ABSTRACT
Cetaceans represent a natural experiment within the tree of life in which a lineage changed from terrestrial to aquatic habitats. This shift involved phenotypic modifications, representing an opportunity to explore the genetic bases of phenotypic diversity. Among the different molecular systems that maintain cellular homeostasis, ion channels are crucial for the proper physiological functioning of all living species. This study aims to explore the evolution of ion channels during the evolutionary history of cetaceans. To do so, we created a bioinformatic pipeline to annotate the repertoire of ion channels in the genome of the species included in our sampling. Our main results show that cetaceans have, on average, fewer protein-coding genes and a higher percentage of annotated ion channels than non-cetacean mammals. Signals of positive selection were detected in ion channels related to the heart, locomotion, visual and neurological phenotypes. Interestingly, we predict that the NaV1.5 ion channel of most toothed whales (odontocetes) is sensitive to tetrodotoxin, similar to NaV1.7, given the presence of tyrosine instead of cysteine, in a specific position of the ion channel. Finally, the gene turnover rate of the cetacean crown group is more than three times faster than that of non-cetacean mammals.
Subject(s)
Cetacea , Evolution, Molecular , Ion Channels , Animals , Cetacea/genetics , Cetacea/physiology , Ion Channels/genetics , Ion Channels/metabolism , Phylogeny , Computational Biology/methods , GenomeABSTRACT
BACKGROUND: Marine mammals, which have evolved independently into three distinct lineages, share common physiological features that contribute to their adaptation to the marine environment. OBJECTIVE: To identify positively selected genes (PSGs) for adaptation to the marine environment using available genomic data from three taxonomic orders: cetaceans, pinnipeds, and sirenians. METHODS: Based on the genomes within each group of Artiodactyla, Carnivora and Afrotheria, we performed selection analysis using the branch-site model in CODEML. RESULTS: Based on the branch-site model, 460, 614, and 359 PSGs were predicted for the cetaceans, pinnipeds, and sirenians, respectively. Functional enrichment analysis indicated that genes associated with hemostasis were positively selected across all lineages of marine mammals. We observed positive selection signals for the hemostasis and coagulation-related genes plasminogen activator, urokinase (PLAU), multimerin 1 (MMRN1), gamma-glutamyl carboxylase (GGCX), and platelet endothelial aggregation receptor 1 (PEAR1). Additionally, we found out that the sodium voltage-gated channel alpha subunit 9 (SCN9A), serine/arginine repetitive matrix 4 (SRRM4), and Ki-ras-induced actin-interacting protein (KRAP) are under positive selection pressure and are associated with cognition, neurite outgrowth, and IP3-mediated Ca2 + release, respectively. CONCLUSION: This study will contribute to our understanding of the adaptive evolution of marine mammals by providing information on a group of candidate genes that are predicted to influence adaptation to aquatic environments, as well as their functional characteristics.
Subject(s)
Adaptation, Physiological , Cetacea , Selection, Genetic , Animals , Adaptation, Physiological/genetics , Cetacea/genetics , Mammals/genetics , Aquatic Organisms/genetics , Phylogeny , Evolution, Molecular , Carnivora/genetics , Artiodactyla/genetics , Artiodactyla/physiology , Caniformia/geneticsABSTRACT
Cetaceans and pinnipeds are lineages of mammals that have independently returned to the aquatic environment, acquiring varying degrees of dependence on it while sharing adaptations for underwater living. Here, we focused on one critical adaptation from both groups, their ability to withstand the ischemia and reperfusion experienced during apnea diving, which can lead to the production of reactive oxygen species (ROS) and subsequent oxidative damage. Previous studies have shown that cetaceans and pinnipeds possess efficient antioxidant enzymes that protect against ROS. In this study, we investigated the molecular evolution of key antioxidant enzyme genes (CAT, GPX3, GSR, PRDX1, PRDX3, and SOD1) and the ROS-producing gene XDH, in cetaceans and pinnipeds lineages. We used the ratio of non-synonymous (dN) to synonymous (dS) substitutions as a measure to identify signatures of adaptive molecular evolution in these genes within and between the two lineages. Additionally, we performed protein modeling and variant impact analyzes to assess the functional consequences of observed mutations. Our findings revealed distinct selective regimes between aquatic and terrestrial mammals in five of the examined genes, including divergences within cetacean and pinniped lineages, between ancestral and recent lineages and between crowns groups. We identified specific sites under positive selection unique to Cetacea and Pinnipedia, with one site showing evidence of convergent evolution in species known for their long and deep-diving capacities. Notably, many sites under adaptive selection exhibited radical changes in amino acid properties, with some being damaging mutations in human variations, but with no apparent detrimental impacts on aquatic mammals. In conclusion, our study provides insights into the adaptive changes that have occurred in the antioxidant systems of aquatic mammals throughout their evolutionary history. We observed both distinctive features within each group of Cetacea and Pinnipedia and instances of convergence. These findings highlight the dynamic nature of the antioxidant system in response to challenges of the aquatic environment and provide a foundation for further investigations into the molecular mechanisms underlying these adaptations.
