Cidaris cidaris) and three species exploited by fisheries, i.e. two fish species (Capros aper and Trachurus trachurus) and one crustacean (Nephrops norvegicus) (section 6).&amp;nbsp;Results from genetic analyses and modelling simulations are mostly concordant for , indicating that L. pertusa forms a large panmictic genetic cluster (ie, a group with random mating) along most of the NE Atlantic European margins (excluding the Mediterranean Sea). The large individual&amp;nbsp;aggregations associated to a long larval dispersal time mediated by ocean currents may lead to high gene flow among the distant NE Atlantic cold-water coral reefs. Cases of inconsistent findings between observed genetic data and dispersal simulations, such as the location of hypothetical past climatic refugia that may have acted as post-glacial colonization sources, highlighted that other processes not yet captured may be operating (eg, the degree to which larval dispersal is driving genetic patterns across the seascape, habitat quality, variation in reproduction, population density and local selection), as well as differences between the location of genetic samples and modelled spatial extent. Despite local discrepancies, biophysical models have helped understand the complex process of gene flow and can inform future work.&lt;br&gt; With the echinoid Cidaris cidaris, the population genetics results are tentative as the high-resolution genomic single nucleotide polymorphism (SNP) dataset is still undergoing quality control and analysis. The preliminary examination of COI mitochondrial gene fragments indicates no clear barriers to connectivity between North Atlantic and Western Mediterranean specimens, or between specimens collected between 200 m and 1200 m depth; consistent with a theorised highly dispersive planktotrophic larval phase in the Cidaris genus, whereby larvae feed near the surface and are transported by faster surface currents. The higher resolution genomic SNP dataset may yet reveal subtle patterns of geographic constraints on long-distance gene flow, or regionally determined variability in selective pressures, however.&lt;br&gt; The genetic studies of Caprus aper clearly demonstrated that the species does not constitute a single panmictic population across the sampled range. Samples from the Mediterranean Sea showed the largest genetic differentiation. Similarly, studies on Nephrops norvegicus indicated that the Mediterranean samples from the Adriatic Sea are significantly differentiated from the Atlantic samples analysed. Furthermore, both species showed further diferentiation, although weaker, among the Atlantic samples. The studies of Trachururs trachurus are ongoing (samples from the Mediterranenan Sea are yet to be analysed) but the preliminary results indicate that the species is represented by multiple populations. In summary, there is clear population structure within all three species exploited by fisheries and this information could be used by managers to improve the management of these marine resources.&lt;br&gt; Among all ten species for which advances could be made either in terms of knowledge of the reproductive biology, dispersal modelling or population genomics, a full set of information could be gathered for the emblematic reef-building L. pertusa, and the consortium is also trying to finalize the genomic data production for the exploited fish H. dactylopterus.&amp;nbsp;Perpectives beyond this report include the finalization of data production and analysis, and the test of a new method to go beyond the usual &amp;ldquo;side by side&amp;rdquo; comparison of predicted (lagrangian modelling) versus realized (inferences from population genomics) dispersal by integrating the Lagrangian matrices of connectivity as priors of a Bayesian analysis (Gaggiotti, 2017) of the genetic dataset characterizing the metapopulation system being studied. Such integrative framework has long been expected by the scientific community addressing connectivity through the use of a diversity of tools and theoretical framework as the ones detailed in this report. The recent development of this new analytical tool will allow testing this approach on the scleractinian coral L. pertusa. All results obtained here will be used to deliver information useful for the conservation and management of VMEs and fisheries resources (WP 6 and 7), an advance that will be formalized in the next report of WP4, DL4.5 &amp;ldquo;Integrated management considering connectivity patterns&amp;rdquo;.&amp;nbsp;&lt;/p&gt;</dct:description>
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