Revised taxonomy of eastern North Pacific killer whales (Orcinus orca): Bigg's and resident ecotypes deserve species status.

Killer whales (Orcinus orca) are currently recognized as a single ecologically and morphologically diverse, globally distributed species. Multiple morphotypes or ecotypes have been described, often associated with feeding specialization, and several studies have suggested taxonomic revision to include multiple subspecies or species in the genus. We review the ecological, morphological and genetic data for the well-studied 'resident' and Bigg's (aka 'transient') ecotypes in the eastern North Pacific and use quantitative taxonomic guidelines and standards to determine whether the taxonomic status of these killer whale ecotypes should be revised. Our review and new analyses indicate that species-level status is justified in both cases, and we conclude that eastern North Pacific Bigg's killer whales should be recognized as Orcinus rectipinnus (Cope in Scammon, 1869) and resident killer whales should be recognized as Orcinus ater (Cope in Scammon, 1869).

The genomic footprint of whaling and isolation in fin whale populations.

Twentieth century industrial whaling pushed several species to the brink of extinction, with fin whales being the most impacted. However, a small, resident population in the Gulf of California was not targeted by whaling. Here, we analyzed 50 whole-genomes from the Eastern North Pacific (ENP) and Gulf of California (GOC) fin whale populations to investigate their demographic history and the genomic effects of natural and human-induced bottlenecks. We show that the two populations diverged ~16,000 years ago, after which the ENP population expanded and then suffered a 99% reduction in effective size during the whaling period. In contrast, the GOC population remained small and isolated, receiving less than one migrant per generation. However, this low level of migration has been crucial for maintaining its viability. Our study exposes the severity of whaling, emphasizes the importance of migration, and demonstrates the use of genome-based analyses and simulations to inform conservation strategies.

Guidelines and quantitative standards for improved cetacean taxonomy using full mitochondrial genomes.

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.

Diversity of mitochondrial DNA in 3 species of great whales before and after modern whaling.

The 20th century commercial whaling industry severely reduced populations of great whales throughout the Southern Hemisphere. The effect of this exploitation on genetic diversity and population structure remains largely undescribed. Here, we compare pre- and post-whaling diversity of mitochondrial DNA (mtDNA) control region sequences for 3 great whales in the South Atlantic, such as the blue, humpback, and fin whale. Pre-whaling diversity is described from mtDNA extracted from bones collected near abandoned whaling stations, primarily from the South Atlantic island of South Georgia. These bones are known to represent the first stage of 20th century whaling and thus pre-whaling diversity of these populations. Post-whaling diversity is described from previously published studies reporting large-scale sampling of living whales in the Southern Hemisphere. Despite relatively high levels of surviving genetic diversity in the post-whaling populations, we found evidence of a probable loss of mtDNA lineages in all 3 species. This is evidenced by the detection of a large number of haplotypes found in the pre-whaling samples that are not present in the post-whaling samples. A rarefaction analysis further supports a loss of haplotypes in the South Atlantic humpback and Antarctic blue whale populations. The bones from former whaling stations in the South Atlantic represent a remarkable molecular archive for further investigation of the decline and ongoing recovery in the great whales of the Southern Hemisphere.

Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters.

Parallel evolution provides strong evidence of adaptation by natural selection due to local environmental variation. Yet, the chronology, and mode of the process of parallel evolution remains debated. Here, we harness the temporal resolution of paleogenomics to address these long-standing questions, by comparing genomes originating from the mid-Holocene (8610-5626 years before present, BP) to contemporary pairs of coastal-pelagic ecotypes of bottlenose dolphin. We find that the affinity of ancient samples to coastal populations increases as the age of the samples decreases. We assess the youngest genome (5626 years BP) at sites previously inferred to be under parallel selection to coastal habitats and find it contained coastal-associated genotypes. Thus, coastal-associated variants rose to detectable frequencies close to the emergence of coastal habitat. Admixture graph analyses reveal a reticulate evolutionary history between pelagic and coastal populations, sharing standing genetic variation that facilitated rapid adaptation to newly emerged coastal habitats.

Possible niche compression and individual specialization in Pacific Arctic beluga (Delphinapterus leucas) from the 19th to 20th century.

