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Blubber is a hydrostatic pressure-resistant and insulating vascularized layer of subcutaneous adipose tissue beneath the skin found in cetaceans, pinnipeds, and sirenians. Little is known about the molecular genetics of blubber formation, and it is unclear when the blubber observed today began to develop during the evolution of the marine mammal groups. Here we screen for genes lost in cetaceans and find that ADRB3 (β 3 -adrenergic receptor), a gene essential for adipose tissue lipolysis and thermogenesis, acquired inactivating mutations in crown cetaceans 20 million years after its downstream effector uncoupling protein 1 ( UCP1 ) gained partial loss-of-function mutations in semi-aquatic stem cetaceans. Both in vivo and in vitro experiments indicate that cetacean ADRB3 is not functional, suggesting that crown cetaceans abolished cold-induced non-shivering thermogenesis to favor lipid storage for thermal insulation. Our study supports that cetacean blubber evolved stepwise along their transition to an aquatic environment and implies that ADRB3 loss was critical for the radiation and dispersal of toothed and baleen whales. Blubber is a key adaptation of modern cetaceans, but its molecular evolution remains incompletely understood. Here, Tian and colleagues identify loss of the master adipose tissue regulator β3-adrenergic receptor in crown cetaceans, possibly providing a means for later radiation and dispersal.

Cetaceans (whales, dolphins, and porpoises) are a group of mammals adapted to various aquatic habitats, from oceans to freshwater rivers. We report the sequencing, de novo assembly and analysis of a finless porpoise genome, and the re-sequencing of an additional 48 finless porpoise individuals. We use these data to reconstruct the demographic history of finless porpoises from their origin to the occupation into the Yangtze River. Analyses of selection between marine and freshwater porpoises identify genes associated with renal water homeostasis and urea cycle, such as urea transporter 2 and angiotensin I-converting enzyme 2, which are likely adaptations associated with the difference in osmotic stress between ocean and rivers. Our results strongly suggest that the critically endangered Yangtze finless porpoises are reproductively isolated from other porpoise populations and harbor unique genetic adaptations, supporting that they should be considered a unique incipient species. Whales, dolphins and porpoises are adapted to various aquatic habitats. Here, Zhou et al. show that polymorphisms associated with renal function and the urea cycle have undergone selection in the freshwater Yangtze finless porpoise and provide genomic evidence of incipient speciation.

Background The Antarctic krill ( Euphausia superba ) is a keystone species in the Southern Ocean ecosystem, influencing food web dynamics and ecosystem functionality. Despite its ecological importance, further exploration is essential to understand their population dynamics. Results In this study, we present the complete mitogenome of the Antarctic krill. The assembly is 18,926 bp, including a notably large 3,952 bp control region (CR). The CR features a satellite repeat spanning 2,289 bp, showcasing the effectiveness of long-read sequencing in resolving complex genomic regions. Additionally, we identified 900 nuclear-mitochondrial segments (NUMTs) totaling 2.79 Mb, shedding light on the dynamic integration of mitochondrial DNA (mtDNA) into the nuclear genomes. By establishing a dataset comprising 80 krill mitogenomes, we unveil substantial mitochondrial diversity, particularly within the ND4 gene. While our analysis reveals no significant differentiation among four geographically distinct groups, we identify at least four maternal genetic clusters. Haplotype network analysis and demographic reconstructions suggest a recent population expansion, likely driven by favorable environmental conditions during the late Pleistocene. Furthermore, our investigation into selection pressures on mitochondrial genes reveals evidence of purifying selection across all 13 protein-coding genes, underscoring the pivotal role of mtDNA conservation in maintaining mitochondrial function under extreme environments. Conclusions This study provides a repository of Antarctic krill mitogenomes and insights into the population genetics and evolutionary history of this ecologically important species from a mitogenomic perspective, with implications for krill conservation and management in the Southern Ocean.

