Our study helps refine knowledge of population structure in the Antarctic blue whale, B. m. intermedia. A Bayesian clustering assignment method based on microsatellite DNA provided evidence that three genetically differentiated populations occur sympatrically off Antarctica during the austral summer feeding season. For simplicity, these are henceforth referred to as populations. The levels of differentiation were low and similar between the populations and consistent between analyses of microsatellites and the mtDNA control region. Genetic variation based on microsatellites and the mtDNA control region was similar in the three populations.

Previous studies were unable to detect the multiple, sympatric populations of Antarctic blue whales, even though they also used the same standard Bayesian clustering method40,42,43. This is because of either smaller sample sizes, smaller number of markers, not specifically investigating population structure within the Antarctic subspecies, or a combination of these. Fixation indices, which require a priori putative populations, have previously40 and in the current study detected genetic differentiation between some IWC management Areas. Given the results of the current study for analyses that do not require a priori groupings, this genetic differentiation between Areas could be due to different proportions of the populations in different management Areas.

The only longitudinal range where the proportion of different populations can be accurately assessed is between 0° and 20°E since 57% of samples were from this area. Here, there is an almost equal ratio of individuals from each population (number of samples from population 1 = 25, population 2 = 26, population 3 = 30). In contrast, in the Pacific Ocean basin sector there is perhaps greater proportions of populations 1 and 2 compared with population 3 as only three of the 26 individuals there were identified as belonging to population 3 and these had low memberships (estimated in STRUCTURE) to population 3 of 0.547 to 0.597 inclusive. These individuals and others with relatively low membership to their assigned population may have admixed ancestry to multiple populations43; in other words, they may have immediate ancestors (e.g. parents, grandparents) from different populations. An alternative explanation for low membership is insufficient power for accurate assignment given the low levels of population differentiation.

The movement data available for Antarctic blue whales corroborate the current study’s findings. They show large-scale movements off Antarctica – including movements that cross IWC management Areas and ocean basins – as well as small-scale movements. The data are from a wide range of methodologies and are across a wide time span: Discovery marks deployed from the 1934/35 to 1962/63 season and recaptured until the 1966/67 season33, photo-identifications from the 1987/88 to 2014/15 season34,35,36,37, Olson pers. comm. and satellite tagging and tracking within the 2012/13 season38 (Table 3). Longitudinal movements around the Antarctic require less travelling due to the high latitudes than the same amount of longitudinal movement at low latitudes, allowing the blue whales to move relatively easily between longitudes when in the Antarctic. The geographic distance was typically closer for intra-seasonal recaptures compared with inter-seasonal recaptures, though inter-seasonal recaptures still included small-scale movements33,35. The small-scale movements indicate site fidelity and the potential for different proportions of populations in different areas and the large-scale movements indicate the potential for sympatry of populations.

Table 3 Summary of movement data for Antarctic blue whales generated by previous studies through Discovery marking, photo-identification and satellite tagging. Full size table

The individual whales likely move depending on the densities of their prey due to their high energetic requirements as the largest extant animal44. Blue whales are specialist predators that feed on krill (order Euphausiacea). The Antarctic has high biological productivity, including Antarctic krill (Euphausia superba)45, due to the Antarctic Circumpolar Current generating upwelling and circumpolar fronts46. In the summer feeding season the Antarctic blue whales are generally south of the Antarctic Polar Front (also known as the Antarctic Convergence)33, a region associated with particularly high biological productivity47 and where blue whales feed on Antarctic krill48. The distribution and density of Antarctic krill changes within and between seasons depending on environmental conditions49, requiring marine predators, such as blue whales, to move to find sufficient amounts of their prey e.g.50,51,52. Such dependence is particularly important to consider given evidence of changes in Antarctic krill demographics due to recent climate change53,54. The dependence of blue whales on high concentrations of krill may also occur outside their feeding grounds33,55,56, unlike traditional thinking that baleen whales fast during migration and at breeding grounds. This means the specific locations of Antarctic blue whale breeding grounds may be influenced by the location and abundance of krill during the austral winter.

The exact breeding ground locations of Antarctic blue whales are unknown. One possibility is that populations breed at different ocean basins. This means that populations would be physically separated by the continental land masses of South America, Africa and Australia during the austral winter breeding season. It has long been suggested that at least one Antarctic population breeds in each of these physically separated regions57. Acoustic recordings of Antarctic blue whale calls in the austral winter indicate their breeding grounds include low latitudes of the Indian Ocean and eastern Pacific Ocean58,59. Their breeding grounds may also include low latitudes of the South Atlantic Ocean, with perhaps no recordings of their calls in that basin due to insufficient effort39. For example, the Atlantic Ocean region off south-west Africa has been suggested as a breeding location based on seasonality of Antarctic blue whale historical catches in south-west Africa24,33. However, since whaling there have been only two recorded blue whale sightings off that coast33. There is also a paucity of data on the population structure of other Antarctic baleen whales. There is evidence that populations of humpback whales (Megaptera novaeangliae) – arguably the most well-understood Antarctic baleen whale – have discrete distributions in the Antarctic, with overlap in the distribution of some populations60. They are thought to breed at lower latitudes segregated across the three ocean basins, but also with multiple populations breeding discretely in each ocean basin60. The Antarctic minke whale (B. bonaerensis) may also have a similar pattern of discrete population distributions in the Antarctic with some overlap61. Outside the Antarctic there is evidence of populations in sympatry at feeding grounds. The common minke whale (B. acutorostrata) appears to have complete sympatry on feeding grounds in the North Atlantic62.