Subject(s)
Antioxidants , Caniformia , Cetacea , Evolution, Molecular , Animals , Cetacea/genetics , Cetacea/metabolism , Caniformia/genetics , Antioxidants/metabolism , Phylogeny , Adaptation, Physiological/genetics , Reactive Oxygen Species/metabolism , Selection, GeneticABSTRACT
BACKGROUND: Cetaceans, having experienced prolonged adaptation to aquatic environments, have undergone evolutionary changes in their respiratory systems. This process of evolution has resulted in the emergence of distinctive phenotypic traits, notably the abundance of elastic fibers and thickened alveolar walls in their lungs, which may facilitate alveolar collapse during diving. This structure helps selective exchange of oxygen and carbon dioxide, while minimizing nitrogen exchange, thereby reducing the risk of DCS. Nevertheless, the scientific inquiry into the mechanisms through which these unique phenotypic characteristics govern the diving behavior of marine mammals, including cetaceans, remains unresolved. RESULTS: This study entails an evolutionary analysis of 42 genes associated with pulmonary fibrosis across 45 mammalian species. Twenty-one genes in cetaceans exhibited accelerated evolution, featuring specific amino acid substitutions in 14 of them. Primarily linked to the development of the respiratory system and lung morphological construction, these genes play a crucial role. Moreover, among marine mammals, we identified eight genes undergoing positive selection, and the evolutionary rates of three genes significantly correlated with diving depth. Specifically, the SFTPC gene exhibited convergent amino acid substitutions. Through in vitro cellular experiments, we illustrated that convergent amino acid site mutations in SFTPC contribute positively to pulmonary fibrosis in marine mammals, and the presence of this phenotype can induce deep alveolar collapse during diving, thereby reducing the risk of DCS during diving. CONCLUSIONS: The study unveils pivotal genetic signals in cetaceans and other marine mammals, arising through evolution. These genetic signals may influence lung characteristics in marine mammals and have been linked to a reduced risk of developing DCS. Moreover, the research serves as a valuable reference for delving deeper into human diving physiology.
Subject(s)
Pulmonary Fibrosis , Animals , Humans , Cetacea/genetics , Cetacea/metabolism , Lung/metabolism , Mammals/metabolism , Oxygen/metabolismABSTRACT
The major histocompatibility complex (MHC) is a highly polymorphic gene family that is crucial in immunity, and its diversity can be effectively used as a fitness marker for populations. Despite this, MHC remains poorly characterised in non-model species (e.g., cetaceans: whales, dolphins and porpoises) as high gene copy number variation, especially in the fast-evolving class I region, makes analyses of genomic sequences difficult. To date, only small sections of class I and IIa genes have been used to assess functional diversity in cetacean populations. Here, we undertook a systematic characterisation of the MHC class I and IIa regions in available cetacean genomes. We extracted full-length gene sequences to design pan-cetacean primers that amplified the complete exon 2 from MHC class I and IIa genes in one combined sequencing panel. We validated this panel in 19 cetacean species and described 354 alleles for both classes. Furthermore, we identified likely assembly artefacts for many MHC class I assemblies based on the presence of class I genes in the amplicon data compared to missing genes from genomes. Finally, we investigated MHC diversity using the panel in 25 humpback and 30 southern right whales, including four paternity trios for humpback whales. This revealed copy-number variable class I haplotypes in humpback whales, which is likely a common phenomenon across cetaceans. These MHC alleles will form the basis for a cetacean branch of the Immuno-Polymorphism Database (IPD-MHC), a curated resource intended to aid in the systematic compilation of MHC alleles across several species, to support conservation initiatives.