Sirenians of the superorder Afrotheria were the first mammals to transition from land to water and are the only herbivorous marine mammals. Here, we generated a chromosome-level dugong ( Dugong dugon ) genome. A comparison of our assembly with other afrotherian genomes reveals possible molecular adaptations to aquatic life by sirenians, including a shift in daily activity patterns (circadian clock) and tolerance to a high-iodine plant diet mediated through changes in the iodide transporter NIS ( SLC5A5 ) and its co-transporters. Functional in vitro assays confirm that sirenian amino acid substitutions alter the properties of the circadian clock protein PER2 and NIS. Sirenians show evidence of convergent regression of integumentary system (skin and its appendages) genes with cetaceans. Our analysis also uncovers gene losses that may be maladaptive in a modern environment, including a candidate gene ( KCNK18 ) for sirenian cold stress syndrome likely lost during their evolutionary shift in daily activity patterns. Genomes from nine Australian locations and the functionally extinct Okinawan population confirm and date a genetic break ~10.7 thousand years ago on the Australian east coast and provide evidence of an associated ecotype, and highlight the need for whole-genome resequencing data from dugong populations worldwide for conservation and genetic management. Sirenians are aquatic mammals that originated in Africa ~60 million years ago. Using comparative genomics of a new dugong genome, this study finds genetic adaptations shared by extant sirenians and assessed the diversity of dugongs in Australian waters and the functionally extinct Okinawan dugong.

Elucidating cellular architecture and cell-type evolution across species is central to understanding immune system function and susceptibility to disease. Adaptive immunity is a shared trait of the common ancestor of cartilaginous and bony fishes. However, evolutionary features of lymphocytes in these two jawed vertebrates remain unclear. Here, we present a single-cell RNA sequencing atlas of immune cells from cartilaginous (white-spotted bamboo shark) and bony (zebrafish and Chinese tongue sole) fishes. Cross-species comparisons show that the same cell types across different species exhibit similar transcriptional profiles. In the bamboo shark, we identify a phagocytic B cell population expressing several pattern recognition receptors, as well as a T cell sub-cluster co-expressing both T and B cell markers. In contrast to a division by function in the bony fishes, we show close linkage and poor functional specialization among lymphocytes in the cartilaginous fish. Our cross-species single-cell comparison presents a resource for uncovering the origin and evolution of the gnathostome immune system. Both cartilaginous and bony fishes have adaptive immune cells, but the evolutionary features of these diverse cell populations remain understudied. Here the authors report single-cell RNA sequencing atlas of both species to define these features and to find reduced evolutionary diversification of immune cells in cartilaginous fishes.

Cetaceans are a group of marine mammals whose ancestors were adaptated for life on land. Life in an aquatic environment poses many challenges for air-breathing mammals. Diving marine mammals have adapted to rapid reoxygenation and reactive oxygen species (ROS)-mediated reperfusion injury. Here, we considered the evolution of the glutathione transferase (GST) gene family which has important roles in the detoxification of endogenously-derived ROS and environmental pollutants. We characterized the cytosolic GST gene family in 21 mammalian species; cetaceans, sirenians, pinnipeds, and their terrestrial relatives. All seven GST classes were identified, showing that GSTs are ubiquitous in mammals. Some GST genes are the product of lineage-specific duplications and losses, in line with a birth-and-death evolutionary model. We detected sites with signatures of positive selection that possibly influence GST structure and function, suggesting that adaptive evolution of GST genes is important for defending mammals from various types of noxious environmental compounds. We also found evidence for loss of alpha and mu GST subclass genes in cetacean lineages. Notably, cetaceans have retained a homolog of at least one of the genes GSTA1, GSTA4, and GSTM1; GSTs that are present in both the cytosol and mitochondria. The observed variation in number and selection pressure on GST genes suggest that the gene family structure is dynamic within cetaceans.

Background Lindaspio polybranchiata , a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings. Results We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism’s ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments. Conclusions Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.

