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Phylogenetic relationships, population genetics and hybridisation of two species of southern fur seal (Arctocephalus spp.)

Wynen, LP 2002 , 'Phylogenetic relationships, population genetics and hybridisation of two species of southern fur seal (Arctocephalus spp.)', PhD thesis, University of Tasmania.

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This research investigated the phylogenetic relationships and population genetics of two species of fur seal in order to provide a basis for the study of the hybridisation of these species at Macquarie Island. The Antarctic (Arctocephalus gaze/la) and subantarctic fur seals (Arctocepha/us tropicalis) occur throughout the subantarctic region of the Southern Ocean, hauling out on remote islands throughout the region to breed. Both species were subject to intense sealing activities in the 18th and 19th centuries. The competitive and indiscriminate nature of the industry ensured that all populations were greatly reduced in size, with some becoming extinct. The cessation of sealing in the early 20th century has allowed both species to recover in number, and recolonise islands across their former range. The current range for the Antarctic fur seal overlaps with that of the subantarctic fur seal at lies Crozet, Marion Island and Macquarie Island. Hybridisation has been reported at low levels at Marion Island, and at higher levels at Macquarie Island. The situation at Macquarie Island is further complicated by the presence of an additional species, the New Zealand fur seal (Arctocephalus forsteri) While this species is not breeding on the island, some males participate in the breeding process, with some hybrids being produced This research seeks to apply molecular methods to investigate the hybridisation that is occurring at Macquarie Island within the context of the evolutionary and recent history of the two breeding fur seal species, and to a lesser extent, the New Zealand fur seal.
The phylogenetic relationships of the Antarctic and subantarctic fur seals were investigated within the context of the family Otariidae. This family include the nine species of fur seal (Genera Arctocephalus and Callorhinus), and five species of sea lion (Genera Neophoca, Phocarctos, Eumetopias, Zalophus, and Otaria). A 360 base pair region of the cytochrome b gene in the maternally inherited mitochondrial genome was used for the primary phylogenetic analysis of the family, while a 356 base pair fragment of the mitochondrial control region was used to enhance resolution of the terminal nodes. The traditional classification of the family into the two. subfamilies Arctocephalinae (fur seals) and Otariinae (sea lioris) was not supported, as the fur seal Cal/orhinus ursinus was found to be basal to all other fur seal and sea lion taxa. While four sea lion clades and five fur seal clades were consistently observed through all analyses conducted, it was not possible to adequately resolve the relationships among these clades. This probably reflects the rapid radiation of these taxa that occurred about 3 million years ago. The subantarctic fur seal was found to be most closely related to the Australian and Cape fur seals (A. pusillus) while the closest species related to the Antarctic fur seal was not clearly resolved. However, there were discrete species specific differences observed between the Antarctic, subantarctic and New Zealand fur seals in both the cytochrome b gene and the control region, providing the basis for species identification within the hybridising population at Macquarie Island.
The investigation into the level and distribution of genetic variation in the Antarctic and subantarctic fur seals was conducted using two classes of molecular marker. The mitochondrial control region is a commonly used marker for investigation into population genetics issues, due in part to the relatively high rate of mutation. Microsatellites are highly variable regions within the nuclear genome, and with a bi-parental mode of inheritance, provide a natural complement to the maternally inherited mitochondrial genes. Given that historic records indicate both fur seal species had passed through population bottlenecks as a result of sealing, it was suspected that the current level of genetic variation may be low. This is because reduced levels of variation have been observed in other species that have passed through extreme population bottlenecks at some stage in the recent past (eg. the northern elephant seal, Mirounga angustirostris). Surprisingly, the nucleotide diversities of the Antarctic and subantarctic fur seals, as determined by the mitochondrial control region, were found to be high (3.2% and 4.8% respectively). The level of genetic variation as exhibited by the 10 microsatellite loci was generally high (overall heterozygosity levels 0.54-0.62 for the three species), though variable between loci. Despite the overlapping allele size ranges for most of the loci, significant allelic and genotypic differentiation was observed between the three species (P < 