Subject(s)
Cetacea , Major Histocompatibility Complex , Sequence Analysis, DNA , Animals , Cetacea/genetics , Cetacea/immunology , Cetacea/classification , Major Histocompatibility Complex/genetics , Sequence Analysis, DNA/methods , Genetic Variation , DNA Primers/geneticsABSTRACT
Marine mammals, especially cetaceans, have evolved a very special form of sleep characterized by unihemispheric slow-wave sleep (USWS) and a negligible amount or complete absence of rapid-eye-movement sleep; however, the underlying genetic mechanisms remain unclear. Here, we detected unique, significant selection signatures in basic helix-loop-helix ARNT like 2 (BMAL2; also called ARNTL2), a key circadian regulator, in marine mammal lineages, and identified two nonsynonymous amino acid substitutions (K204E and K346Q) in the important PER-ARNT-SIM domain of cetacean BMAL2 via sequence comparison with other mammals. In vitro assays revealed that these cetacean-specific mutations specifically enhanced the response to E-box-like enhancer and consequently promoted the transcriptional activation of PER2, which is closely linked to sleep regulation. The increased PER2 expression, which was further confirmed both in vitro and in vivo, is beneficial for allowing cetaceans to maintain continuous movement and alertness during sleep. Concordantly, the locomotor activities of zebrafish overexpressing the cetacean-specific mutant bmal2 were significantly higher than the zebrafish overexpressing the wild-type gene. Subsequently, transcriptome analyses revealed that cetacean-specific mutations caused the upregulation of arousal-related genes and the downregulation of several sleep-promoting genes, which is consistent with the need to maintain hemispheric arousal during USWS. Our findings suggest a potential close relationship between adaptive changes in BMAL2 and the remarkable adaptation of USWS and may provide novel insights into the genetic basis of the evolution of animal sleep.
Subject(s)
ARNTL Transcription Factors , Cetacea , Sleep, Slow-Wave , Animals , Locomotion/genetics , Mammals , Sleep/genetics , Sleep, Slow-Wave/genetics , Zebrafish , ARNTL Transcription Factors/genetics , ARNTL Transcription Factors/metabolism , Cetacea/geneticsABSTRACT
The genetic basis underlying adaptive physiological mechanisms has been extensively explored in mammals after colonizing the seas. However, independent lineages of aquatic mammals exhibit complex patterns of secondary colonization in freshwater environments. This change in habitat represents new osmotic challenges, and additional changes in key systems, such as the osmoregulatory system, are expected. Here, we studied the selective regime on coding and regulatory regions of 20 genes related to the osmoregulation system in strict aquatic mammals from independent evolutionary lineages, cetaceans, and sirenians, with representatives in marine and freshwater aquatic environments. We identified positive selection signals in genes encoding the protein vasopressin (AVP) in mammalian lineages with secondary colonization in the fluvial environment and in aquaporins for lineages inhabiting the marine and fluvial environments. A greater number of sites with positive selection signals were found for the dolphin species compared to the Amazonian manatee. Only the AQP5 and AVP genes showed selection signals in more than one independent lineage of these mammals. Furthermore, the vasopressin gene tree indicates greater similarity in river dolphin sequences despite the independence of their lineages based on the species tree. Patterns of distribution and enrichment of Transcription Factors in the promoter regions of target genes were analyzed and appear to be phylogenetically conserved among sister species. We found accelerated evolution signs in genes ACE, AQP1, AQP5, AQP7, AVP, NPP4, and NPR1 for the fluvial mammals. Together, these results allow a greater understanding of the molecular bases of the evolution of genes responsible for osmotic control in aquatic mammals.
Subject(s)
Dolphins , Osmoregulation , Animals , Osmoregulation/genetics , Cetacea/genetics , Mammals/genetics , Fresh Water , Vasopressins/genetics , Evolution, Molecular , PhylogenyABSTRACT
In the context of macroevolutionary transitions, environmental changes prompted vertebrates already bearing genetic variations to undergo gradual adaptations resulting in profound anatomical, physiological, and behavioral adaptations. The emergence of new genes led to the genetic variation essential in metazoan evolution, just as was gene loss, both sources of genetic variation resulting in adaptive phenotypic diversity. In this context, F12-coding protein with defense and hemostatic roles emerged some 425 Mya, and it might have contributed in aquatic vertebrates to the transition from water-to-land. Conversely, the F12 loss in marine, air-breathing mammals like cetaceans has been associated with phenotypic adaptations in some terrestrial mammals in their transition to aquatic lifestyle. More recently, the advent of technological innovations in western lifestyle with blood-contacting devices and harmful environmental nanoparticles, has unfolded new roles of FXII. Environment operates as either a positive or a relaxed selective pressure on genes, and consequently genes are selected or lost. FXII, an old dog facing environmental novelties can learn new tricks and teach us new therapeutic avenues.
