Combining population genomics and biophysical modelling to assess connectivity patterns in an Antarctic fish.

Connectivity is a fundamental process of population dynamics in marine ecosystems. In the last decade, with the emergence of new methods, combining different approaches to understand the patterns of connectivity among populations and their regulation has become increasingly feasible. The Western Antarctic Peninsula (WAP) is characterized by complex oceanographic dynamics, where local conditions could act as barriers to population connectivity. Here, the notothenioid fish Harpagifer antarcticus, a demersal species with a complex life cycle (adults with poor swim capabilities and pelagic larvae), was used to assess connectivity along the WAP by combining biophysical modelling and population genomics methods. Both approaches showed congruent patterns. Areas of larvae retention and low potential connectivity, observed in the biophysical model output, coincide with four genetic groups within the WAP: (1) South Shetland Islands, (2) Bransfield Strait, (3) the central and (4) the southern area of WAP (Marguerite Bay). These genetic groups exhibited limited gene flow between them, consistent with local oceanographic conditions, which would represent barriers to larval dispersal. The joint effect of geographic distance and larval dispersal by ocean currents had a greater influence on the observed population structure than each variable evaluated separately. The combined effect of geographic distance and a complex oceanographic dynamic would be generating limited levels of population connectivity in the fish H. antarcticus along the WAP. Based on this, population connectivity estimations and priority areas for conservation were discussed, considering the marine protected area proposed for this threatened region of the Southern Ocean.

Unveiling the co-phylogeny signal between plunderfish Harpagifer spp. and their gut microbiomes across the Southern Ocean.

Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. However, closely related hosts are valuable models for deciphering the contribution of host evolutionary history to microbiome assembly, through the underscoring of phylosymbiosis and co-phylogeny patterns. Here, we propose that the recent diversification of several Harpagifer species across the Southern Ocean would allow the detection of robust phylogenetic congruence between the host and its microbiome. We characterized the gut mucosa microbiome of 77 individuals from four field-collected species of the plunderfish Harpagifer (Teleostei, Notothenioidei), distributed across three biogeographic regions of the Southern Ocean. We found that seawater physicochemical properties, host phylogeny, and geography collectively explained 35% of the variation in bacterial community composition in Harpagifer gut mucosa. The core microbiome of Harpagifer spp. gut mucosa was characterized by a low diversity, mostly driven by selective processes, and dominated by a single Aliivibrio Operational Taxonomic Unit (OTU) detected in more than 80% of the individuals. Nearly half of the core microbiome taxa, including Aliivibrio, harbored co-phylogeny signal at microdiversity resolution with host phylogeny, indicating an intimate symbiotic relationship and a shared evolutionary history with Harpagifer. The clear phylosymbiosis and co-phylogeny signals underscore the relevance of the Harpagifer model in understanding the role of fish evolutionary history in shaping the gut microbiome assembly. We propose that the recent diversification of Harpagifer may have led to the diversification of Aliivibrio, exhibiting patterns that mirror the host phylogeny. IMPORTANCE: Although challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it highlights intimate associations between hosts and ecologically relevant microbial symbionts. Our study leverages a natural system of closely related fish species in the Southern Ocean to unveil new insights into the contribution of host evolutionary trajectory on gut microbiome assembly, an underappreciated driver of the global marine fish holobiont. Notably, we unveiled striking evidence of co-diversification between Harpagifer and its microbiome, demonstrating both phylosymbiosis of gut bacterial communities and co-phylogeny of some specific bacterial symbionts, mirroring the host diversification patterns. Given Harpagifer's significance as a trophic resource in coastal areas and its vulnerability to climatic and anthropic pressures, understanding the potential evolutionary interdependence between the hosts and its microbiome provides valuable microbial candidates for future monitoring, as they may play a pivotal role in host species acclimatization to a rapidly changing environment.

Is the southern crab Halicarcinus planatus (Fabricius, 1775) the next invader of Antarctica?