It is also possible that at least one population of Antarctic blue whales is resident in the Antarctic throughout the year. A resident population may follow the ice edge as it expands northwards in the austral winter and recedes in the austral summer. This is suggested by year-round acoustic detections of the Antarctic subspecies off the western coast of the Western Antarctic Peninsula63,64 and off eastern Antarctica at 67°S, 70°E64. Antarctic blue whales have also been recorded year-round off the Crozet Islands59,65 based on acoustics and off the sub-Antarctic island of South Georgia based on whaling catch data33. Blue whales of other subspecies have also been recorded at some localities year-round59,65,66,67,68 and other baleen whale species have been recorded in the Antarctic69,70,71 and other locations72,73,74,75 year-round. Some of these are likely to be resident populations72,73.

Another explanation for year-round presence at a feeding ground is overlapping timing of departures and arrivals. This overlap could be mediated by temporal segregation of migration based on age, sex, reproductive state, or migratory destination, as is thought for humpback whales76,77. Alternatively, a proportion of a population or populations may remain at the feeding grounds year-round. These could be individuals that are sexually or physically immature, or as also suggested for humpback whales78, mature females that are currently not breeding. Sexual maturity in blue whales is only reached at 10 years and physical maturity afterwards79,80,81. Female blue whales are not thought to breed each season as they have a two to three year inter-calf interval, gestation lasting at least 10 months, weaning lasting seven months and simultaneous pregnancy and lactation is rare80,81. However, the vocalizations that are geographically distinct in blue whales and appear as songs are likely only produced by males17,18 and the distinct Antarctic blue whale vocalization was used to report the year-round presence of blue whales in the Antarctic63,64. This means males are present year-round, with or without females.

It is possible that whaling has influenced the population structure detected here. Exploitation can lead to the formation or loss of populations, or for the level of genetic differentiation between populations to increase or decrease82. This can be due to increased genetic drift and associated loss of variation and increased genetic differentiation and changes in the degree of gene flow between populations. Ideally, a sufficient number of pre-whaling samples from the same locations as the current samples should be used to determine if the population structure of blue whales has changed due to human impacts83, but such samples are not available in the present study. However, the most likely pre-whaling scenarios of blue whale populations can be inferred based on non-genetic data and the biology of this species. It is likely that there were multiple populations of Antarctic blue whales before whaling. While there are different possibilities regarding the breeding ground locations of Antarctic blue whales, acoustic and whaling catch data indicate that they include different ocean basins24,33,58,59. This would promote the formation of different populations, as seen in humpback whales60, because land barriers between ocean basins would hinder movement between breeding grounds. Philopatry to basins may be mediated by maternally-directed cultural learning of migratory routes and destinations, which makes population-level conservation particularly imperative as extirpation of a population could result in no re-colonization of the associated breeding ground84. In addition, it is likely that Antarctic blue whale populations were sympatric in the Antarctic before whaling. This is because there are no obvious differences in the pattern of blue whale movements in the Antarctic according to Discovery mark33 and photo-identification34,35,36,37 datasets, which together span from the 1934/35 to 2014/15 season. The non-genetic data therefore indicate that different populations likely existed within Antarctic blue whales before whaling and these were sympatric in the Antarctic.

The current level of gene flow between populations may be greater than that prior to whaling, which could account for the low level of genetic differentiation and evidence of admixture found in the current study. Increased gene flow may occur because individuals need to travel further afield to find mates given that the number of Antarctic blue whales reduced from 239,000 to 360 individuals due to whaling26. Indeed, hybridization between the Antarctic blue whale and pygmy blue whale subspecies may have begun occurring or increased in occurrence within the last four decades due to whaling or climate change43. Although, there may have always been high levels of gene flow between the Antarctic populations. The low differentiation can otherwise be explained by the Antarctic populations being founded relatively recently (but still prior to whaling) on an evolutionary timescale, which is unlikely given evidence that Antarctic blue whales are the ancestral subspecies of blue whales in the Southern Hemisphere85. It is also unlikely that whaling has caused an increase in population differentiation through genetic drift because increased genetic drift has not yet existed for long enough to have a major effect; blue whales are long-lived with a generation time of 31 years86 and Antarctic blue whales were hunted from the 1904/05 to 1972/73 season, so the populations have only had a reduced size for about three to four generations.

Locating the breeding grounds of blue whales feeding off Antarctica is needed to confirm their current population structure. The biopsy samples used in the current study and the raw data for much of the discussed post-whaling Antarctic blue whale research, including photo-identifications34,35,36,37, abundance estimates26,27, past genetic research40,42,43 and satellite tagging38, were collected through international, collaborative vessel surveys in the Antarctic. The breeding grounds of Antarctic blue whales would ideally be located through continuing collaborative efforts to satellite tag Antarctic blue whales while they are feeding and tracking their subsequent movements38. Despite current longevity issues12, there has been much success in using tags to determine movements and migratory destinations87,88 and to assess inter-year and individual variation when enough tags are deployed55. In addition, tags continue to be improved to increase their longevity12,13. Subsequent genetic samples from breeding grounds would allow confirmatory genetic structure analyses with biologically reasonable a priori groupings and a baseline for comparative genetic analyses of samples collected off Antarctica. Monitoring each population’s abundance would then need to be performed at their breeding grounds. Monitoring is needed because the populations may differ in pre- and post-whaling abundance and recovery trends, especially because they occupy different migratory routes and breeding grounds with likely different carrying capacities and anthropogenic threats.