Genomics of post-bottleneck recovery in the northern elephant seal.

Populations and species are threatened by human pressure, but their fate is variable. Some depleted populations, such as that of the northern elephant seal (Mirounga angustirostris), recover rapidly even when the surviving population was small. The northern elephant seal was hunted extensively and taken by collectors between the early 1800s and 1892, suffering an extreme population bottleneck as a consequence. Recovery was rapid and now there are over 200,000 individuals. We sequenced 260 modern and 8 historical northern elephant seal nuclear genomes to assess the impact of the population bottleneck on individual northern elephant seals and to better understand their recovery. Here we show that inbreeding, an increase in the frequency of alleles compromised by lost function, and allele frequency distortion, reduced the fitness of breeding males and females, as well as the performance of adult females on foraging migrations. We provide a detailed investigation of the impact of a severe bottleneck on fitness at the genomic level and report on the role of specific gene systems.

Skinny dolphins: Can poor body condition explain population decline in Indo-Pacific humpback dolphins (Sousa chinensis)?

Indo-Pacific humpback dolphins (IPHDs) who form resident populations along the Chinese coastline are facing a wide range of anthropogenic disturbances including intense fishing and some populations have been shown to experience a severe decline. Body condition is thought to be a good indicator of health since it is linked to survival and reproductive success. In order to better understand population trends, we investigated whether the body condition of IPHDs is poorer in populations whose status is alarming than in other populations. UAV flights were conducted from 2022 to 2023 in four locations (i.e., Sanniang Bay, Leizhou Bay, Jiangmen, and Lingding Bay) in the northern South China Sea. Body ratios were calculated using the body length and widths of IPHDs and were used to analyze differences among seasons, locations, and demographic parameters. A PCA was then used to obtain a detailed picture of the body condition composition of dolphins at each location. Results showed that dolphins from Leizhou Bay and Jiangmen were in better body condition than those from Sanniang Bay and Lingding Bay. Since populations inhabiting Sanniang Bay and Lingding Bay have been shown to experience a sharp decline, it can be hypothesized that poor body condition may have played a role in such a trend. Further investigations of the factors impacting IPHDs' body condition are needed, including monitoring of prey density, contaminant concentration, stress levels, and impacts of human activities on dolphins' behavior. In addition, the creation of a robust scoring method would allow for regular monitoring of IPHDs' body condition to inform conservation measures.

Geographic and tissue-specific variations of the trace elements and trophic niches of three offshore cetaceans in Chinese waters.

Systematical investigation on trace elements' (TEs) distribution and trophic niches of cetaceans are essential to understand marine mammal ecology and environmental toxicology. Here, the concentrations of 10 TEs and isotopic values in six tissues of stranded Stenella attenuata (SA) and Kogia breviceps (KB) from the northern South China Sea (SCS) and Peponocephala electra (PE) from the East China Sea (ECS) were investigated. The TEs levels of the studied cetaceans were characterized by geo- and tissue-specific distributions. For SA and KB, most TEs levels were in the normal ranges, with low toxicological risk. For PE, several toxic TEs accumulated above the thresholds up to 892.80 µg/g of Hg and 335.24 µg/g of Cd, indicating that land-based anthropogenic pollution may be an ongoing threat to top predators in the ECS. The liver, spleen, and kidney are the main organs that accumulate toxic TEs, and there are strong positive, such as Se-Hg, correlations in several tissues. In particular, for PE with severe Hg and Cd exposure, tissue-specific distribution and correlations were more obvious. The results of stable carbon and nitrogen isotopes showed partly overlapped trophic niches of the three cetaceans, with similar calculated trophic levels in a narrow range of 4.29-4.43.

Inbreeding depression explains killer whale population dynamics.

Understanding the factors that cause endangered populations to either grow or decline is crucial for preserving biodiversity. Conservation efforts often address extrinsic threats, such as environmental degradation and overexploitation, that can limit the recovery of endangered populations. Genetic factors such as inbreeding depression can also affect population dynamics but these effects are rarely measured in the wild and thus often neglected in conservation efforts. Here we show that inbreeding depression strongly influences the population dynamics of an endangered killer whale population, despite genomic signatures of purging of deleterious alleles via natural selection. We find that the 'Southern Residents', which are currently endangered despite nearly 50 years of conservation efforts, exhibit strong inbreeding depression for survival. Our population models suggest that this inbreeding depression limits population growth and predict further decline if the population remains genetically isolated and typical environmental conditions continue. The Southern Residents also had more inferred homozygous deleterious alleles than three other, growing, populations, further suggesting that inbreeding depression affects population fitness. These results demonstrate that inbreeding depression can substantially limit the recovery of endangered populations. Conservation actions focused only on extrinsic threats may therefore fail to account for key intrinsic genetic factors that also limit population growth.

