Morphology and diet are decoupled in nearshore notothenoids from King George Island, West Antarctica.

Antarctic notothenioid fishes show wide adaptive morphological radiation, linked to habitat preferences and food composition. However, direct comparisons of phenotypic variability and feeding habits are still lacking, particularly in stages inhabiting nearshore areas. To assess these relationships, we collected juveniles and adults of the most common benthic species inhabiting shallow waters off the South Shetland Islands within a similar size range, the plunderfish Harpagifer antarcticus, the black rockcod Notothenia coriiceps, and the marbled rockcod Notothenia rossii. Individual size ranges varied from 44.0 to 98.9 mm standard length (LS) (H. antarcticus), from 95.8 to 109.3 mm LS (N. coriiceps), and from 63.0 to 113.0 mm LS (N. rossii). Notothenioid fish showed different morphospace variability, being larger for H. antarcticus than the other Notothenia species and associated with the position of the posterior end of the operculum, along with the location and relative size of the eye. The evolutionary allometry was low, but the static allometry was much higher, especially for H. antarcticus and N. rossii. The diet was mainly carnivorous, consisting of amphipods and euphausiids. Macroalgae were scarce or totally absent in the gut contents of all species. Only H. antarcticus showed an increase in the prey number and ingested prey volume with fish size. Finally, there was a significant covariation between shape changes and LS in all species (allometric effects), however, not with prey composition, probably due to the small size range or ontogenetic stage and the relative similarity (or lack of contrast) in the benthic environment that they utilized.

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish.

White-blooded Antarctic icefishes, a family within the adaptive radiation of Antarctic notothenioid fishes, are an example of extreme biological specialization to both the chronic cold of the Southern Ocean and life without hemoglobin. As a result, icefishes display derived physiology that limits them to the cold and highly oxygenated Antarctic waters. Against these constraints, remarkably one species, the pike icefish Champsocephalus esox, successfully colonized temperate South American waters. To study the genetic mechanisms underlying secondarily temperate adaptation in icefishes, we generated chromosome-level genome assemblies of both C. esox and its Antarctic sister species, Champsocephalus gunnari. The C. esox genome is similar in structure and organization to that of its Antarctic congener; however, we observe evidence of chromosomal rearrangements coinciding with regions of elevated genetic divergence in pike icefish populations. We also find several key biological pathways under selection, including genes related to mitochondria and vision, highlighting candidates behind temperate adaptation in C. esox. Substantial antifreeze glycoprotein (AFGP) pseudogenization has occurred in the pike icefish, likely due to relaxed selection following ancestral escape from Antarctica. The canonical AFGP locus organization is conserved in C. esox and C. gunnari, but both show a translocation of two AFGP copies to a separate locus, previously unobserved in cryonotothenioids. Altogether, the study of this secondarily temperate species provides an insight into the mechanisms underlying adaptation to ecologically disparate environments in this otherwise highly specialized group.

Patterns and drivers of benthic macroinvertebrate assemblages in the kelp forests of southern Patagonia.

The kelp forests of southern Patagonia have a large diversity of habitats, with remote islands, archipelagos, peninsulas, gulfs, channels, and fjords, which are comprised of a mixture of species with temperate and sub-Antarctic distributions, creating a unique ecosystem that is among the least impacted on Earth. We investigated the distribution, diversity, and abundance of marine macroinvertebrate assemblages from the kelp forests of southern Patagonia over a large spatial scale and examined the environmental drivers contributing to the observed patterns in assemblage composition. We analyzed data from 120 quantitative underwater transects (25 x 2 m) conducted within kelp forests in the southern Patagonian fjords in the Kawésqar National Reserve (KNR), the remote Cape Horn (CH) and Diego Ramírez (DR) archipelagos of southern Chile, and the Mitre Peninsula (MP) and Isla de los Estados (IE) in the southern tip of Argentina. We observed rich assemblages of macroinvertebrates among these kelp forests, with a total of 185 unique taxa from 10 phyla and 23 classes/infraorders across the five regions. The number of taxa per transect was highest at IE, followed by MP, CH, and KNR, with the lowest number recorded at DR. The trophic structure of the macroinvertebrate assemblages was explained mostly by wave exposure (28% of the variation), followed by salinity (12%) and the KNR region (11%). KNR was most distinct from the other regions with a greater abundance of deposit feeders, likely driven by low salinity along with high turbidity and nutrients from terrigenous sources and glacial melt. Our study provides the first broad-scale description of the benthic assemblages associated with kelp forests in this vast and little-studied region and helps to establish baselines for an area that is currently lightly influenced by local anthropogenic factors and less impacted by climate change compared with other kelp forests globally.

