Fabiola León’s research while affiliated with Pontifical Catholic University of Chile and other places

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Publications (6)


Skuas mortalities linked to positives HPAIV A/H5 beyond Polar Antarctic Circle
  • Preprint
  • File available

March 2025

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141 Reads

fabiola Leon

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The ongoing extinction crisis, driven by human activity, poses a significant threat to seabirds and it's especially relevant in highly valuable environments such as Antarctica. Among these threats, seabirds face the risk of local extinctions due to emerging infectious diseases like the Highly Pathogenic Avian Influenza Virus (HPAIV).Progressive spread of HPAIV A/H5N1 outbreaks across South America and the sub-Antarctic islands have been detected, reaching the northern regions of the West Antarctic Peninsula (WAP) during the 2023-2024 season. Here we conducted a comprehensive epidemiological survey conducted on sixteen seabird nesting localities along the WAP from November 2024 to January 2025 to assess the health status of the Antarctic seabirds and detect the presence of HPAIV. We observed unusual mortalities among nesting populations of skuas, with a total of 35 deaths skuas recorded along the WAP and beyond the Antarctic Polar Circle, including Important bird breeding areas around Margarita Bay. HPAIV A/H5 was confirmed in all dead skuas sampled (n=11), from six different locations. This finding represents the southernmost record of seabird mortality in Antarctica related to HPAIV to date. The expansion of HPAIV observed here raises concerns about further spread of avian flu out the Antarctic Peninsula, potentially leading to increased mortality rates in the Antarctic bird populations. These findings are relevant for the assessment of the general health status of Antarctic seabird populations and provide a baseline for the continuous monitoring of the HPAIV spread in avian species during the next breeding seasons.

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Left: Current distribution of Striated Caracara (yellow), in the context of the Southern South American landscape configuration during the Last Glacial Maximum, showing the extent of the ice sheet (blue) and the emerged land (grey, 120 m isobath) (BirdLife International 2016; Davies et al. 2020). Coloured circles depict sampling sites in the Fuegian archipelago (Isla de los Estados) and in the Malvinas/Falkland Islands (Saunders, New Island and Bleaker). Right: Maximum likelihood phylogenetic tree (colours correspond to sampling sites) obtained using over 51,000 independent SNPs, with the White‐throated Caracara (P. albogularis) and the Chimango caracara (P. chimango) as outgroups.
Schematic representation of the 12 scenarios tested in the demographic history modelling of the Striated Caracara. Malvinas/Falklands (orange) and Isla de los Estados (light blue) populations are shown as bars representing their occurrence. Y‐axis represents a theoretical time since the present. The processes involved and the rationale for the inclusion of the scenarios are detailed in Table 1.
(a) Expected heterozygosity for each Striated Caracara population based on 3546 independent SNPs. (b) Relatedness coefficient based on the same dataset.
(a) Coancestry matrix implemented in fineRADstructure. (b) The first two principal components from PCA. Both analyses suggest differentiation etween Isla de los Estados and IM/FI and a finer‐scale structure within IM/FI, which splits eastern (Bleaker) from western (Saunders and New Island) populations.
The best supported demographic scenario based on fastsimcoal2 simulations. Divergence times are expressed in years and effective population sizes in number of individuals. Migration among clusters is qualitatively expressed with arrows. Each estimated parameter has its 95%, bootstrap‐generated confidence intervals between parenthesis. The last glacial period is qualitatively depicted in shaded grey. Figure design by Samanta Dodino.
Glacial History and Ecological Restrictions Shape Island‐Scale Genetic Structure and Demography in the Southernmost Bird of Prey