Cetaceans have shown a potential to be used as sentinel species for tracking environmental change in marine ecosystems, yet our assessment of change is typically limited to recent decades and lacks ecological baselines. Using historical museum specimens, we compared community niche metrics and degree of individual dietary specialization in groups of Pacific Arctic beluga (Delphinapterus leucas) from the 1800s (n = 5) to 1900s (n = 10) using stable carbon and nitrogen isotopes drilled from teeth. Beluga occupied a broader trophic niche and demonstrated a higher degree of individual specialization in the 1800s than in the 1900s. The cause of this shift is difficult to confirm given long timescales and constraints of specimen-based research but could indicate changes in the prey base or competition. The scale and nature of this detected shift provide perspective for continued research on these climate-vulnerable species.

Historical Mitogenomic Diversity and Population Structuring of Southern Hemisphere Fin Whales.

Fin whales Balaenoptera physalus were hunted unsustainably across the globe in the 19th and 20th centuries, leading to vast reductions in population size. Whaling catch records indicate the importance of the Southern Ocean for this species; approximately 730,000 fin whales were harvested during the 20th century in the Southern Hemisphere (SH) alone, 94% of which were at high latitudes. Genetic samples from contemporary whales can provide a window to past population size changes, but the challenges of sampling in remote Antarctic waters limit the availability of data. Here, we take advantage of historical samples in the form of bones and baleen available from ex-whaling stations and museums to assess the pre-whaling diversity of this once abundant species. We sequenced 27 historical mitogenomes and 50 historical mitochondrial control region sequences of fin whales to gain insight into the population structure and genetic diversity of Southern Hemisphere fin whales (SHFWs) before and after the whaling. Our data, both independently and when combined with mitogenomes from the literature, suggest SHFWs are highly diverse and may represent a single panmictic population that is genetically differentiated from Northern Hemisphere populations. These are the first historic mitogenomes available for SHFWs, providing a unique time series of genetic data for this species.

Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition.

Biodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well-being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize, and interpret biodiversity observation data from diverse sources. Mapping and analyzing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within-species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modeling, and technological advances. We propose four Genetic EBVs: (i) Genetic Diversity; (ii) Genetic Differentiation; (iii) Inbreeding; and (iv) Effective Population Size (Ne ). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modeling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large-scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species' long-term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.

Acoustic differentiation and classification of wild belugas and narwhals using echolocation clicks.

Belugas (Delphinapterus leucas) and narwhals (Monodon monoceros) are highly social Arctic toothed whales with large vocal repertoires and similar acoustic profiles. Passive Acoustic Monitoring (PAM) that uses multiple hydrophones over large spatiotemporal scales has been a primary method to study their populations, particularly in response to rapid climate change and increasing underwater noise. This study marks the first acoustic comparison between wild belugas and narwhals from the same location and reveals that they can be acoustically differentiated and classified solely by echolocation clicks. Acoustic recordings were made in the pack ice of Baffin Bay, West Greenland, during 2013. Multivariate analyses and Random Forests classification models were applied to eighty-one single-species acoustic events comprised of numerous echolocation clicks. Results demonstrate a significant difference between species' acoustic parameters where beluga echolocation was distinguished by higher frequency content, evidenced by higher peak frequencies, center frequencies, and frequency minimums and maximums. Spectral peaks, troughs, and center frequencies for beluga clicks were generally > 60 kHz and narwhal clicks < 60 kHz with overlap between 40-60 kHz. Classification model predictive performance was strong with an overall correct classification rate of 97.5% for the best model. The most important predictors for species assignment were defined by peaks and notches in frequency spectra. Our results provide strong support for the use of echolocation in PAM efforts to differentiate belugas and narwhals acoustically.

Selection on ancestral genetic variation fuels repeated ecotype formation in bottlenose dolphins.

Studying repeated adaptation can provide insights into the mechanisms allowing species to adapt to novel environments. Here, we investigate repeated evolution driven by habitat specialization in the common bottlenose dolphin. Parapatric pelagic and coastal ecotypes of common bottlenose dolphins have repeatedly formed across the oceans. Analyzing whole genomes of 57 individuals, we find that ecotype evolution involved a complex reticulated evolutionary history. We find parallel linked selection acted upon ancient alleles in geographically distant coastal populations, which were present as standing genetic variation in the pelagic populations. Candidate loci evolving under parallel linked selection were found in ancient tracts, suggesting recurrent bouts of selection through time. Therefore, despite the constraints of small effective population size and long generation time on the efficacy of selection, repeated adaptation in long-lived social species can be driven by a combination of ecological opportunities and selection acting on ancestral standing genetic variation.