Unraveling the morphological patterns of a subantarctic eelpout: a geometric morphometric approach.

Phenotypic variation in organisms depends on the genotype and the environmental constraints of the habitat that they exploit. Therefore, for marine species inhabiting contrasting aquatic conditions, it is expected to find covariation between the shape and its spatial distribution. We studied the morphology of the head and cephalic sensory canals of the eelpout Austrolycus depressiceps (4.5-22.5 cm TL) across its latitudinal distribution in South Pacific (45°S-55°S). Geometric morphometric analyses show that the shape varied from individuals with larger snout and an extended suborbital canal to individuals with shorter snouts and frontally compressed suborbital canal. There was size variation across the sampled populations, but that size does not have a clear latitudinal gradient. Only 8% of the shape variation relates to this size variation (allometry), represented by a decrease in the relative size of the eye, and a depression of the posterior margin of the head. There were spatial differences in the shape of the head, but these differences were probably caused by allometric effects. Additionally, 2 of the canals of the cephalic lateralis pores and the head shape showed modularity in its development. This study shows that the morphology of marine fish with a shallow distribution varies across distances of hundreds of kilometers (i.e., phenotypic modulation).

Assemblage structure and spatial diversity patterns of kelp forest-associated fishes in Southern Patagonia.

Knowledge of the ecology of the fish fauna associated with kelp (primarily Macrocystis pyrifera) forests in Southern Patagonia is scarce, especially in how abiotic and biotic variables influence their structure, diversity, and distribution. This information is important for the management and conservation of this unique ecosystem, which has minimal anthropogenic impacts at present. We analyzed data from 122 quantitative underwater transects conducted within kelp forests at 61 stations from Chile's southern Patagonian fjords to the Cape Horn and Diego Ramirez archipelagos and the southern tip of Argentina, including the Mitre Peninsula and Isla de los Estados. In total, 25 fish species belonging to 13 families were observed. Multivariate analysis indicated that there are significant differences in fish assemblage structure among locations and wave exposures, which was driven primarily by Patagonotothen sima and Paranotothenia magellanica, which occurred on exposed and semi-exposed stations. P. cornucola was mainly distributed across sheltered stations of the Kawésqar National Park. Temperature, salinity, depth, and kelp density influenced fish assemblage structure, with the highest diversity in areas with the lowest temperature and greater depth at Isla de los Estados. In contrast, species richness, diversity, abundance, and biomass were all lower in areas with high density of the understory kelp Lessonia spp., which might be driven by the absence of P. tessellata, P. squamiceps and P. cornucola, the most important species in terms of occurrence, abundance, and biomass. Our study provides the first broad-scale description of the fish assemblages associated with kelp forests along the southern cone of South America based on non-invasive visual transects, improving our knowledge of the distribution of fish assemblages across several environmental conditions in this vast and little-studied area.

Marine communities of the newly created Kawésqar National Reserve, Chile: From glaciers to the Pacific Ocean.

