Gisele P. M. Dantas

Have historical climate changes affected Gentoo penguin (Pygoscelis papua) populations in Antarctica

The West Antarctic Peninsula (WAP) has been suffering an increase in its atmospheric temperature during the last 50 years, mainly associated with global warming. This increment of temperature trend associated with changes in sea-ice dynamics has an impact on organisms, affecting their phenology, physiology and distribution range. For instance, rapid demographic changes in Pygoscelis penguins have been reported over the last 50 years in WAP, resulting in population expansion of sub-Antarctic Gentoo penguin (P. papua) and retreat of Antarctic Adelie penguin (P. adeliae). Current global warming has been mainly associated with human activities; however these climate trends are framed in a historical context of climate changes, particularly during the Pleistocene, characterized by an alternation between glacial and interglacial periods. During the last maximal glacial (LGM∼21,000 BP) the ice sheet cover reached its maximum extension on the West Antarctic Peninsula (WAP), causing local extinction of Antarctic taxa, migration to lower latitudes and/or survival in glacial refugia. We studied the HRVI of mtDNA and the nuclear intron βfibint7 of 150 individuals of the WAP to understand the demographic history and population structure of P. papua. We found high genetic diversity, reduced population genetic structure and a signature of population expansion estimated around 13,000 BP, much before the first paleocolony fossil records (∼1,100 BP). Our results suggest that the species may have survived in peri-Antarctic refugia such as South Georgia and North Sandwich islands and recolonized the Antarctic Peninsula and South Shetland Islands after the ice sheet retreat.

The niche and phylogeography of a passerine reveal the history of biological diversification between the Andean and the Atlantic forests

The Atlantic Forest is separated from the Andean tropical forest by dry and open vegetation biomes (Chaco and Cerrado). Despite this isolation, both rainforests share closely related lineages, which suggest a past connection. This connection could have been important for forest taxa evolution. In this study, we used the Saffron-billed Sparrow (Arremon flavirostris) as a model to evaluate whether the Andean and the Atlantic forests act as a refugia system, as well as to test for a history of biogeographic connection between them. In addition, we evaluated the molecular systematic of intraspecific lineages of the studied species. We modeled the current and past distribution of A. flavirostris, performed phylogeographic analyses based on mitochondrial and nuclear genes, and used Approximate Bayesian Computation (ABC) analyses to test for biogeographic scenarios. The major phylogeographic disjunction within A. flavirostris was found between the Andean and the Atlantic forests, with a divergence that occurred during the Mid-Pleistocene. Our paleodistribution models indicated a connection between these forest domains in different periods and through both the Chaco and Cerrado. Additionally, the phylogeographic and ABC analyses supported that the Cerrado was the main route of connection between these rainforests, but without giving decisive evidence against a Chaco connection. Our study with A. flavirostris suggest that the biodiversity of the Andean and of the Atlantic forests could have been impacted (and perhaps enriched?) by cycles of connections through the Cerrado and Chaco. This recurrent cycle of connection between the Andean and the Atlantic Forest could have been important for the evolution of Neotropical forest taxa. In addition, we discussed taxonomic implications of the results and proposed to split the studied taxon into two full 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.

Molecular Epidemiology of Avian Malaria in Wild Breeding Colonies of Humboldt and Magellanic Penguins in South America

Abstract Avian malaria is a disease caused by species of the genera Haemoproteus, Leucocytozoon, and Plasmodium. It affects hundreds of bird species, causing varied clinical signs depending on the susceptibility of the host species. Although high mortality has been reported in captive penguins, limited epidemiological studies have been conducted in wild colonies, and isolated records of avian malaria have been reported mostly from individuals referred to rehabilitation centers. For this epidemiological study, we obtained blood samples from 501 adult Humboldt and 360 adult Magellanic penguins from 13 colonies throughout South America. To identify malaria parasitaemia, we amplified the mtDNA cytochrome b for all three parasite genera. Avian malaria was absent in most of the analyzed colonies, with exception of the Punta San Juan Humboldt penguin colony, in Peru, where we detected at least two new Haemoproteus lineages in three positive samples, resulting in a prevalence of 0.6% for the species. The low prevalence of avian malaria detected in wild penguins could be due to two possible causes: A low incidence, with high morbidity and mortality in wild penguins or alternatively, penguins sampled in the chronic stage of the disease (during which parasitaemia in peripheral blood samples is unlikely) would be detected as false negatives.

