Genomic evidence for homoploid hybrid speciation in a marine mammal apex predator.

Hybridization is widespread and constitutes an important source of genetic variability and evolution. In animals, its role in generating novel and independent lineages (hybrid speciation) has been strongly debated, with only a few cases supported by genomic data. The South American fur seal (SAfs) Arctocephalus australis is a marine apex predator of Pacific and Atlantic waters, with a disjunct set of populations in Peru and Northern Chile [Peruvian fur seal (Pfs)] with controversial taxonomic status. We demonstrate, using complete genome and reduced representation sequencing, that the Pfs is a genetically distinct species with an admixed genome that originated from hybridization between the SAfs and the Galapagos fur seal (Arctocephalus galapagoensis) ~400,000 years ago. Our results strongly support the origin of Pfs by homoploid hybrid speciation over alternative introgression scenarios. This study highlights the role of hybridization in promoting species-level biodiversity in large vertebrates.

Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere.

The phylogeny and systematics of fur seals and sea lions (Otariidae) have long been studied with diverse data types, including an increasing amount of molecular data. However, only a few phylogenetic relationships have reached acceptance because of strong gene-tree species tree discordance. Divergence times estimates in the group also vary largely between studies. These uncertainties impeded the understanding of the biogeographical history of the group, such as when and how trans-equatorial dispersal and subsequent speciation events occurred. Here, we used high-coverage genome-wide sequencing for 14 of the 15 species of Otariidae to elucidate the phylogeny of the family and its bearing on the taxonomy and biogeographical history. Despite extreme topological discordance among gene trees, we found a fully supported species tree that agrees with the few well-accepted relationships and establishes monophyly of the genus Arctocephalus. Our data support a relatively recent trans-hemispheric dispersal at the base of a southern clade, which rapidly diversified into six major lineages between 3 and 2.5 Ma. Otaria diverged first, followed by Phocarctos and then four major lineages within Arctocephalus. However, we found Zalophus to be nonmonophyletic, with California (Zalophus californianus) and Steller sea lions (Eumetopias jubatus) grouping closer than the Galapagos sea lion (Zalophus wollebaeki) with evidence for introgression between the two genera. Overall, the high degree of genealogical discordance was best explained by incomplete lineage sorting resulting from quasi-simultaneous speciation within the southern clade with introgresssion playing a subordinate role in explaining the incongruence among and within prior phylogenetic studies of the family. [Hybridization; ILS; phylogenomics; Pleistocene; Pliocene; monophyly.].

Divergent allele advantage at MHC-DRB through direct and maternal genotypic effects and its consequences for allele pool composition and mating.

It is still debated whether main individual fitness differences in natural populations can be attributed to genome-wide effects or to particular loci of outstanding functional importance such as the major histocompatibility complex (MHC). In a long-term monitoring project on Galápagos sea lions (Zalophus wollebaeki), we collected comprehensive fitness and mating data for a total of 506 individuals. Controlling for genome-wide inbreeding, we find strong associations between the MHC locus and nearly all fitness traits. The effect was mainly attributable to MHC sequence divergence and could be decomposed into contributions of own and maternal genotypes. In consequence, the population seems to have evolved a pool of highly divergent alleles conveying near-optimal MHC divergence even by random mating. Our results demonstrate that a single locus can significantly contribute to fitness in the wild and provide conclusive evidence for the 'divergent allele advantage' hypothesis, a special form of balancing selection with interesting evolutionary implications.

Male reproductive success and its behavioural correlates in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki).

Sexual selection theory predicts competitive males and choosy females. Nevertheless, since molecular marker-based studies, paternity outside the expected mating patterns has increasingly been described. Even in highly polygynous systems, where paternity is expected to be strongly skewed towards large, dominant males, alternative mating tactics have been suggested. We examined reproductive success in the polygynous Galápagos sea lion (Zalophus wollebaeki). Semiaquatic territoriality allows females to move freely and may lower the degree of polygyny otherwise suggested by both territorial behaviour and strong sexual dimorphism. We assigned paternities with 22 microsatellites and analysed how male reproductive success was related to size, dominance status, intra-sexual agonistic behaviour, proximity to females, and attendance in the colony. Male behaviour was consistent across two seasons for all parameters under consideration. Attendance was by far the most important determinant of paternal success. Skew in reproductive success towards large, dominant males was weak and dominance status played no role. This appears to be caused by an extremely long reproductive season lasting five or more months, making it difficult for any male to monopolize receptive females. Females seem to choose displaying males that were present in the colony for a long time rather than dominance per se. Sexual dimorphism in Galápagos sea lions may thus be more influenced by selection for fasting than fighting ability. Our data provide further evidence for alternative mating tactics, as several males gained relatively high reproductive success despite short attendance and hardly any involvement in agonistic interactions.

Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations.

BACKGROUND: Oceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation. RESULTS: We find significant ecological, morphological and genetic divergence between the western colonies and colonies from the central region of the archipelago that are exposed to different ecological conditions. Stable isotope analyses indicate that western animals use different food sources than those from the central area. This is likely due to niche partitioning with the second Galápagos eared seal species, the Galápagos fur seal (Arctocephalus galapagoensis) that exclusively dwells in the west. Stable isotope patterns correlate with significant differences in foraging-related skull morphology. Analyses of mitochondrial sequences as well as microsatellites reveal signs of initial genetic differentiation. CONCLUSION: Our results suggest a key role of intra- as well as inter-specific niche segregation in the evolution of genetic structure among populations of a highly mobile species under conditions of free movement. Given the monophyletic arrival of the sea lions on the archipelago, our study challenges the view that geographical barriers are strictly needed for the build-up of genetic divergence. The study further raises the interesting prospect that in social, colonially breeding mammals additional forces, such as social structure or feeding traditions, might bear on the genetic partitioning of populations.

Beyond habitat requirements: individual fine-scale site fidelity in a colony of the Galapagos sea lion (Zalophus wollebaeki) creates conditions for social structuring.

Site fidelity has been widely discussed, but rarely been related explicitly to a species' social context. This is surprising, as fine-scale site fidelity constitutes an important structural component in animal societies by setting limits to an individual's social interaction space. The study of fine-scale site fidelity is complicated by the fact that it is inextricably linked to patterns of habitat use. We here document fine-scale site fidelity in the Galapagos sea lion (Zalophus wollebaeki) striving to disentangle these two aspects of spatial behaviour. Regardless of sex and age, all individuals used small, cohesive home ranges, which were stable in size across the reproductive and non-reproductive season. Home ranges showed a large individual component and did not primarily reflect age- or sex-specific habitat requirements. Site specificity could be illustrated up to a resolution of several metres. Long-term site fidelity was indicated by home range persistence over 3 years and the degree of site fidelity was unaffected by habitat, but showed seasonal differences: it was lower between reproductive and non-reproductive periods than between reproductive seasons. We further examined static and social interaction within mother-offspring pairs, which constitute a central social unit in most mammalian societies. Regardless of the occupied habitat type, adult females with offspring had smaller home range sizes than non-breeding females, demonstrating the importance of spatial predictability for mother-offspring pairs that recurrently have to reunite after females' foraging sojourns. While social interaction with the mother dropped to naught in both sexes after weaning, analysis of static interaction suggested female-biased home range inheritance. Dispersal decisions were apparently not based on habitat quality, but determined by the offspring's sex. We discuss the implication of observed fine-scale site fidelity patterns on habitat use, dispersal decisions and social structure in colonial breeding pinnipeds.