Echolocation clicks of free-ranging Indo-Pacific finless porpoises (Neophocaena phocaenoides) in Hainan waters.

The echolocation clicks of free-ranging Indo-Pacific finless porpoises (IPFPs, Neophocaena phocaenoides) have been rarely studied in the wild. This paper aims at describing the echolocation-click characteristics of IPFPs and examining whether IPFPs adapt their sonar system to the habitats in Hainan waters, China. The echolocation clicks were recorded using a 13 elements star-shaped array of hydrophones. A total of 65 on-axis clicks were identified and analyzed. IPFPs use echolocation clicks with a source level (SL) of 158 ± 9 dB re: 1 µPa peak-peak, mean peak, and centroid frequency of 134 ± 3 kHz, -3 dB bandwidth of 14 ± 2 kHz and produce at inter-click intervals of 104 ± 51 ms. The results relative to other porpoises show that finless porpoises in Hainan waters produce clicks with moderate SLs and high peak frequency. These results could be useful in detecting the presence and estimating the density of IPFPs during passive acoustic monitoring in the study area and serve to shed light on the interpopulation variation of click characteristics of finless porpoises as well.

A genome and single-nucleus cerebral cortex transcriptome atlas of the short-finned pilot whale Globicephala macrorhynchus.

Cetaceans (dolphins, whales, and porpoises) have large and anatomically sophisticated brains. To expand our understanding of the cellular makeup of cetacean brains and the similarities and divergence between the brains of cetaceans and terrestrial mammals, we report a short-finned pilot whale (Globicephala macrorhynchus) single-nucleus transcriptome atlas. To achieve this goal, we assembled a chromosome-scale reference genome spanning 2.25 Gb on 22 chromosomes and profiled the gene expression of five major anatomical cortical regions of the short-finned pilot whale by single-nucleus RNA-sequencing (snRNA-seq). We identified six major cell lineages in the cerebral cortex (excitatory neurons, inhibitory neurons, oligodendrocytes, oligodendrocyte precursor cells, astrocytes, and endothelial cells), eight molecularly distinct subclusters of excitatory neurons, and four subclusters of inhibitory neurons. Finally, a comparison of snRNA-seq data from the short-finned pilot whale, human, and rhesus macaque revealed a broadly conserved cellular makeup of brain cell types. Our study provides genomic resources and molecular insights into cetacean brain evolution.

Ranging pattern development of a declining delphinid population: A potential cascade effect of vessel activities.

It is generally accepted that vessel activity causes various behavioral responses of cetaceans and undermines individual fitness. Whether or how it can lead to a demographic response of populations remains rarely examined. In the northern Beibu Gulf, China, vessel activities have sharply increased in the past two decades, while abnormal demographic dynamics was recently noted for the resident Indo-Pacific humpback dolphins. The present study first examined the humpback dolphins' utilization distribution (UD) from 2003 to 2019. Habitat suitability was then modeled with the sighting data collected before the most recent population reduction. Finally, we tried to disentangle the anthropogenic driver of dolphin demography by cross-referring the spatiotemporal development of dolphins' UD, vessel activities, and habitat suitability. Our results showed that the dolphins' UD shrank substantially during the port expansion in the early 2010s, and we suggest that the consequential increase in vessel activities might impose extra marine stressors on the resident humpback dolphins. To reduce the boat interaction, the dolphins steadily shifted their core area to a less suitable area in the east during 2015-2017, when unnaturally low survivals were recorded. Afterward, the dolphin core area partially shifted back to the more suitable area in the west, which corresponded to the improving dolphin survival in 2018. Our finding suggested that the vessel activity may be responsible for the dolphin displacement, while staying in the less suitable area may further lead to a more severe and acute demographic consequence on the population. The underlying and indirect impact of vessel activities as disclosed by the present study is particularly important for port management, marine planning, and conservation practice regarding coastal cetaceans, especially for those resident and endangered populations inhabiting the urbanized coastal areas.