Contrasting patterns of selection between MHC I and II across populations of Humboldt and Magellanic penguins

Abstract The evolutionary and adaptive potential of populations or species facing an emerging infectious disease depends on their genetic diversity in genes, such as the major histocompatibility complex (MHC). In birds, MHC class I deals predominantly with intracellular infections (e.g., viruses) and MHC class II with extracellular infections (e.g., bacteria). Therefore, patterns of MHC I and II diversity may differ between species and across populations of species depending on the relative effect of local and global environmental selective pressures, genetic drift, and gene flow. We hypothesize that high gene flow among populations of Humboldt and Magellanic penguins limits local adaptation in MHC I and MHC II, and signatures of selection differ between markers, locations, and species. We evaluated the MHC I and II diversity using 454 next‐generation sequencing of 100 Humboldt and 75 Magellanic penguins from seven different breeding colonies. Higher genetic diversity was observed in MHC I than MHC II for both species, explained by more than one MHC I loci identified. Large population sizes, high gene flow, and/or similar selection pressures maintain diversity but limit local adaptation in MHC I. A pattern of isolation by distance was observed for MHC II for Humboldt penguin suggesting local adaptation, mainly on the northernmost studied locality. Furthermore, trans‐species alleles were found due to a recent speciation for the genus or convergent evolution. High MHC I and MHC II gene diversity described is extremely advantageous for the long‐term survival of the species.

Landscape genomics: Natural selection drives the evolution of mitogenome in penguins

BackgroundMitochondria play a key role in the balance of energy and heat production, and therefore the mitochondrial genome is under natural selection by environmental temperature and food availability, since starvation can generate more efficient coupling of energy production. However, selection over mitochondrial DNA (mtDNA) genes has usually been evaluated at the population level. We sequenced by NGS 12 mitogenomes and with four published genomes, assessed genetic variation in ten penguin species distributed from the equator to Antarctica. Signatures of selection of 13 mitochondrial protein-coding genes were evaluated by comparing among species within and among genera (Spheniscus, Pygoscelis, Eudyptula, Eudyptes and Aptenodytes). The genetic data were correlated with environmental data obtained through remote sensing (sea surface temperature [SST], chlorophyll levels [Chl] and a combination of SST and Chl [COM]) through the distribution of these species.ResultsWe identified the complete mtDNA genomes of several penguin species, including ND6 and 8 tRNAs on the light strand and 12 protein coding genes, 14 tRNAs and two rRNAs positioned on the heavy strand. The highest diversity was found in NADH dehydrogenase genes and the lowest in COX genes. The lowest evolutionary divergence among species was between Humboldt (Spheniscus humboldti) and Galapagos (S. mendiculus) penguins (0.004), while the highest was observed between little penguin (Eudyptula minor) and Adélie penguin (Pygoscelis adeliae) (0.097). We identified a signature of purifying selection (Ka/Ks < 1) across the mitochondrial genome, which is consistent with the hypothesis that purifying selection is constraining mitogenome evolution to maintain Oxidative phosphorylation (OXPHOS) proteins and functionality. Pairwise species maximum-likelihood analyses of selection at codon sites suggest positive selection has occurred on ATP8 (Fixed-Effects Likelihood, FEL) and ND4 (Single Likelihood Ancestral Counting, SLAC) in all penguins. In contrast, COX1 had a signature of strong negative selection. ND4 Ka/Ks ratios were highly correlated with SST (Mantel, p-value: 0.0001; GLM, p-value: 0.00001) and thus may be related to climate adaptation throughout penguin speciation.ConclusionsThese results identify mtDNA candidate genes under selection which could be involved in broad-scale adaptations of penguins to their environment. Such knowledge may be particularly useful for developing predictive models of how these species may respond to severe climatic changes in the future.

Correction to: Chinstrap penguin population genetic structure: one or more populations along the Southern Ocean?

Correction to: BMC Evolutionary Biology (2018) 18:90https://doi.org/10.1186/s12862-018-1207-0.