Subject(s)
Cetacea , Vertebrates , Animals , Cetacea/genetics , MammalsABSTRACT
In many organisms, especially those of conservation concern, traditional lines of evidence for taxonomic delineation, such as morphological data, are often difficult to obtain. In these cases, genetic data are often the only source of information available for taxonomic studies. In particular, population surveys of mitochondrial genomes offer increased resolution and precision in support of taxonomic decisions relative to conventional use of the control region or other gene fragments of the mitochondrial genome. To improve quantitative guidelines for taxonomic decisions in cetaceans, we build on a previous effort targeting the control region and evaluate, for whole mitogenome sequences, a suite of divergence and diagnosability estimates for pairs of recognized cetacean populations, subspecies, and species. From this overview, we recommend new guidelines based on complete mitogenomes, combined with other types of evidence for isolation and divergence, which will improve resolution for taxonomic decisions, especially in the face of small sample sizes or low levels of genetic diversity. We further use simulated data to assist interpretations of divergence in the context of varying forms of historical demography, culture, and ecology.
Subject(s)
Genome, Mitochondrial , Animals , Cetacea/genetics , Demography , Ecology , Sample Size , PhylogenyABSTRACT
The mammalian skin exhibits a rich spectrum of evolutionary adaptations. The pilosebaceous unit, composed of the hair shaft, follicle, and the sebaceous gland, is the most striking synapomorphy. The evolutionary diversification of mammals across different ecological niches was paralleled by the appearance of an ample variety of skin modifications. Pangolins, order Pholidota, exhibit keratin-derived scales, one of the most iconic skin appendages. This formidable armor is intended to serve as a deterrent against predators. Surprisingly, while pangolins have hair on their abdomens, the occurrence of sebaceous and sweat glands is contentious. Here, we explore various molecular modules of skin physiology in four pangolin genomes, including that of sebum production. We show that genes driving wax monoester formation, Awat1/2, show patterns of inactivation in the stem pangolin branch, while the triacylglycerol synthesis gene Dgat2l6 seems independently eroded in the African and Asian clades. In contrast, Elovl3 implicated in the formation of specific neutral lipids required for skin barrier function is intact and expressed in the pangolin skin. An extended comparative analysis shows that genes involved in skin pathogen defense and structural integrity of keratinocyte layers also show inactivating mutations: associated with both ancestral and independent pseudogenization events. Finally, we deduce that the suggested absence of sweat glands is not paralleled by the inactivation of the ATP-binding cassette transporter Abcc11, as previously described in Cetacea. Our findings reveal the sophisticated and complex history of gene retention and loss as key mechanisms in the evolution of the highly modified mammalian skin phenotypes.
Subject(s)
Gene Regulatory Networks , Pangolins , Animals , Pangolins/genetics , Sebaceous Glands , Mammals/genetics , Cetacea/geneticsABSTRACT
Convergent adaptation to the same environment by multiple lineages frequently involves rapid evolutionary change at the same genes, implicating these genes as important for environmental adaptation. Such adaptive molecular changes may yield either change or loss of protein function; loss of function can eliminate newly deleterious proteins or reduce energy necessary for protein production. We previously found a striking case of recurrent pseudogenization of the Paraoxonase 1 (Pon1) gene among aquatic mammal lineages-Pon1 became a pseudogene with genetic lesions, such as stop codons and frameshifts, at least four times independently in aquatic and semiaquatic mammals. Here, we assess the landscape and pace of pseudogenization by studying Pon1 sequences, expression levels, and enzymatic activity across four aquatic and semiaquatic mammal lineages: pinnipeds, cetaceans, otters, and beavers. We observe in beavers and pinnipeds an unexpected reduction in expression of Pon3, a paralog with similar expression patterns but different substrate preferences. Ultimately, in all lineages with aquatic/semiaquatic members, we find that preceding any coding-level pseudogenization events in Pon1, there is a drastic decrease in expression, followed by relaxed selection, thus allowing accumulation of disrupting mutations. The recurrent loss of Pon1 function in aquatic/semiaquatic lineages is consistent with a benefit to Pon1 functional loss in aquatic environments. Accordingly, we examine diving and dietary traits across pinniped species as potential driving forces of Pon1 functional loss. We find that loss is best associated with diving activity and likely results from changes in selective pressures associated with hypoxia and hypoxia-induced inflammation.