Floating macro-litter pollution in the northern South China Sea.

Marine litter pollution, particularly plastics pollution, is an increasing global concern. While various studies have contributed useful information on this topic, there has been a scarcity of data on floating marine macro-litter (FMML) in poorly monitored areas such as the South China Sea (SCS). This paper describes a large-scale FMML assessment research in the northern SCS. Our data indicated the ubiquitous presence, abundant quantity, spatiotemporal variability, complex composition, and potential sources of FMML in the investigated region during boreal spring-summer periods over multiple years. According to observer-based records, the average FMML density was estimated to be 131.0 ± 91.8 items/km2 (mean ± SD), with anthropogenic FMML density of 118.7 ± 86.2 items/km2. Anthropogenic and natural items accounted for 90.6% and 5.5% of the total, respectively. Plastics (72.0%) and styrofoam (9.3%) dominated the recorded items. The great majority of items (92.1%) were characterized by small size of ≤20 cm. Labels of plastic bottle/packaging litter indicated that identifiable sources included surrounding countries of the SCS. Fishing activities were recognized as key sources of FMML, with 15.3% of FMML items likely being fishing-related. Globally, known estimates of FMML densities could vary from 0.002 to 578 items/km2, with plastics accounting for 34.8-99.0%. Therefore, marine pollution from anthropogenic FMML in our investigated area ranked at a medium-to-high level around the globe. To conclude, this study demonstrated that the SCS is one of the world's hotspot areas with FMML pollution and sheds light on marine litter pollution, especially plastics pollution, in this intensively human-exploited but poorly monitored region. In future research, FMML pollution in other sections of SCS and possible negative impacts of FMML on marine ecosystems and megafauna should be further examined.

Functional extinction of dugongs in China.

Dugongs (Dugong dugon) experienced a serious population decline in China during the twentieth century, and their regional status is poorly understood. To determine their current distribution and status, we conducted a large-scale interview survey of marine resource users across four Chinese provinces and reviewed all available historical data covering the past distribution of dugongs in Chinese waters. Only 5% of 788 respondents reported past dugong sightings, with a mean last-sighting date of 23 years earlier, and only three respondents reported sightings from within the past 5 years. Historical records of dugongs peak around 1960 and then decrease rapidly from 1975 onwards; no records are documented after 2008, with no verified field observations after 2000. Based on these findings, we are forced to conclude that dugongs have experienced rapid population collapse during recent decades and are now functionally extinct in China. Our study provides evidence of a new regional loss of a charismatic marine megafaunal species, and the first reported functional extinction of a large vertebrate in Chinese marine waters. This rapid documented population collapse also serves as a sobering reminder that extinctions can occur before effective conservation actions are developed.

Gut Microbial Characterization of Melon-Headed Whales (Peponocephala electra) Stranded in China.

Although gut microbes are regarded as a significant component of many mammals and play a very important role, there is a paucity of knowledge around marine mammal gut microbes, which may be due to sampling difficulties. Moreover, to date, there are very few, if any, reports on the gut microbes of melon-headed whales. In this study, we opportunistically collected fecal samples from eight stranded melon-headed whales (Peponocephala electra) in China. Using high-throughput sequencing technology of partial 16S rRNA gene sequences, we demonstrate that the main taxa of melon-headed whale gut microbes are Firmicutes, Fusobacteriota, Bacteroidota, and Proteobacteria (Gamma) at the phylum taxonomic level, and Cetobacterium, Bacteroides, Clostridium sensu stricto, and Enterococcus at the genus taxonomic level. Meanwhile, molecular ecological network analysis (MENA) shows that two modules (a set of nodes that have strong interactions) constitute the gut microbial community network of melon-headed whales. Module 1 is mainly composed of Bacteroides, while Module 2 comprises Cetobacterium and Enterococcus, and the network keystone genera are Corynebacterium, Alcaligenes, Acinetobacter, and Flavobacterium. Furthermore, by predicting the functions of the gut microbial community through PICRUSt2, we found that although there are differences in the composition of the gut microbial community in different individuals, the predicted functional profiles are similar. Our study gives a preliminary inside look into the composition of the gut microbiota of stranded melon-headed whales.