0.000). Significant population structure was evident within the subantarctic fur seal with both the mitochondrial (<PsT=0.19) and microsatellite DNA (unbiased RsT=0.122; P<<0.001 ). Population pairwise comparisons among subantarctic fur seals, suggest gene flow from Gough Island in the South Atlantic eastwards to Marion Island and lies Amsterdam, and from Marion Island in the South Indian Ocean eastwards to the recolonised population at lies Crozet. Less population structure was evident within the Antarctic fur seal based on mitochondrial DNA (<PsT =0.074), but two genetically differentiated regions were recognised. In contrast, no genetic heterogeneity was observed with microsatellite DNA (unbiased RsT=0.003; P=0.501 ), suggesting panmixia despite the large geographic range of the species. Overall, less structure was evident with microsatellite DNA compared with mtDNA data for both species. This could be due to there being a greater effective population size for microsatellites compared with mitochondrial DNA, or the results may reflect the greater male mediated dispersal reported in fur seals. In any case, both markers indicate that the recolonisation of Macquarie Island is most likely to have originated from lies Kerguelen for the Antarctic fur seals, and Marion Island and lie Amsterdam for the subantarctic fur seals.
The presence of three fur seal species and their hybrids within the Macquarie Island population renders the identification of individuals to species problematic. The extent of hybridisation was initially investigated within a single cohort of pups (n=130), through the comparison of mitochondrial and microsatellite DNA methods developed in previous chapters, with a number of field-based methods The latter group include: the 'Overall Phenotype' method, where the investigator considers traits such as external appearance, behaviour, and vocalisations in providing an overall picture of the individual; and the 'Phenotype Score' method, where a prescribed set of phenotype traits are scored in an objective manner for each individual. This study also aimed to investigate the direction of hybridisation by comparing the incidence within the pup population with that observed in the breeding population of males and females. The two phenotype-based methods found that the incidence of hybridisation within the cohort ranged from 5.5% to 7.7%. The molecular methods relied on comparing the genotypes of all pups with a reference data set of the species, either with an assignment test or by eye. The assignment test method was easy to use, but was unable to categorically assign individuals to a hybrid class in an objective manner. If a subjective variation of the test is used, then the estimated level of hybridisation was found to be 18.4%. This is lower than the estimate obtained when assessing the genotypes by eye, which was 30.4%. While the phenotype-based methods had a high success rate in classifying individuals to the correct species (75.8% to 70.9%), they severely underestimated the number of hybrids in the population. The incidence of hybridisation within the pup cohort was much greater than observed in the breeding female population (17.5%), but much less than was observed in the breeding male population (48.5%). If the males are grouped as territorial males and challenger males, it can be seen that the proportion of hybrids w1th1n each class also differs (58.8% and 37.5% respectively).
The study of the Antarctic and subantarctic fur seals in the light of their evolutionary relationships, combined with an investigation into the levels and distribution of genetic variation in the context of their recent hist~ry, has laid the ground work for a comprehensive examination of hybridisation at Macquarie Island. However, there are still many questions remaining, and a longitudinal study adopting a holistic approach (encompassing molecular data, field observations, morphological measurements, and the study of pre- and post-mating isolating systems) is required to understand the longer term implications of hybridisation in this population.

Item Type: Thesis - PhD
Authors/Creators:Wynen, LP
Keywords: Southern fur seals, Southern fur seals
Additional Information:

Chapter 2 appears to be the equivalent of a post-print version of an article published as: Wynen, L. P., Goldsworthy, S. D., Insley, S. J. et al., 2001. Phylogenetic relationships within the eared seals (Otariidae: Carnivora): implications for the historical biogeography of the family, Molecular phylogenetics and evolution, 21(2), 270-284

Chapter 3 appears to be the equivalent of the peer reviewed version of the following article: Wynen, L. P., Goldsworthy, S. D., Guinet, C., Bester, M. N., Boyd, I. L., Gjertz, I., Hofmeyr, G. J. G., White, R. W. G., Slade, R., (2000). Postsealing genetic variation and population structure of two species of fur seal (Arctocephalus gazella and A. tropicalis), Molecular ecology, 9(3), 299–314, which has been published in final form at This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

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