Subject(s)
Aryldialkylphosphatase , Caniformia , Animals , Aryldialkylphosphatase/genetics , Mammals/genetics , Cetacea/genetics , Rodentia , HypoxiaABSTRACT
Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macroevolution.1,2,3,4 Evolution by natural selection across an adaptive landscape should drive lineages toward fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales.5 The location and breadth of these peaks in phenotypic space can also evolve,4 but whether phylogenetic comparative methods can detect such patterns has largely remained unexplored.6 Here, we characterize the global and local adaptive landscape for total body length in cetaceans (whales, dolphins, and relatives), a trait that spans an order of magnitude, across their â¼53-million-year evolutionary history. Using phylogenetic comparative methods, we analyze shifts in long-term mean body length7 and directional changes in average trait values8 for 345 living and fossil cetacean taxa. Remarkably, we find that the global macroevolutionary adaptive landscape of cetacean body length is relatively flat, with very few peak shifts occurring after cetaceans entered the oceans. Local peaks are more numerous and manifest as trends along branches linked to specific adaptations. These results contrast with previous studies using only extant taxa,9 highlighting the vital role of fossil data for understanding macroevolution.10,11,12 Our results indicate that adaptive peaks are dynamic and are associated with subzones of local adaptations, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes and suggest that multiple approaches are required to characterize complex hierarchical patterns of adaptation in deep time.
Subject(s)
Adaptation, Physiological , Biological Evolution , Animals , Phylogeny , Body Size , Cetacea/geneticsABSTRACT
Cetaceans are a group of aquatic mammals with the largest body sizes among living animals, including giant representatives such as blue and fin whales. To understand the genetic bases of gigantism in cetaceans, we performed molecular evolutionary analyses on five genes (GHSR, IGF2, IGFBP2, IGFBP7, and EGF) from the growth hormone/insulin-like growth factor axis, and four genes (ZFAT, EGF, LCORL, and PLAG1) previously described as related to the size of species evolutionarily close to cetaceans, such as pigs, cows, and sheep. Our dataset comprised 19 species of cetaceans, seven of which are classified as giants because they exceed 10 m in length. Our results revealed signs of positive selection in genes from the growth hormone/insulin-like growth factor axis and also in those related to body increase in cetacean-related species. In addition, pseudogenization of the EGF gene was detected in the lineage of toothless cetaceans, Mysticeti. Our results suggest the action of positive selection on gigantism in genes that act both in body augmentation and in mitigating its consequences, such as cancer suppression when involved in processes such as division, migration, and cell development control.
Subject(s)
Cetacea , Epidermal Growth Factor , Animals , Cattle , Sheep , Swine , Phylogeny , Epidermal Growth Factor/genetics , Cetacea/genetics , Evolution, Molecular , Growth Hormone/geneticsABSTRACT
The identification of patterns in trait evolution is essential to understand the interaction of evolutionary forces, and provides useful information for species management. Cetaceans are a phylogenetically well-resolved infraorder that exhibit distinct trait variation across behavioral, molecular, and life history dimensions, yet few researchers have applied a meta-analytic or comparative approach to these traits. To understand cetacean trait evolution, we used a phylogenetic generalized least squares approach to examine the cognitive buffer hypothesis (CBH). A large brain should buffer individuals against environmental challenges through increasing survival rates, and a longer lifespan should buffer individuals against the cost of extended development for larger brains according to the CBH, leading to an expected positive correlation between brain size and lifespan. In contrast to this expectation, previously observed in taxa including primates, we found a negative correlation between brain size and lifespan in cetaceans. This suggests cetaceans experience selective pressures different from most other mammals in these traits but may be more similar to some social mammalian carnivores that display alloparenting. We also provide a comprehensive dataset to explore additional aspects of trait evolution but which would greatly benefit from studies on behavioral ecology across cetaceans and increased focus on data deficient species.