The newly created Kawésqar National Park (KNP) and National Reserve (KNR) in southern Chile consists of diverse terrestrial and marine habitats, which includes the southern terminus of the Andes, the Southern Patagonia Ice Fields, sub-Antarctic rainforests, glaciers, fjords, lakes, wetlands, valleys, channels, and islands. The marine environment is influenced by wide ranging hydrological factors such as glacier melt, large terrigenous inputs, high precipitation, strong currents, and open ocean water masses. Owing to the remoteness, rugged terrain, and harsh environmental conditions, little is known about this vast region, particularly the marine realm. To this end, we conducted an integrated ecological assessment using SCUBA and remote cameras down to 600 m to examine this unique and largely unexplored ecosystem. Kelp forests (primarily Macrocystis pyrifera) dominate the nearshore ecosystem and provide habitat for myriad benthic organisms. In the fjords, salinity was low and both turbidity and nutrients from terrigenous sources were high, with benthic communities dominated by active suspension feeders (e.g., Bivalvia, Ascidiacea, and Bryozoa). Areas closer to the Pacific Ocean showed more oceanic conditions with higher salinity and lower turbidity, with benthic communities experiencing more open benthic physical space in which predators (e.g., Malacostraca and Asteroidea) and herbivorous browsers (e.g., Echinoidea and Gastropoda) were more conspicuous components of the community compared to the inner fjords. Hagfish (Myxine sp.) was the most abundant and frequently occurring fish taxa observed on deep-sea cameras (80% of deployments), along with several taxa of sharks (e.g., Squaliformes, Etmopteridae, Somniosidae, Scyliorhinidae), which collectively were also observed on 80% of deep-sea camera deployments. The kelp forests, deep fjords, and other nearshore habitats of the KNR represent a unique ecosystem with minimal human impacts at present. The KNR is part of the ancestral territory of the indigenous Kawésqar people and their traditional knowledge, including the importance of the land-sea connection in structuring the marine communities of this region, is strongly supported by our scientific findings.

Spatial patterns of continental shelf faunal community structure along the Western Antarctic Peninsula.

Knowledge of continental shelf faunal biodiversity of Antarctica is patchy and as such, the ecology of this unique ecosystem is not fully understood. To this end, we deployed baited cameras at 20 locations along ~ 500 km of the Western Antarctic Peninsula (WAP) at depths from 90 to 797 m. We identified 111 unique taxa, with mud bottom accounting for 90% of the dominant (≥ 50% cover) habitat sampled. Amphipoda comprised 41% of the total maximum number of individuals per camera deployment (MaxN) and occurred on 75% of deployments. Excluding this taxon, the highest MaxN occurred around King George/25 de Mayo Island and was driven primarily by the abundance of krill (Euphausiidae), which accounted for 36% of total average MaxN among deployments around this island. In comparison, krill comprised 22% of total average MaxN at Deception Island and only 10% along the peninsula. Taxa richness, diversity, and evenness all increased with depth and depth explained 18.2% of the variation in community structure among locations, which may be explained by decreasing ice scour with depth. We identified a number of Vulnerable Marine Ecosystem taxa, including habitat-forming species of cold-water corals and sponge fields. Channichthyidae was the most common fish family, occurring on 80% of all deployments. The Antarctic jonasfish (Notolepis coatsorum) was the most frequently encountered fish taxa, occurring on 70% of all deployments and comprising 25% of total MaxN among all deployments. Nototheniidae was the most numerically abundant fish family, accounting for 36% of total MaxN and was present on 70% of the deployments. The WAP is among the fastest warming regions on Earth and mitigating the impacts of warming, along with more direct impacts such as those from fishing, is critical in providing opportunities for species to adapt to environmental change and to preserve this unique ecosystem.

Kelp forests at the end of the earth: 45 years later.

The kelp forests of southern South America are some of the least disturbed on the planet. The remoteness of this region has, until recently, spared it from many of the direct anthropogenic stressors that have negatively affected these ecosystems elsewhere. Re-surveys of 11 locations at the easternmost extent of Tierra del Fuego originally conducted in 1973 showed no significant differences in the densities of adult and juvenile Macrocystis pyrifera kelp or kelp holdfast diameter between the two survey periods. Additionally, sea urchin assemblage structure at the same sites were not significantly different between the two time periods, with the dominant species Loxechinus albus accounting for 66.3% of total sea urchin abundance in 2018 and 61.1% in 1973. Time series of Landsat imagery of the region from 1998 to 2018 showed no long-term trends in kelp canopy over the past 20 years. However, ~ 4-year oscillations in canopy fraction were observed and were strongly and negatively correlated with the NOAA Multivariate ENSO index and sea surface temperature. More extensive surveying in 2018 showed significant differences in benthic community structure between exposed and sheltered locations. Fish species endemic to the Magellanic Province accounted for 73% of all nearshore species observed and from 98-100% of the numerical abundance enumerated at sites. Fish assemblage structure varied significantly among locations and wave exposures. The recent creation of the Yaganes Marine Park is an important step in protecting this unique and biologically rich region; however, the nearshore waters of the region are currently not included in this protection. There is a general lack of information on changes in kelp forests over long time periods, making a global assessment difficult. A complete picture of how these ecosystems are responding to human pressures must also include remote locations and locations with little to no impact.