The potential for biological colonization of Antarctic shores is an increasingly important topic in the context of anthropogenic warming. Successful Antarctic invasions to date have been recorded exclusively from terrestrial habitats. While non-native marine species such as crabs, mussels and tunicates have already been reported from Antarctic coasts, none have as yet established there. Among the potential marine invaders of Antarctic shallow waters is Halicarcinus planatus (Fabricius, 1775), a crab with a circum-Subantarctic distribution and substantial larval dispersal capacity. An ovigerous female of this species was found in shallow waters of Deception Island, South Shetland Islands in 2010. A combination of physiological experiments and ecological modelling was used to assess the potential niche of H. planatus and estimate its future southward boundaries under climate change scenarios. We show that H. planatus has a minimum thermal limit of 1°C, and that its current distribution (assessed by sampling and niche modelling) is physiologically restricted to the Subantarctic region. While this species is presently unable to survive in Antarctica, future warming under both 'strong mitigation' and 'no mitigation' greenhouse gas emission scenarios will favour its niche expansion to the Western Antarctic Peninsula (WAP) by 2100. Future human activity also has potential to increase the probability of anthropogenic translocation of this species into Antarctic ecosystems.

Unveiling the unknown phylogenetic position of the scallop Austrochlamys natans and its implications for marine stewardship in the Magallanes Province.

Two species of scallop, Austrochlamys natans ("Ostión del Sur") and Zygochlamys patagonica ("Ostión patagonico") are presently exploited in the southern part of the Magallanes Province (MP). The lack of clarity in taxonomic identification and ecological aspects is generating both erroneous extraction statistics and an unperceived harvesting pressure on A. natans and Z. patagonica. We aim to discriminate these Magallanes scallops accurately, improve our understanding of their complex natural history and discuss possible implications for their management and conservation status, given the current fisheries statistics. To achieve these goals, we present a complete review of the historical identification of the Magallanes scallop and a multi-locus molecular phylogeny which allowed us to recover the phylogenetic position of A. natans. We sampled 54 individuals from five localities across the southern Pacific coast of the MP. We calculated the depth of the byssal notch (BND) and shell height (VH) ratio from morphological characters and conducted phylogenetic reconstructions with mitochondrial (12S and 16S) and nuclear markers (28S) using Bayesian and maximum likelihood analyses. Both morphology and molecular phylogeny identified two distinct entities, Z. patagonica and a distinct, highly divergent lineage that corresponds to A. natans. Our study provides integrative evidence to alert the current fishery management and the need for further conservation studies.

Next-generation sequencing yields the complete organellar genomes of kelp Lessonia flavicans (Lessoniaceae, Phaeophyceae) from the Sub-Antarctic ecoregion of Magallanes, Chile.

The generitype Lessonia flavicans Bory is an endemic and important kelp from Sub-Antarctic Magellanic ecoregion that shows affinity to extreme salinity, temperature, and photoperiod conditions. Genomic analysis of L. flavicans from Rinconada Bulnes, Punta Arenas, Chile, resulted in the assembly of its organellar genomes. The L. flavicans complete mitogenome is 37,226 base pairs (bp) in length and contains 66 genes (GenBank accession number MN561186), the complete plastid genome is 130,085 bp and has 173 genes (MN561187) and the data assembled 8205 bp of the nuclear ribosomal cistron (MN561188). The organellar genomes are similar in structure and content to L. spicata (Suhr) Santelices and other Laminariales.

Mitogenomics of Perumytilus purpuratus (Bivalvia: Mytilidae) and its implications for doubly uniparental inheritance of mitochondria.

Animal mitochondria are usually inherited through the maternal lineage. The exceptional system allowing fathers to transmit their mitochondria to the offspring exists in some bivalves. Its taxonomic spread is poorly understood and new mitogenomic data are needed to fill the gap. Here, we present for the first time the two divergent mitogenomes from Chilean mussel Perumytilus purpuratus. The existence of these sex-specific mitogenomes confirms that this species has the doubly uniparental inheritance (DUI) of mitochondria. The genetic distance between the two mitochondrial lineages in P. purpuratus is not only much bigger than in the Mytilus edulis species complex but also greater than the distance observed in Musculista senhousia, the only other DUI-positive member of the Mytilidae family for which both complete mitochondrial genomes were published to date. One additional, long ORF (open reading frame) is present exclusively in the maternal mitogenome of P. purpuratus. This ORF evolves under purifying selection, and will likely be a target for future DUI research.

Genetic structure and demographic inference of the regular sea urchin Sterechinus neumayeri (Meissner, 1900) in the Southern Ocean: The role of the last glaciation.

