History of Diversification and Adaptation from North to South Revealed by Genomic Data: Guanacos from the Desert to Sub-Antarctica.

The increased availability of quality genomic data has greatly improved the scope and resolution of our understanding of the recent evolutionary history of wild species adapted to extreme environments and their susceptibility to anthropogenic impacts. The guanaco (Lama guanicoe), the largest wild ungulate in South America, is a good example. The guanaco is well adapted to a wide range of habitats, including the Sechura Desert, the high Andes Mountains to the north, and the extreme temperatures and conditions of Navarino Island to the south. Guanacos also have a long history of overexploitation by humans. To assess the evolutionary impact of these challenging habitats on the genomic diversity, we analyzed 38 genomes (∼10 to 16×) throughout their extensive latitudinal distribution from the Sechura and Atacama Desert to southward into Tierra del Fuego Island. These included analyses of patterns of unique differentiation in the north and geographic region further south with admixture among L. g. cacsilensis and L. g. guanicoe. Our findings provide new insights on the divergence of the subspecies ∼800,000 yr BP and document two divergent demographic trajectories and to the initial expansion of guanaco into the more southern portions of the Atacama Desert. Patagonian guanacos have experienced contemporary reductions in effective population sizes, likely the consequence of anthropogenic impacts. The lowest levels of genetic diversity corresponded to their northern and western limits of distribution and some varying degrees of genetic differentiation. Adaptive genomic diversity was strongly linked with environmental variables and was linked with colonization toward the south followed by adaptation.

Genome-wide analyses reveal drivers of penguin diversification.

Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and that Aptenodytes is the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (Ne ) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increased Ne between 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.

Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird.

Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depend on the local pathogen composition, which is in turn determined by biotic and abiotic features of the environment. However, little is known about adaptation to local pathogen threats in wild animals. The Gentoo penguin (Pygoscelis papua) is a species complex that lends itself to the study of immune adaptation because of its circumpolar distribution over a large latitudinal range, with little or no admixture between different clades. In this study, we examine the diversity in a key family of innate immune genes-the Toll-like receptors (TLRs)-across the range of the Gentoo penguin. The three TLRs that we investigated present varying levels of diversity, with TLR4 and TLR5 greatly exceeding the diversity of TLR7. We present evidence of positive selection in TLR4 and TLR5, which points to pathogen-driven adaptation to the local pathogen milieu. Finally, we demonstrate that two positively selected cosegregating sites in TLR5 are sufficient to alter the responsiveness of the receptor to its bacterial ligand, flagellin. Taken together, these results suggest that Gentoo penguins have experienced distinct pathogen-driven selection pressures in different environments, which may be important given the role of the Gentoo penguin as a sentinel species in some of the world's most rapidly changing environments.

Comparative genome-wide polymorphic microsatellite markers in Antarctic penguins through next generation sequencing.

Microsatellites are valuable molecular markers for evolutionary and ecological studies. Next generation sequencing is responsible for the increasing number of microsatellites for non-model species. Penguins of the Pygoscelis genus are comprised of three species: Adélie (P. adeliae), Chinstrap (P. antarcticus) and Gentoo penguin (P. papua), all distributed around Antarctica and the sub-Antarctic. The species have been affected differently by climate change, and the use of microsatellite markers will be crucial to monitor population dynamics. We characterized a large set of genome-wide microsatellites and evaluated polymorphisms in all three species. SOLiD reads were generated from the libraries of each species, identifying a large amount of microsatellite loci: 33,677, 35,265 and 42,057 for P. adeliae, P. antarcticus and P. papua, respectively. A large number of dinucleotide (66,139), trinucleotide (29,490) and tetranucleotide (11,849) microsatellites are described. Microsatellite abundance, diversity and orthology were characterized in penguin genomes. We evaluated polymorphisms in 170 tetranucleotide loci, obtaining 34 polymorphic loci in at least one species and 15 polymorphic loci in all three species, which allow to perform comparative studies. Polymorphic markers presented here enable a number of ecological, population, individual identification, parentage and evolutionary studies of Pygoscelis, with potential use in other penguin species.

Comparative genome-wide polymorphic microsatellite markers in Antarctic penguins through next generation sequencing

Abstract Microsatellites are valuable molecular markers for evolutionary and ecological studies. Next generation sequencing is responsible for the increasing number of microsatellites for non-model species. Penguins of the Pygoscelis genus are comprised of three species: Adélie (P. adeliae), Chinstrap (P. antarcticus) and Gentoo penguin (P. papua), all distributed around Antarctica and the sub-Antarctic. The species have been affected differently by climate change, and the use of microsatellite markers will be crucial to monitor population dynamics. We characterized a large set of genome-wide microsatellites and evaluated polymorphisms in all three species. SOLiD reads were generated from the libraries of each species, identifying a large amount of microsatellite loci: 33,677, 35,265 and 42,057 for P. adeliae, P. antarcticus and P. papua, respectively. A large number of dinucleotide (66,139), trinucleotide (29,490) and tetranucleotide (11,849) microsatellites are described. Microsatellite abundance, diversity and orthology were characterized in penguin genomes. We evaluated polymorphisms in 170 tetranucleotide loci, obtaining 34 polymorphic loci in at least one species and 15 polymorphic loci in all three species, which allow to perform comparative studies. Polymorphic markers presented here enable a number of ecological, population, individual identification, parentage and evolutionary studies of Pygoscelis, with potential use in other penguin species.

Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean.

Two main hypotheses have been debated about the biogeography of the Southern Ocean: (1) the Antarctic Polar Front (APF), acting as a barrier between Antarctic and sub-Antarctic provinces, and (2) the Antarctic Circumpolar Current (ACC), promoting gene flow among sub-Antarctic areas. The Gentoo penguin is distributed throughout these two provinces, separated by the APF. We analyzed mtDNA (HVR1) and 12 microsatellite loci of 264 Gentoo penguins, Pygoscelis papua, from 12 colonies spanning from the Western Antarctic Peninsula and the South Shetland Islands (WAP) to the sub-Antarctic Islands (SAI). While low genetic structure was detected among WAP colonies (mtDNA ФST=0.037-0.133; microsatellite FST=0.009-0.063), high differentiation was found between all SAI and WAP populations (mtDNA ФST=0.678-0.930; microsatellite FST=0.110-0.290). These results suggest that contemporary dispersal around the Southern Ocean is very limited or absent. As predicted, the APF appears to be a significant biogeographical boundary for Gentoo penguin populations; however, the ACC does not promote connectivity in this species. Our data suggest demographic expansion in the WAP during the last glacial maximum (LGM, about 20kya), but stability in SAI. Phylogenetic analyses showed a deep divergence between populations from the WAP and those from the SAI. Therefore, taxonomy should be further revised. The Crozet Islands resulted as a basal clade (3.57Mya), followed by the Kerguelen Islands (2.32Mya) as well as a more recent divergence between the Falkland/Malvinas Islands and the WAP (1.27Mya). Historical isolation, local adaptation, and past climate scenarios of those Evolutionarily Significant Units may have led to different potentials to respond to climate changes.