Subject(s)
Carnivora , Life History Traits , Animals , Phylogeny , Longevity , Organ Size , Cetacea/genetics , Brain , Primates , Biological EvolutionABSTRACT
Heteroplasmy in the mitochondrial genome offers a rare opportunity to track the evolution of a newly arising maternal lineage in populations of non-model species. Here, we identified a previously unreported mitochondrial DNA haplotype while assembling an integrated database of DNA profiles and photo-identification records from humpback whales in southeastern Alaska (SEAK). The haplotype, referred to as A8, was shared by only 2 individuals, a mature female with her female calf, and differed by only a single base pair from a common haplotype in the North Pacific, referred to as A-. To investigate the origins of the A8 haplotype, we reviewed n = 1,089 electropherograms (including replicate samples) of n = 710 individuals with A- haplotypes from an existing collection. From this review, we found 20 individuals with clear evidence of heteroplasmy for A-/A8 (parental/derived) haplotypes. Of these, 15 were encountered in SEAK, 4 were encountered on the Hawaiian breeding ground (the primary migratory destination for whales in SEAK), and 1 was encountered in the northern Gulf of Alaska. We used genotype exclusion and likelihood to identify one of the heteroplasmic females as the likely mother of the A8 cow and grandmother of the A8 calf, establishing the inheritance and germ-line fixation of the new haplotype from the parental heteroplasmy. The mutation leading to this heteroplasmy and the fixation of the A8 haplotype provide an opportunity to document the population dynamics and regional fidelity of a newly arising maternal lineage in a population recovering from exploitation.
Subject(s)
Humpback Whale , Animals , Female , Cattle , Humpback Whale/genetics , DNA, Mitochondrial/genetics , Heteroplasmy , Mitochondria/genetics , Cetacea/geneticsABSTRACT
Uncoupling protein 1 (UCP1) is an essential protein in the mitochondrial inner membrane that mediates nonshivering thermogenesis (NST) and plays an important role in thermoregulation and fat deposition. However, the relationship between the evolution of UCP1 and fat deposition in the blubber layer in cetaceans remains unclear. Here, frameshift mutations, premature termination, and relaxed selection pressure (ω = 0.9557, P < 0.05) were detected in UCP1 in cetaceans, suggesting that UCP1 was inactivated during cetacean evolution. By time estimation, it was found that the inactivation of UCP1 in cetaceans occurred between 53.1 and 50.2 Ma. However, combined with findings from immunohistochemical analysis of the blubber layer of the Yangtze finless porpoise and in vitro functional assays, a premature termination of cetacean UCP1 resulted in a reduction of UCP1-mediated NST capacity (about 50%) and lipolytic capacity (about 40%), both of which were beneficial to maintain blubber layer and body temperature without excessive fat consumption. This study provides new insights into the molecular mechanisms of the blubber thickening in cetaceans and highlights the importance of UCP1 attenuation in cetaceans for secondary aquatic adaptation.
Subject(s)
Cetacea , Thermogenesis , Animals , Uncoupling Protein 1/genetics , Uncoupling Protein 1/metabolism , Thermogenesis/genetics , Cetacea/genetics , Cetacea/metabolism , Adaptation, Physiological , Acclimatization , Mitochondrial Proteins/genetics , Mitochondrial Proteins/metabolismABSTRACT
Parasite biodiversity in cetaceans represents a neglected component of the marine ecosystem. This study aimed to investigate the distribution and genetic diversity of anisakid nematodes of the genus Anisakis sampled in cetaceans from the Northeast Atlantic Ocean and the Mediterranean Sea. A total of 478 adults and pre-adults of Anisakis spp. was identified by a multilocus genetic approach (mtDNA cox2, EF1 α - 1 nDNA and nas 10 nDNA gene loci) from 11 cetacean species. A clear pattern of host preference was observed for Anisakis spp. at cetacean family level: A. simplex (s.s.) and A. pegreffii infected mainly delphinids; A. physeteris and A. brevispiculata were present only in physeterids, and A. ziphidarum occurred in ziphiids. The role of cetacean host populations from different waters in shaping the population genetic structure of A. simplex (s.s.), A. pegreffii and A. physeteris was investigated for the first time. Significant genetic sub-structuring was found in A. simplex (s.s.) populations of the Norwegian Sea and the North Sea compared to those of the Iberian Atlantic, as well as in A. pegreffii populations of the Adriatic and the Tyrrhenian Seas compared to those of the Iberian Atlantic waters. Substantial genetic homogeneity was detected in the Mediterranean Sea population of A. physeteris. This study highlights a strong preference by some Anisakis spp. for certain cetacean species or families. Information about anisakid biodiversity in their cetacean definitive hosts, which are apex predators of marine ecosystems, acquires particular importance for conservation measures in the context of global climate change phenomena.