One of the most relevant characteristics of the extant Southern Ocean fauna is its resiliency to survive glacial processes of the Quaternary. These climatic events produced catastrophic habitat reductions and forced some marine benthic species to move, adapt or go extinct. The marine benthic species inhabiting the Antarctic upper continental shelf faced the Quaternary glaciations with different strategies that drastically modified population sizes and thus affected the amount and distribution of intraspecific genetic variation. Here we present new genetic information for the most conspicuous regular sea urchin of the Antarctic continental shelf, Sterechinus neumayeri. We studied the patterns of genetic diversity and structure in this broadcast-spawner across three Antarctic regions: Antarctic Peninsula, the Weddell Sea and Adélie Land in East Antarctica. Genetic analyses based on mitochondrial and nuclear markers suggested that S. neumayeri is a single genetic unit around the Antarctic continent. The species is characterized by low levels of genetic diversity and exhibits a typical star-like haplotype genealogy that supports the hypothesis of a single in situ refugium. Based on two mutation rates standardized for this genus, the Bayesian Skyline plot analyses detected a rapid demographic expansion after the Last Glacial Maximum. We propose a scenario of rapid postglacial expansion and recolonization of Antarctic shallow areas from a less ice-impacted refugium where the species survived the LGM. Considering the patterns of genetic diversity and structure recorded in the species, this refugium was probably located in East Antarctica.

Trophic ecology of two co-existing Sub-Antarctic limpets of the genus Nacella: spatio-temporal variation in food availability and diet composition of Nacella magellanica and N. deaurata.

Interactions between algae and herbivores can be affected by various factors, such as seasonality and habitat structure. Among herbivores inhabiting marine systems, species of the order Patellogastropoda are considered key organisms in many rocky coasts of the world. Nacella species are one of the most dominant macro-herbivores on the rocky shores of the sub-Antarctic ecoregion of Magellan. However, the importance of its key role must be associated with its trophic ecology. The objective of this work was to evaluate spatial and temporal variabilities in the dietary composition of two intertidal Nacella species, considering grazing on macro- (macroalgae) and microscopic (periphyton) food. The composition of periphyton and the availability of macroalgae in the winter and summer seasons were examined at two localities of the Magellanic province, alongside the gut contents of N. magellanica and N. deaurata. The dietary composition differed between the two Nacella species, as well as between seasons and locations. The differences observed in the diet of the two species of Nacella may be mainly due to their respective distributions in the intertidal zone. Both species presented a generalist strategy of grazing, which is relationed to the seasonality of micro- and macroalgae availability and to the variability of the assemblages between the localities. This research was the first to perform a detailed study of the diet of intertidal Nacella species.

Genetics, Gene Flow, and Glaciation: The Case of the South American Limpet Nacella mytilina.