The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonian robalo genomes.

BACKGROUND: The Southern Ocean is the coldest ocean on Earth but a hot spot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation, forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and the rapid expansion of the Antarctic notothenioids remain poorly understood. RESULTS: We sequenced and compared 2 notothenioid genomes-the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo Eleginops maclovinus, representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis, and freeze resistance. Besides antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys-transfer RNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to the achievement of neutral buoyancy and pelagicism. CONCLUSIONS: Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

Marine biodiversity at the end of the world: Cape Horn and Diego Ramírez islands.

The vast and complex coast of the Magellan Region of extreme southern Chile possesses a diversity of habitats including fjords, deep channels, and extensive kelp forests, with a unique mix of temperate and sub-Antarctic species. The Cape Horn and Diego Ramírez archipelagos are the most southerly locations in the Americas, with the southernmost kelp forests, and some of the least explored places on earth. The giant kelp Macrocystis pyrifera plays a key role in structuring the ecological communities of the entire region, with the large brown seaweed Lessonia spp. forming dense understories. Kelp densities were highest around Cape Horn, followed by Diego Ramírez, and lowest within the fjord region of Francisco Coloane Marine Park (mean canopy densities of 2.51 kg m-2, 2.29 kg m-2, and 2.14 kg m-2, respectively). There were clear differences in marine communities among these sub-regions, with the lowest diversity in the fjords. We observed 18 species of nearshore fishes, with average species richness nearly 50% higher at Diego Ramírez compared with Cape Horn and Francisco Coloane. The number of individual fishes was nearly 10 times higher at Diego Ramírez and 4 times higher at Cape Horn compared with the fjords. Dropcam surveys of mesophotic depths (53-105 m) identified 30 taxa from 25 families, 15 classes, and 7 phyla. While much of these deeper habitats consisted of soft sediment and cobble, in rocky habitats, echinoderms, mollusks, bryozoans, and sponges were common. The southern hagfish (Myxine australis) was the most frequently encountered of the deep-sea fishes (50% of deployments), and while the Fueguian sprat (Sprattus fuegensis) was the most abundant fish species, its distribution was patchy. The Cape Horn and Diego Ramírez archipelagos represent some of the last intact sub-Antarctic ecosystems remaining and a recently declared large protected area will help ensure the health of this unique region.

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.

Contrasting Genetic Structure and Diversity of Galaxias maculatus (Jenyns, 1848) Along the Chilean Coast: Stock Identification for Fishery Management.

Galaxias maculatus (Pisces: Galaxiidae) commonly known as "puye" has a disjunct distribution along the Southern Hemisphere including landlocked and migratory populations at latitudes over 30°S in South America, Australia, Tasmania, and New Zealand. Chilean artisanal fishery of G. maculatus has become less important as a resource due to multiple factors including overexploitation, pollution, introduction of predators, and competitors. At the same time, the current conservation status of the species in Chile is still uncertain. Here, we used mtDNA control region sequences (925bp) to investigate main patterns of genetic diversity and structure in populations from 2 biogeographic areas along the Chilean coast. Extremely high levels of genetic diversity characterize the species, suggesting a low amount of influence of the last glacial cycle over its demography compared with other studies in freshwater and marine South American fishes. However, we recognized contrasting genetic patterns between the Intermediate Area (between 30°S and 42°S) and the Magellanic Province (between 42°S and 56°S). On the one hand, over a narrow geographical range (<200 km) each Intermediate Area estuarine population constitutes a different genetic unit. On the other hand, the Magellanic populations of the species exhibited low levels of differentiation in an area extending for more than 500 km. Such differences may be a consequence of different coastal configurations, oceanographic regimes, and Quaternary glacial histories. Finally, our results support the existence of different stock units for G. maculatus and this information should be integrated in future management strategies and aquaculture programs for this species.