Subject(s)
Anisakis , Fish Diseases , Animals , Anisakis/genetics , Atlantic Ocean , Cetacea/genetics , Ecosystem , Fish Diseases/parasitology , Genetic Variation , Humans , Larva/genetics , Mediterranean Sea , PhylogenyABSTRACT
Nasopulmonary mites (NPMs) of the family Halarachnidae are obligate endoparasites that colonize the respiratory tracts of mammals. NPMs damage surface epithelium resulting in mucosal irritation, respiratory illness, and secondary infection, yet the role of NPMs in facilitating pathogen invasion or dissemination between hosts remains unclear. Using 16S rRNA massively parallel amplicon sequencing of six hypervariable regions (or "16S profiling"), we characterized the bacterial community of NPMs from 4 southern sea otters (Enhydra lutris nereis). This data was paired with detection of a priority pathogen, Streptococcus phocae, from NPMs infesting 16 southern sea otters and 9 California sea lions (Zalophus californianus) using nested conventional polymerase chain reaction (nPCR). The bacteriome of assessed NPMs was dominated by Mycoplasmataceae and Vibrionaceae, but at least 16 organisms with pathogenic potential were detected as well. Importantly, S. phocae was detected in 37% of NPM by nPCR and was also detected by 16S profiling. Detection of multiple organisms with pathogenic potential in or on NPMs suggests they may act as mechanical vectors of bacterial infection for marine mammals.
Subject(s)
Caniformia , Mites , Otters , Sea Lions , Animals , Caniformia/genetics , Cetacea/genetics , Mites/genetics , Otters/genetics , RNA, Ribosomal, 16S/genetics , Sea Lions/genetics , Streptococcus/geneticsABSTRACT
Viruses are the most common and abundant organisms in the marine environment. To better understand how cetaceans have adapted to this virus-rich environment, we compared cetacean virus-responsive genes to those from terrestrial mammals. We identified virus-responsive gene sequences in seven species of cetaceans, which we compared with orthologous sequences in seven terrestrial mammals. As a result of evolution analysis using the branch model and the branch-site model, 21 genes were selected using at least one model. IFN-ε, an antiviral cytokine expressed at mucous membranes, and its receptor IFNAR1 contain cetacean-specific amino acid substitutions that might change the interaction between the two proteins and lead to regulation of the immune system against viruses. Cetacean-specific amino acid substitutions in IL-6, IL-27, and the signal transducer and activator of transcription (STAT)1 are also predicted to alter the mucosal immune response of cetaceans. Since mucosal membranes are the first line of defense against the external environment and are involved in immune tolerance, our analysis of cetacean virus-responsive genes suggests that genes with cetacean-specific mutations in mucosal immunity-related genes play an important role in the protection and/or regulation of immune responses against viruses.
Subject(s)
Cetacea , Immunity, Mucosal , Animals , Immunity, Mucosal/genetics , Phylogeny , Cetacea/genetics , Mammals , Adaptation, PhysiologicalABSTRACT
The adaptation of vertebrates to different environments was associated with changes in the molecular composition and regulation of epithelia. Whales and dolphins, together forming the clade cetaceans, have lost multiple epithelial keratins during or after their evolutionary transition from life on land to life in water. It is unknown whether the changes in keratins were accompanied by gain or loss of cytoskeletal adapter proteins of the plakin family. Here we investigated whether plakin proteins are conserved in cetaceans and other vertebrates. Comparative analysis of genome sequences showed conservation of dystonin, microtubule actin crosslinking factor 1 (MACF1), plectin, desmoplakin, periplakin and envoplakin in cetaceans. By contrast, EPPK1 (epiplakin) was disrupted by inactivating mutations in all cetaceans investigated. Orthologs of EPPK1 are present in bony and cartilaginous fishes and tetrapods, indicating an evolutionary origin of EPPK1 in a common ancestor of jawed vertebrates (Gnathostomes). In many vertebrates, EPPK1 is flanked by an as-yet uncharacterized gene that encodes protein domains homologous to the carboxy-terminal segment of MACF1. We conclude that epiplakin, unlike other plakins, was lost in cetaceans.