First circumglobal assessment of Southern Hemisphere humpback whale mitochondrial genetic variation and implications for management

Abstract

The description of genetic population structure over a species' geographic range can provide insights into its evolutionary history and also support effective management efforts. Assessments for globally distributed species are rare, however, requiring significant international coordination and collaboration. The global distribution of demographically discrete populations for the humpback whale Megaptera novaeangliae is not fully known, hampering the definition of appropriate management units. Here, we present the first circumglobal assessment of mitochondrial genetic population structure across the species' range in the Southern Hemisphere and Arabian Sea. We combine new and existing data from the mitochondrial (mt)DNA control region that resulted in a 311 bp consensus sequence of the mtDNA control region for 3009 individuals sampled across 14 breeding stocks and subpopulations currently recognized by the International Whaling Commission. We assess genetic diversity and test for genetic differentiation and also estimate the magnitude and directionality of historic matrilineal gene flow between putative populations. Our results indicate that maternally directed site fidelity drives significant genetic population structure between breeding stocks within ocean basins. However, patterns of connectivity differ across the circumpolar range, possibly as a result of differences in the extent of longitudinal movements on feeding areas. The number of population comparisons observed to be significantly differentiated were found to diminish at the subpopulation scale when nucleotide differences were examined, indicating that more complex processes underlie genetic structure at this scale. It is crucial that these complexities and uncertainties are afforded greater consideration in management and regulatory efforts.

Feeding ecology and population delineation of south‐eastern Atlantic and south‐western Indian Ocean humpback whales using stable isotope analysis

“…Whales sampled from the breeding area off Gabon in the Gulf of Guinea (BSB1) exhibit relatively higher levels of genetic differentiation on feeding areas, and analyses support that the westward Margin and Nucleus areas for BSB do appear to represent the primary feeding areas for this breeding stock, as currently hypothesized under AH1 (Amaral et al, ; IWC, ; Kershaw, ). In contrast, whales observed migrating past and feeding off western South Africa (BSB2) and the substocks of BSC in the western Indian Ocean show relatively high levels of mixing across feeding areas (Kershaw, ), mirroring the high levels of connectivity previously observed between the corresponding breeding areas for these substocks (Best et al, ; Carvalho, Brito, dos Santos, & Rosenbaum, ; Cerchio et al, ; Ersts et al, ; Fossette et al, ; Kershaw et al, ; Rosenbaum et al, ; Rosenbaum et al, ). BSC is broadly associated with Management Area III (Amaral et al, ), and assessments of population structure show that BSC1–BSC3 exhibit significant genetic differentiation from the BSB Nucleus feeding area but not the BSB/BSC Margin or BSC Nucleus (IWC, ).…”

“…There are seven genetically distinct ‘breeding stocks’ (termed BSA to BSG) of humpback whales managed by the International Whaling Commission (IWC) in the Southern Hemisphere (IWC, ; Rosenbaum et al, ). Table defines all breeding stocks worldwide.…”

“…Nucleus and Margin feeding areas as denoted by the International Whaling Commission under Allocation Hypothesis 1 (AH1) are labelled for the map area. Views of the wider breeding stock structure can be found in Rosenbaum et al ()…”

“…Resolving gaps in knowledge of the distribution of breeding stocks on feeding areas has direct relevance for informing estimates of pre‐exploitation sizes and assessments of recovery of the species from whaling. These uncertainties regarding the delineation of humpback whale populations preclude a robust recovery assessment for all regions (Rosenbaum et al, ).…”

Distribution of breeding humpback whale habitats and overlap with cumulative anthropogenic impacts in the Eastern Tropical Atlantic

“…Humpback whales utilizing breeding areas off Gabon and Congo are termed “Breeding Substock B1” (“BSB1”), and those observed migrating and occasionally feeding off west South Africa and Namibia are termed “Breeding Substock B2” (“BSB2”) (Barendse, Best, Carvalho, & Pomilla, ; Findlay et al, ; IWC, ; Kershaw et al, ; Rosenbaum et al, , ). The breeding area for BSB2 is currently unknown (Barendse et al, 2013; Rosenbaum et al, ). The genetic distinctiveness of BSB1 is considered high, with individuals returning to the same relatively well‐known breeding areas off Gabon and Congo each year.…”