"Type D" killer whale genomes reveal long-term small population size and low genetic diversity.

Genome sequences can reveal the extent of inbreeding in small populations. Here, we present the first genomic characterization of type D killer whales, a distinctive eco/morphotype with a circumpolar, subantarctic distribution. Effective population size is the lowest estimated from any killer whale genome and indicates a severe population bottleneck. Consequently, type D genomes show among the highest level of inbreeding reported for any mammalian species (FROH ≥ 0.65). Detected recombination cross-over events of different haplotypes are up to an order of magnitude rarer than in other killer whale genomes studied to date. Comparison of genomic data from a museum specimen of a type D killer whale that stranded in New Zealand in 1955, with 3 modern genomes from the Cape Horn area, reveals high covariance and identity-by-state of alleles, suggesting these genomic characteristics and demographic history are shared among geographically dispersed social groups within this morphotype. Limitations to the insights gained in this study stem from the nonindependence of the 3 closely related modern genomes, the recent coalescence time of most variation within the genomes, and the nonequilibrium population history which violates the assumptions of many model-based methods. Long-range linkage disequilibrium and extensive runs of homozygosity found in type D genomes provide the potential basis for both the distinctive morphology, and the coupling of genetic barriers to gene flow with other killer whale populations.

Increasing numbers of killer whale individuals use fisheries as feeding opportunities within subantarctic populations.

Fisheries can generate feeding opportunities for large marine predators in the form of discards or accessible catch. How the use of this anthropogenic food may spread as a new behaviour, across individuals within populations over time, is poorly understood. This study used a 16-year (2003-2018) monitoring of two killer whale Orcinus orca subantarctic populations (regular and Type-D at Crozet), and Bayesian multistate capture-mark-recapture models, to assess temporal changes in the number of individuals feeding on fish caught on hooks ('depredation' behaviour) of a fishery started in 1996. For both populations, the number of depredating individuals increased during the study period (34 to 94 for regular; 17 to 43 for Type-D). Increasing abundance is unlikely to account for this and, rather, the results suggest depredation was acquired by increasing numbers of existing individuals. For regular killer whales, a plateau reached from 2014 suggests that it took 18 years for the behaviour to spread across the whole population. A more recent plateau was apparent for Type-Ds but additional years are needed to confirm this. These findings show how changes in prey availability caused by human activities lead to rapid, yet progressive, innovations in killer whales, likely altering the ecological role of this top-predator.

Role of sociality in the response of killer whales to an additive mortality event.

In highly social top predators, group living is an ecological strategy that enhances individual fitness, primarily through increased foraging success. Additive mortality events across multiple social groups in populations may affect the social structure, and therefore the fitness, of surviving individuals. This hypothesis was examined in a killer whale (Orcinus orca) population that experienced a 7-y period of severe additive mortality due to lethal interactions with illegal fishing vessels. Using both social and demographic analyses conducted on a unique long-term dataset encompassing periods before, during, and after this event, results indicated a decrease in both the number and the mean strength of associations of surviving individuals during the additive mortality period. A positive significant correlation between association strength and apparent survival suggested that the fitness of surviving individuals was impacted by the additive mortality event. After this event, individuals responded to the loss of relatives in their social groups by associating with a greater number of other social groups, likely to maintain a functional group size that maximized their foraging success. However, these associations were loose; individuals did not reassociate in highly stable social groups, and their survival remained low years after the mortality event. These findings demonstrate how the disruption of social structure in killer whales may lead to prolonged negative effects of demographic stress beyond an additive mortality event. More importantly, this study shows that sociality has a key role in the resilience of populations to human-induced mortality; this has major implications for the conservation of highly social and long-lived species.

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.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Behavioural heterogeneity across killer whale social units in their response to feeding opportunities from fisheries.

Intra-population heterogeneity in the behavioural response of predators to changes in prey availability caused by human activities can have major evolutionary implications. Among these activities, fisheries, while extracting resources, also provide new feeding opportunities for marine top predators. However, heterogeneity in the extent to which individuals have responded to these opportunities within populations is poorly understood. Here, we used 18 years of photo-identification data paired with statistical models to assess variation in the way killer whale social units within a subantarctic population (Crozet Islands) interact with fisheries to feed on fish caught on fishing gear (i.e., depredation behaviour). Our results indicate large heterogeneity in both the spatial and temporal extents of depredation across social units. While some frequently depredated on fishery catches over large areas, others sporadically did so and in small areas consistently over the years. These findings suggest that killer whale social units are exposed to varying levels of impacts of depredation, both negative (potential retaliation from fishers) and positive (food provisioning), on their life history traits, and may explain the contrasted demographic patterns observed within the declining population at Crozet but also potentially within the many other killer whale populations documented depredating on fisheries catches worldwide.

Using ecotourism boats for estimating the abundance of a bottlenose dolphin population in south-eastern Australia.