Glacial episodes of the Quaternary, and particularly the Last Glacial Maximum (LGM) drastically altered the distribution of the Southern-Hemisphere biota, principally at higher latitudes. The irregular coastline of Patagonia expanding for more than 84.000 km constitutes a remarkable area to evaluate the effect of Quaternary landscape and seascape shifts over the demography of near-shore marine benthic organisms. Few studies describing the biogeographic responses of marine species to the LGM have been conducted in Patagonia, but existing data from coastal marine species have demonstrated marked genetic signatures of post-LGM recolonization and expansion. The kelp-dweller limpet Nacella mytilina is broadly distributed along the southern tip of South America and at the Falkland/Malvinas Islands. Considering its distribution, abundance, and narrow bathymetry, N. mytilina represents an appropriate model to infer how historical and contemporary processes affected the distribution of intraspecific genetic diversity and structure along the southern tip of South America. At the same time, it will be possible to determine how life history traits and the ecology of the species are responsible for the current pattern of gene flow and connectivity across the study area. We conducted phylogeographic and demographic inference analyses in N. mytilina from 12 localities along Pacific Patagonia (PP) and one population from the Falkland/Malvinas Islands (FI). Analyses of the mitochondrial gene COI in 300 individuals of N. mytilina revealed low levels of genetic polymorphism and the absence of genetic differentiation along PP. In contrast, FI showed a strong and significant differentiation from Pacific Patagonian populations. Higher levels of genetic diversity were also recorded in the FI population, together with a more expanded genealogy supporting the hypothesis of glacial persistence of the species in these islands. Haplotype genealogy, and mismatch analyses in the FI population recognized an older and more complex demographic history than in PP. Demographic reconstructions along PP suggest a post-LGM expansion process (7.5 ka), also supported by neutrality tests, mismatch distribution and maximum parsimony haplotype genealogies. Migration rate estimations showed evidence of asymmetrical gene flow from PP to FI. The absence of genetic differentiation, the presence of a single dominant haplotype, high estimated migration rates, and marked signal of recent demographic growth, support the hypothesis of rapid post-glacial expansion in N. mytilina along PP. This expansion could have been sustained by larval and rafting-mediated dispersal of adults from northernmost populations following the Cape Horn Current System. Marked genetic differentiation between PP and FI could be explained through differences in their respective glacial histories. During the LGM, Pacific Patagonia (PP) was almost fully covered by the Patagonian Ice Sheet, while sheet coverage in the FI ice was restricted to small cirques and valleys. As previously recorded in the sister-species N. magellanica, the FI rather than represent a classical glacial refugium for N. mytilina, seems to represent a sink area and/or a secondary contact zone. Accordingly, historical and contemporary processes, contrasting glacial histories between the analyzed sectors, as well as life history traits constitute the main factors explaining the current biogeographical patterns of most shallow Patagonian marine benthic organisms.

Does natural selection explain the fine scale genetic structure at the nuclear exon Glu-5' in blue mussels from Kerguelen?

The Kerguelen archipelago, isolated in the Southern Ocean, shelters a blue mussel Mytilus metapopulation far from any influence of continental populations or any known hybrid zone. The finely carved coast leads to a highly heterogeneous habitat. We investigated the impact of the environment on the genetic structure in those Kerguelen blue mussels by relating allele frequencies to habitat descriptors. A total sample comprising up to 2248 individuals from 35 locations was characterized using two nuclear markers, mac-1 and Glu-5', and a mitochondrial marker (COI). The frequency data from 9 allozyme loci in 9 of these locations were also reanalyzed. Two other nuclear markers (EFbis and EFprem's) were monomorphic. Compared to Northern Hemisphere populations, polymorphism in Kerguelen blue mussels was lower for all markers except for the exon Glu-5'. At Glu-5', genetic differences were observed between samples from distinct regions (F CT = 0.077), as well as within two regions, including between samples separated by <500 m. No significant differentiation was observed in the AMOVA analyses at the two other markers (mac-1 and COI). Like mac-1, all allozyme loci genotyped in a previous publication, displayed lower differentiation (Jost's D) and F ST values than Glu-5'. Power simulations and confidence intervals support that Glu-5' displays significantly higher differentiation than the other loci (except a single allozyme for which confidence intervals overlap). AMOVA analyses revealed significant effects of the giant kelp Macrocystis and wave exposure on this marker. We discuss the influence of hydrological conditions on the genetic differentiation among regions. In marine organisms with high fecundity and high dispersal potential, gene flow tends to erase differentiation, but this study showed significant differentiation at very small distance. This may be explained by the particular hydrology and the carved coastline of the Kerguelen archipelago, together with spatially variable selection at Glu-5'.

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

BACKGROUND: Understanding the limits and population dynamics of closely related sibling species in the marine realm is particularly relevant in organisms that require management. The crown-of-thorns starfish Acanthaster planci, recently shown to be a species complex of at least four closely related species, is a coral predator infamous for its outbreaks that have devastated reefs throughout much of its Indo-Pacific distribution. METHODOLOGY/PRINCIPAL FINDINGS: In this first Indian Ocean-wide genetic study of a marine organism we investigated the genetic structure and inferred the paleohistory of the two Indian Ocean sister-species of Acanthaster planci using mitochondrial DNA sequence analyses. We suggest that the first of two main diversification events led to the formation of a Southern and Northern Indian Ocean sister-species in the late Pliocene-early Pleistocene. The second led to the formation of two internal clades within each species around the onset of the last interglacial. The subsequent demographic history of the two lineages strongly differed, the Southern Indian Ocean sister-species showing a signature of recent population expansion and hardly any regional structure, whereas the Northern Indian Ocean sister-species apparently maintained a constant size with highly differentiated regional groupings that were asymmetrically connected by gene flow. CONCLUSIONS/SIGNIFICANCE: Past and present surface circulation patterns in conjunction with ocean primary productivity were identified as the processes most likely to have shaped the genetic structure between and within the two Indian Ocean lineages. This knowledge will help to understand the biological or ecological differences of the two sibling species and therefore aid in developing strategies to manage population outbreaks of this coral predator in the Indian Ocean.

Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis.

Population outbreaks of the coral-eating starfish, Acanthaster planci, are hypothesized to spread to many localities in the Indo-Pacific Ocean through dispersal of planktonic larvae. To elucidate the gene flow of A. planci across the Indo-Pacific in relation to ocean currents and to test the larval dispersal hypothesis, the genetic structure among 23 samples over the Indo-Pacific was analysed using seven highly polymorphic microsatellite loci. The F-statistics and genetic admixture analysis detected genetically distinct groups in accordance with ocean current systems, that is, the Southeast African group (Kenya and Mayotte), the Northwestern Pacific group (the Philippines and Japan), Palau, the North Central Pacific group (Majuro and Pohnpei), the Great Barrier Reef, Fiji, and French Polynesia, with a large genetic break between the Indian and Pacific Oceans. A pattern of significant isolation by distance was observed among all samples (P = 0.001, r = 0.88, n = 253, Mantel test), indicating restricted gene flow among the samples in accordance with geographical distances. The data also indicated strong gene flow within the Southeast African, Northwestern Pacific, and Great Barrier Reef groups. These results suggest that the western boundary currents have strong influence on gene flow of this species and may trigger secondary outbreaks.

Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from Northern and Southern Hemispheres and strong genetic differentiation among southern populations.

Smooth-shelled mussels, Mytilus spp., have an antitropical distribution. In the Northern Hemisphere, the M. edulis complex of species is composed of three genetically well delineated taxa: M. edulis, M. galloprovincialis and M. trossulus. In the Southern Hemisphere, morphological characters, allozymes and intron length polymorphisms suggest that Mytilus spp. populations from South America and Kerguelen Islands are related to M. edulis and those from Australasia to M. galloprovincialis. On the other hand, a phylogeny of the 16S rDNA mitochondrial locus demonstrates a clear distinctiveness of southern mussels and suggests that they are related to Mediterranean M. galloprovincialis. Here, we analysed the faster-evolving cytochrome oxidase subunit I locus. The divergence between haplotypes of populations from the two hemispheres was confirmed and was found to predate the divergence between haplotypes of northern M. edulis and M. galloprovincialis. In addition, strong genetic structure was detected among the southern samples, revealing three genetic entities that correspond to (1) South America and Kerguelen Island, (2) Tasmania, (3) New Zealand. Using the trans-Arctic interchange as a molecular clock calibration, we estimated the time since divergence of populations from the two hemispheres to be between 0.5 million years (MY) and 1.3 MY (average 0.84 MY). The contrasting patterns observed for the nuclear and the organelle genomes suggested two alternative, complex scenarios: two trans-equatorial migrations and the existence of differential barriers to mitochondrial and nuclear gene flow, or a single trans-equatorial migration and a view of the composition of the nuclear genome biased by taxonomic preconception.

Assessment of three mitochondrial loci variability for the crown-of-thorns starfish: a first insight into Acanthaster phylogeography.

Acanthaster planci (L.) is one of the major threats to coral reefs, whose genetic diversity has been mainly studied with allozymes. Allozymes revealed the low genetic differentiation between A. planci populations in the Indo-Pacific area. We obtained sequences of A. planci from Kenya, Mayotte and Madagascar at the three loci cytochrome oxydase subunit I (COI), 16S rDNA (16S) and five tRNAs, analysed together with available sequences of Acanthaster from the Pacific Ocean. The level of genetic diversity varied among the three loci, tRNAs being on average three times less divergent than COI and 16S genes. The genus Acanthaster appeared monophyletic, the two species A. brevispinus (Fisher) and A. planci forming distinct clades in agreement with data from morphology and systematics. The A. planci clade split into a West Indian Ocean group and a Pacific group, in agreement with allozyme data on population differentiation.