A global cline in a colour polymorphism suggests a limited contribution of gene flow towards the recovery of a heavily exploited marine mammal

Abstract

Evaluating how populations are connected by migration is important for understanding species resilience because gene flow can facilitate recovery from demographic declines. We therefore investigated the extent to which migration may have contributed to the global recovery of the Antarctic fur seal (Arctocephalus gazella), a circumpolar distributed marine mammal that was brought to the brink of extinction by the sealing industry in the eighteenth and nineteenth centuries. It is widely believed that animals emigrating from South Georgia, where a relict population escaped sealing, contributed to the re-establishment of formerly occupied breeding colonies across the geographical range of the species. To investigate this, we interrogated a genetic polymorphism (S291F) in the melanocortin 1 receptor gene, which is responsible for a cream-coloured phenotype that is relatively abundant at South Georgia and which appears to have recently spread to localities as far afield as Marion Island in the sub-Antarctic Indian Ocean. By sequencing a short region of this gene in 1492 pups from eight breeding colonies, we showed that S291F frequency rapidly declines with increasing geographical distance from South Georgia, consistent with locally restricted gene flow from South Georgia mainly to the South Shetland Islands and Bouvetøya. The S291F allele was not detected farther afield, suggesting that although emigrants from South Georgia may have been locally important, they are unlikely to have played a major role in the recovery of geographically more distant populations.

The genetic legacy of extreme exploitation in a polar vertebrate

“…It is conceivable that some juveniles, subadults and non-breeders could have escaped the sealers by not coming ashore. However, if this were the case, relict populations should have survived at all of the breeding grounds, whereas our data, together with recent studies and historical accounts, suggest that that Antarctic fur seals may have been locally extirpated at Macquarie, Heard, Crozet and Marion Islands 47,50,51 . We therefore speculate that tiny remnants of once much larger breeding populations may have persisted in a handful of particularly inaccessible locations that were rarely if ever visited by sealers.…”

“…As breeding www.nature.com/scientificreports www.nature.com/scientificreports/ populations were not observed at the other sub-Antarctic islands until the 1950s to the 1980s [39][40][41][42][43][44] , several authors have speculated that the former geographic distribution of this species was likely recolonized from South Georgia 28,38,[45][46][47] . However, a number of studies have reported genetic differences among some of these populations [48][49][50][51] , pointing towards a more complex picture in which more than one relict population may have survived sealing.…”

Antarctic fur seal (Arctocephalus gazella) annual migration and temporal patterns of on-shore occurrence of leucistic individuals on King George Island

“…Also, the records of leucistic individuals over the period under investigation enabled us to find the tendency for the increase in the number of leucistic animals in the successive years although the total population remained unchanged. First incidence of a leucistic individual was noted in 1933 for the population of South Georgia (Bonner 1968) and leucistic animals are relatively prevalent there (Hofmeyr et al 2005), which might be a result of a strong historical bottleneck (Hoffman et al 2011(Hoffman et al , 2018. Leucistic animals were also observed in the South Shetlands, Bouvetøya and Marion Island (Hofmeyr et al 2005;Wege et al 2015), Îles Kerguelen, Macquarie Island, Îles Crozet and Heard Island (Hoffman et al 2018).…”

“…First incidence of a leucistic individual was noted in 1933 for the population of South Georgia (Bonner 1968) and leucistic animals are relatively prevalent there (Hofmeyr et al 2005), which might be a result of a strong historical bottleneck (Hoffman et al 2011(Hoffman et al , 2018. Leucistic animals were also observed in the South Shetlands, Bouvetøya and Marion Island (Hofmeyr et al 2005;Wege et al 2015), Îles Kerguelen, Macquarie Island, Îles Crozet and Heard Island (Hoffman et al 2018). Analysis of the polymorphism in the melanocortin 1 receptor gene, responsible for cream-coloured phenotype in fur seals, indicates a global cline in the frequency of colour polymorphism and suggests a limited contribution of gene flow between South Georgia and other populations (Hoffman et al 2018).…”

“…At the turn of the Nineteenth and Twentieth Centuries, due to intensive commercial sealing the population of Antarctic fur seal Arctocephalus gazella (Peters 1875) in South Georgia and South Shetlands was brought to the brink of extinction (Weddell 1825;Bonner 1968). The current number of Antarctic fur seal population was estimated at 4.5-6.2 million individuals (Hofmeyr 2016), with 97% of individuals observed in South Georgia (Hoffman et al 2018). In the South Shetlands, only Livingston Island and Elephant Island are locations of established breeding colonies of Antarctic fur seals (Bengtson et al 1990;Reid et al 2006), whilst on King George Island non-breeding males haul out during the moulting season (Sierakowski 1991;Salwicka and Rakusa-Suszczewski 2002;Korczak-Abshire et al 2019).…”