It is challenging to collect robust, long-term datasets to properly monitor the viability and social structure of large, long-lived animals, especially marine mammals. The present study used a unique long-term dataset to investigate the population parameters and social structure of a poorly studied population of bottlenose dolphins (Tursiops sp.) in southern Port Phillip Bay, south-eastern Australia. Photo-identification images have been collected between 2012-2022 both opportunistically and following a protocol by patrons, staff, and volunteers of ecotourism companies using their vessels as platforms. The resulting large dataset was available to be processed through the online platform Flukebook and used in capture recapture models to estimate abundance and demographic parameters. In addition, the social structure of the population and the reproductive parameters were investigated. The marked adult population abundance (45.2 ± 2.7 individuals) was found to be stable over the last decade and the calving rate ranged between 0.06-0.19 new calves per identified individuals per year, while the inter-birth interval was 3.7 ± 0.8 years. Social analysis suggested the population has a fission-fusion structure with no apparent clusters. The stability of the population over the study period suggests no deleterious effect of anthropogenic or environmental factors during the last decade. This study is the outcome of the effort of the ecotourism organisations and the results obtained, along with their similarity to those of other dolphin populations worldwide, highlight the importance of such data sources for long-term information that would otherwise be too expensive or logistically difficult to obtain.

Evidence of deep-sea interactions between toothed whales and longlines.

Toothed whales (odontocetes) feeding on fish caught on hooks in longline fisheries is a growing issue worldwide. The substantial impacts that this behaviour, called depredation, can have on the fishing economy, fish stocks and odontocetes populations, raise a critical need for mitigation solutions to be developed. However, information on when, where and how odontocete depredation occurs underwater is still limited, especially in demersal longline fisheries (fishing gear set on the seafloor). In the present study, we investigated depredation by killer whales (Orcinus orca) and sperm whales (Physeter macrocephalus) on demersal longlines in the French Patagonian toothfish fishery (Southern Ocean). Using a combination of animal-borne behavioural and longline-attached data loggers, we demonstrated that both species are able to depredate longlines on the seafloor. This study, therefore, suggests that odontocetes whales-longline interaction events at depth may be unrecorded when assessing depredation rates from surface observations during hauling phases only. This result has implications for the management of fisheries facing similar depredation issues as underestimated depredation rates may result in unaccounted fish mortality in fish-stock assessments. Therefore, while further research should be conducted to assess the extent of deep-sea whale-longline interaction events during soaking, the evidence that depredation can occur at any time during the whole fishing process as brought out by this study should be considered in future developments of mitigation solutions to the issue.

Commercial fishing patterns influence odontocete whale-longline interactions in the Southern Ocean.

The emergence of longline fishing around the world has been concomitant with an increase in depredation-interactions by odontocete whales (removal of fish caught on hooks), resulting in substantial socio-economic and ecological impacts. The extent, trends and underlying mechanisms driving these interactions remain poorly known. Using long-term (2003-2017) datasets from seven major Patagonian toothfish (Dissostichus eleginoides) longline fisheries, this study assessed the levels and inter-annual trends of sperm whale (Physeter macrocephalus) and/or killer whale (Orcinus orca) interactions as proportions of fishing time (days) and fishing area (spatial cells). The role of fishing patterns in explaining between-fisheries variations of probabilities of odontocete interactions was investigated. While interaction levels remained globally stable since the early 2000s, they varied greatly between fisheries from 0 to >50% of the fishing days and area. Interaction probabilities were influenced by the seasonal concentration of fishing effort, size of fishing areas, density of vessels, their mobility and the depth at which they operated. The results suggest that between-fisheries variations of interaction probabilities are largely explained by the extent to which vessels provide whales with opportunities for interactions. Determining the natural distribution of whales will, therefore, allow fishers to implement better strategies of spatio-temporal avoidance of depredation.

Killer whale (Orcinus orca) interactions with blue-eye trevalla (Hyperoglyphe antarctica) longline fisheries.

Over the past five decades, marine mammal interactions with fisheries have become a major human-wildlife conflict globally. The emergence of longline fishing is concomitant with the development of depredation-type interactions i.e., marine mammals feeding on fish caught on hooks. The killer whale (Orcinus orca) is one of the species most involved in depredation on longline fisheries. The issue was first reported in high latitudes but, with increasing expansion of this fishing method, other fisheries have begun to experience interactions. The present study investigated killer whale interactions with two geographically isolated blue-eye trevalla (Hyperoglyphe antarctica) fisheries operating in temperate waters off Amsterdam/St. Paul Islands (Indian Ocean) and south-eastern Australia. These two fisheries differ in the fishing technique used (vertical vs. demersal longlines), effort, catch, fleet size and fishing area size. Using 7-year (2010-16) long fishing and observation datasets, this study estimated the levels of killer whale interactions and examined the influence of spatio-temporal and operational variables on the probability of vessels to experience interactions. Killer whales interactions occurred during 58.4% and 21.2% of all fishing days, and over 94% and 47.4% of the fishing area for both fisheries, respectively. In south-eastern Australia, the probability of occurrence of killer whale interactions during fishing days varied seasonally with a decrease in spring, increased with the daily fishing effort and decreased with the distance travelled by the vessel between fishing days. In Amsterdam/St. Paul, this probability was only influenced by latitude, with an increase in the southern part of the area. Together, these findings document two previously unreported cases of high killer whale depredation, and provide insights on ways to avoid the issue. The study also emphasizes the need to further examine the local characteristics of fisheries and the ecology of local depredating killer whale populations in as important drivers of depredation.