Species diversity and spatiotemporal patterns based on cetacean stranding records in China, 1950-2018.

Stranding data can provide conservation-valuable information on cetaceans over long time and large space, representing a low-cost but useful approach to monitor these indicator species and their inhabiting environments. Here, we established a national dataset by collating all available records of cetacean strandings (CSs) along >30,000-km coastline of China over seven decades. Between 1950 and 2018, a total of 1763 CSs were recorded across 36 cetacean species from eight families. Importantly, 30.5% of the recorded species are currently recognized as threatened levels on the IUCN Red List. In quantity, Odontocete species accounted for 89.9% of total CSs. In 1763 CSs, 91.8% were events of single individual. Furthermore, 31.9% and 42.4% were events of alive and dead animals, respectively. The number of CSs increased gradually from 1950 to 2018, and more rapidly between 1990 and 2018. CSs occurred in all months, while a seasonal pattern could be observed with 38.5% reports between March and June. The most commonly recorded species were finless porpoises (Neophocaena spp., n = 492) and Indo-Pacific humpback dolphin (Sousa chinensis, n = 291). The highest number of CSs (n = 478) was documented in Hong Kong, while the greatest species richness (n = 28) and the highest stranding density (24.6 CSs per 100-km coastline) were observed in Taiwan. Several CS hotspots were identified in the southern and eastern China, while hotspots differed among taxonomic categories. To conclude, these findings provided a comprehensive understanding of cetacean communities in the coastal waters of China, which are beneficial for improving further research, conservation, and management on cetaceans.

Blubber fatty acid compositions in different geographic populations of finless porpoise in Chinese waters: implications for thermal adaptation.

The stratification of blubber fatty acids (FAs) is a widely used strategy in marine mammals and can be influenced by many factors, including their diet, environmental temperature, and physiological status. There are 3 distinct finless porpoise species/subspecies in Chinese coastal and inland waters in a wide range from 20°N to 40°N. The biochemical stratification of the blubbers of finless porpoises in different regions may provide valuable information for understanding their environmental adaptations. The FA compositions of 4 geographic populations of finless porpoise (FP) collected from the Bohai Gulf, East China Sea, South China Sea, and Yangtze River were therefore analyzed and compared. The blubber FA compositions of finless porpoises were dominated by ΣMUFAs, followed by ΣSFAs and ΣPUFAs, and were generally consistent with those of other cetaceans. The blubber of finless porpoises was significantly stratified with increasing levels of ΣMUFAs and decreasing levels of ΣSFAs and ΣPUFAs from the inner to the outer layers. The 3 marine populations shared more similarities in their FA compositions and stratifications compared to the freshwater porpoises, particularly regarding the PUFAs in the inner layers, which might have been mainly influenced by the diet compositions of marine and freshwater porpoises. Contrary to what was expected, in the 3 marine populations, the SFA and MUFA levels showed opposite correlations (negative and positive, respectively) with habitat temperatures, possibly indicating an adaptation mechanism in finless porpoises characterized by a trade-off between the insulation and fluidity properties of the blubber through the adjustment of the compositions and gradients of MUFAs and SFAs across the blubber depth in response to environmental temperature/latitude changes.

Comparative Study of the Gut Microbiota Among Four Different Marine Mammals in an Aquarium.

Despite an increasing appreciation in the importance of host-microbe interactions in ecological and evolutionary processes, information on the gut microbial communities of some marine mammals is still lacking. Moreover, whether diet, environment, or host phylogeny has the greatest impact on microbial community structure is still unknown. To fill part of this knowledge gap, we exploited a natural experiment provided by an aquarium with belugas (Delphinapterus leucas) affiliated with family Monodontidae, Pacific white-sided dolphins (Lagenorhynchus obliquidens) and common bottlenose dolphin (Tursiops truncatus) affiliated with family Delphinidae, and Cape fur seals (Arctocephalus pusillus pusillus) affiliated with family Otariidae. Results show significant differences in microbial community composition of whales, dolphins, and fur seals and indicate that host phylogeny (family level) plays the most important role in shaping the microbial communities, rather than food and environment. In general, the gut microbial communities of dolphins had significantly lower diversity compared to that of whales and fur seals. Overall, the gut microbial communities were mainly composed of Firmicutes and Gammaproteobacteria, together with some from Bacteroidetes, Fusobacteria, and Epsilonbacteraeota. However, specific bacterial lineages were differentially distributed among the marine mammal groups. For instance, Lachnospiraceae, Ruminococcaceae, and Peptostreptococcaceae were the dominant bacterial lineages in the gut of belugas, while for Cape fur seals, Moraxellaceae and Bacteroidaceae were the main bacterial lineages. Moreover, gut microbial communities in both Pacific white-sided dolphins and common bottlenose dolphins were dominated by a number of pathogenic bacteria, including Clostridium perfringens, Vibrio fluvialis, and Morganella morganii, reflecting the poor health condition of these animals. Although there is a growing recognition of the role microorganisms play in the gut of marine mammals, current knowledge about these microbial communities is still severely lacking. Large-scale research studies should be undertaken to reveal the roles played by the gut microbiota of different marine mammal species.