Phylogeography in Galaxias maculatus (Jenyns, 1848) along Two Biogeographical Provinces in the Chilean Coast.

Major geologic and climatic changes during the Quaternary exerted a major role in shaping past and contemporary distribution of genetic diversity and structure of aquatic organisms in southern South America. In fact, the northern glacial limit along the Pacific coast, an area of major environmental changes in terms of topography, currents, and water salinity, represents a major biogeographic transition for marine and freshwater species. We used mitochondrial DNA sequences (D-loop) to investigate the consequences of Quaternary glacial cycles over the pattern of genetic diversity and structure of G. maculatus (Pisces: Galaxiidae) along two biogeographical provinces in the Chilean coast. Extreme levels of genetic diversity and strong phylogeographic structure characterize the species suggesting a low amount of influence of the last glacial cycle over its demography. However, we recognized contrasting patterns of genetic diversity and structure between main biogeographical areas here analyzed. Along the Intermediate Area (38°-41° S) each estuarine population constitutes a different unit. In contrast, Magellanic populations (43°-53° S) exhibited low levels of genetic differentiation. Contrasting patterns of genetic diversity and structure recorded in the species between the analyzed biogeographic areas are consistent with the marked differences in abiotic factors (i.e., different coastal configurations, Quaternary glacial histories, and oceanographic regimes) and to inherent characteristics of the species (i.e., salt-tolerance, physiology, and reproductive behavior).

Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: lessons from the limpet Nacella magellanica (Gmelin, 1791).

BACKGROUND: Patagonia extends for more than 84,000 km of irregular coasts is an area especially apt to evaluate how historic and contemporary processes influence the distribution and connectivity of shallow marine benthic organisms. The true limpet Nacella magellanica has a wide distribution in this province and represents a suitable model to infer the Quaternary glacial legacy on marine benthic organisms. This species inhabits ice-free rocky ecosystems, has a narrow bathymetric range and consequently should have been severely affected by recurrent glacial cycles during the Quaternary. We performed phylogeographic and demographic analyses of N. magellanica from 14 localities along its distribution in Pacific Patagonia, Atlantic Patagonia, and the Falkland/Malvinas Islands. RESULTS: Mitochondrial (COI) DNA analyses of 357 individuals of N. magellanica revealed an absence of genetic differentiation in the species with a single genetic unit along Pacific Patagonia. However, we detected significant genetic differences among three main groups named Pacific Patagonia, Atlantic Patagonia and Falkland/Malvinas Islands. Migration rate estimations indicated asymmetrical gene flow, primarily from Pacific Patagonia to Atlantic Patagonia (Nem=2.21) and the Falkland/Malvinas Islands (Nem=16.6). Demographic reconstruction in Pacific Patagonia suggests a recent recolonization process (< 10 ka) supported by neutrality tests, mismatch distribution and the median-joining haplotype genealogy. CONCLUSIONS: Absence of genetic structure, a single dominant haplotype, lack of correlation between geographic and genetic distance, high estimated migration rates and the signal of recent demographic growth represent a large body of evidence supporting the hypothesis of rapid postglacial expansion in this species in Pacific Patagonia. This expansion could have been sustained by larval dispersal following the main current system in this area. Lower levels of genetic diversity in inland sea areas suggest that fjords and channels represent the areas most recently colonized by the species. Hence recolonization seems to follow a west to east direction to areas that were progressively deglaciated. Significant genetic differences among Pacific, Atlantic and Falkland/Malvinas Islands populations may be also explained through disparities in their respective glaciological and geological histories. The Falkland/Malvinas Islands, more than representing a glacial refugium for the species, seems to constitute a sink area considering the strong asymmetric gene flow detected from Pacific to Atlantic sectors. These results suggest that historical and contemporary processes represent the main factors shaping the modern biogeography of most shallow marine benthic invertebrates inhabiting the Patagonian Province.