The six species of lungfish possess both lungs and gills and are the closest extant relatives of tetrapods. Here, we report a single-cell transcriptome atlas of the West African lungfish ( Protopterus annectens ). This species manifests the most extreme form of terrestrialization, a life history strategy to survive dry periods that can last for years, characterized by dormancy and reversible adaptive changes of the gills and lungs. Our atlas highlights the cell type diversity of the West African lungfish, including gene expression consistent with phenotype changes of terrestrialization. Comparison with terrestrial tetrapods and ray-finned fishes reveals broad homology between the swim bladder and lung cell types as well as shared and idiosyncratic changes of the external gills of the West African lungfish and the internal gills of Atlantic salmon. The single-cell atlas presented here provides a valuable resource for further exploration of the respiratory system evolution in vertebrates and the diversity of lungfish terrestrialization. The water-to-land transition of vertebrates is a landmark event in evolutionary history. This work utilizes single-cell RNA sequencing to explore the adaptations in African lungfish lungs and gills to terrestrialization.

Background Bivalves have independently evolved a variety of symbiotic relationships with chemosynthetic bacteria. These relationships range from endo- to extracellular interactions, making them ideal for studies on symbiosis-related evolution. It is still unclear whether there are universal patterns to symbiosis across bivalves. Here, we investigate the hologenome of an extracellular symbiotic thyasirid clam that represents the early stages of symbiosis evolution. Results We present a hologenome of Conchocele bisecta (Bivalvia: Thyasiridae) collected from deep-sea hydrothermal vents with extracellular symbionts, along with related ultrastructural evidence and expression data. Based on ultrastructural and sequencing evidence, only one dominant Thioglobaceae bacteria was densely aggregated in the large bacterial chambers of C. bisecta , and the bacterial genome shows nutritional complementarity and immune interactions with the host. Overall, gene family expansions may contribute to the symbiosis-related phenotypic variations in different bivalves. For instance, convergent expansions of gaseous substrate transport families in the endosymbiotic bivalves are absent in C. bisecta . Compared to endosymbiotic relatives, the thyasirid genome exhibits large-scale expansion in phagocytosis, which may facilitate symbiont digestion and account for extracellular symbiotic phenotypes. We also reveal that distinct immune system evolution, including expansion in lipopolysaccharide scavenging and contraction of IAP (inhibitor of apoptosis protein), may contribute to the different manners of bacterial virulence resistance in C. bisecta . Conclusions Thus, bivalves employ different pathways to adapt to the long-term co-existence with their bacterial symbionts, further highlighting the contribution of stochastic evolution to the independent gain of a symbiotic lifestyle in the lineage.

Background The transition from land to sea by the ancestor of cetaceans approximately 50 million years ago was an incredible evolutionary event that led to a series of morphological, physiological, and behavioral adaptations. During this transition, bone microstructure evolved from the typical terrestrial form to the specialized structure found in modern cetaceans. While the bone microstructure of mammals has been documented before, investigations of its genetic basis lag behind. The increasing number of cetaceans with whole-genome sequences available may shed light on the mechanism underlying bone microstructure evolution as a result of land to water transitions. Results Cetacean bone microstructure is consistent with their diverse ecological behaviors. Molecular evolution was assessed by correlating bone microstructure and gene substitution rates in terrestrial and aquatic species, and by detecting genes under positive selection along ancestral branches of cetaceans. We found that: 1) Genes involved in osteoclast function are under accelerated evolution in cetaceans, suggestive of important roles in bone remodeling during the adaptation to an aquatic environment; 2) Genes in the Wnt pathway critical for bone development and homeostasis show evidence of divergent evolution in cetaceans; 3) Several genes encoding bone collagens are under selective pressure in cetaceans. Conclusions Our results suggest that evolutionary pressures have shaped the bone microstructure of cetaceans, to facilitate life in diverse aquatic environments.