Identification and genome analysis of a novel picornavirus from captive belugas (Delphinapterus leucas) in China.

The discovery of new viruses is important for predicting their potential threats to the health of humans and other animals. A novel picornavirus was identified from oral, throat, and anal swab samples collected from belugas (Delphinapterus leucas), from Dalian Sun Asia Tourism Holding Co., China, between January and December 2018, using a metagenomics approach. The genome of this novel PicoV-HMU-1 strain was 8197 nucleotides (nt) in length, with a open reading frame (from 1091 to 8074 nt) that encoded a polyprotein precursor of 2328 amino acids. Moreover, the genomic length and GC content of PicoV-HMU-1 were within the ranges found in other picornaviruses, and the genome organization was also similar. Nevertheless, PicoV-HMU-1 had a lower amino acid identity and distinct host species compared with other members of the Picornaviridae family. Phylogenetic trees were constructed based on the P1 and 3D amino acid sequences of PicoV-HMU-1 along with representative members of the Picornaviridae family, which showed that PicoV-HMU-1 was related to unclassified bat picornaviruses groups. These findings suggest that the PicoV-HMU-1 strain represents a potentially novel genus of picornavirus. These data can enhance our understanding of the picornavirus genetic diversity and evolution.

Comparative genomics provides insights into the aquatic adaptations of mammals.

The ancestors of marine mammals once roamed the land and independently committed to an aquatic lifestyle. These macroevolutionary transitions have intrigued scientists for centuries. Here, we generated high-quality genome assemblies of 17 marine mammals (11 cetaceans and six pinnipeds), including eight assemblies at the chromosome level. Incorporating previously published data, we reconstructed the marine mammal phylogeny and population histories and identified numerous idiosyncratic and convergent genomic variations that possibly contributed to the transition from land to water in marine mammal lineages. Genes associated with the formation of blubber (NFIA), vascular development (SEMA3E), and heat production by brown adipose tissue (UCP1) had unique changes that may contribute to marine mammal thermoregulation. We also observed many lineage-specific changes in the marine mammals, including genes associated with deep diving and navigation. Our study advances understanding of the timing, pattern, and molecular changes associated with the evolution of mammalian lineages adapting to aquatic life.

Numerical-modeling-based investigation of sound transmission and reception in the short-finned pilot whale (Globicephala macrorhynchus).

The sound-transmission, beam-formation, and sound-reception processes of a short-finned pilot whale (Globicephala macrorhynchus) were investigated using computed tomography (CT) scanning and numerical simulation. The results showed that sound propagations in the forehead were modulated by the upper jaw, air components, and soft tissues, which attributed to the beam formation in the external acoustic field. These structures owned different acoustic impedance and formed a multiphasic sound transmission system that can modulate sounds into a beam. The reception pathways composed of the solid mandible and acoustic fats in the lower head conducted sounds into the tympano-periotic complex. In the simulations, sounds were emitted in the forehead transmission system and propagated into water to interrogate a steel cylinder. The resulting echoes can be interpreted from multiple perspectives, including amplitude, waveform, and spectrum, to obtain the acoustic cues of the steel cylinder. By taking the short-finned pilot whale as an example, this study provides meaningful information to further deepen our understanding of biosonar system operations, and may expand sound-reception theory in odontocetes.

Runs of homozygosity in killer whale genomes provide a global record of demographic histories.

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.