January 2025

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118 Reads

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1 Citation

Aim To understand the influence of Andean uplifts and glacial cycles on South American biodiversity, we delve into the population genetics and evolutionary history of a unique subantarctic island raptor specialised in exploiting marine food webs. Location Islands in Tierra del Fuego and Malvinas/Falklands. Time period Last glacial period to the present. Taxon Phalcoboenus australis. Methods We used RAD sequencing to assess genetic diversity, population structure and to model demographic history through descriptive and hypothesis‐based evolutionary methods. Results We found evidence of two independent lineages: one inhabiting the Fuegian archipelago and the other one occurring in the Islas Malvinas/Falkland Islands, with the latter presenting higher genetic diversity and evidence of finer‐scale population structure. The best supported demographic scenario places the divergence time of these lineages during the last glacial period (ca. 50,000 years ago), with the occurrence of gene flow during the first 27,000 years after their divergence. Recent demographic modelling supports the general pattern of increasing genetic variability as landmasses were uncovered following the glacial period (i.e., the Fuegian archipelago) in contrast with a decrease in genetic diversity associated to island fragmentation (i.e., in the Islas Malvinas/Falkland Islands). Main Conclusions We propose that post‐glacial sea level rise and the subsequent isolation across the submerging Patagonian Shelf have driven population fragmentation and recent genetic structure in this species. Our findings advocate for recognising the two identified divergent lineages as distinct conservation units. We highlight the intricate interplay of ecological factors, glacial cycles and population dynamics in shaping the evolutionary trajectory of this unique and threatened raptor species in southern South America.


Fig. 3. Whole-genome divergent selection between pairwise Spheniscus species. a) The primary GO and enrichment analysis conducted in the selection analysis between species (a1 to a3). Venn diagrams illustrate the number of outlier SNPs recovered using OUTFLANK, PCAadpt, and GWDS and their intersection. b) The biological functions inferred to be under selection in all 4 banded penguin species. c) Manhattan plots illustrate the SNPs between species and their degree of differentiation.
Fig. 4. Enrichment results of the SNPs under divergent selection between Galápagos and Humboldt penguins. a) The GO of the most relevant biological processes, along with SNPs under selection, identified throughout the genomes of Galápagos and Humboldt penguins. b) The relative proportion of SNPs under selection, linked to genes associated with functions pertaining to spermatogenesis and sperm motility. c) Associations between spermatogenesis loci revealing functional relationships between genes. Interaction types include direct interactions, gene expression regulation, or participation in shared biochemical pathways.
Fig. 5. Comparative gene family analyses among banded and little blue penguins. a) Cluster and protein counts of orthogroups found among banded and little blue penguins. b) Cluster and protein count of orthogroups found among banded penguins. c) Maximum likelihood tree based on single-copy genes showing the gain (red) and loss (blue) of genes across banded penguins lineages. d) Feather keratin Cos2-3 family gene expansion. e) Histone H2B family gene expansion. f) The gene family associated with heat stress response includes the heat shock transcription Y-linked gene. (g and h) The adenylate cyclase type 10 and chromodomain Y-like gene are part of the spermatogenesis expanded gene family. i) The gain in the osmoregulation gene family involved sodium channel genes.
Fig. 6. Banded penguin ecological niche overlap. a) Sea surface temperature across the globe, with breeding colony locations where environmental data were obtained. Graphical representation of the extent of niche overlap (in purple and dark blue) in pairwise comparisons between banded species: b) Galápagos penguins (green) vs. Humboldt (pink); c) Humboldt (pink) vs. Magellanic penguins (yellow); d) Magellanic (yellow) vs. African penguins (light blue).
Comparative Genomics Supports Ecologically Induced Selection as a Putative Driver of Banded Penguin Diversification

August 2024

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187 Reads

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2 Citations

Molecular Biology and Evolution

The relative importance of genetic drift and local adaptation in facilitating speciation remains unclear. This is particularly true for seabirds, who can disperse over large geographic distances, providing opportunities for intermittent gene flow among distant colonies that span the temperature and salinity gradients of the oceans. Here, we delve into the genomic basis of adaptation and speciation of banded penguins, Galápagos (Spheniscus mendiculus), Humboldt (S. humboldti), Magellanic (S. magellanicus) and African penguins (S. demersus), by analyzing 114 genomes from the main 16 breeding colonies. We aim to identify the molecular mechanism and genomic adaptive traits that have facilitated their diversifications. Through positive selection and gene family expansion analyses, we identified candidate genes that may be related to reproductive isolation processes mediated by ecological thermal niche divergence. We recover signals of positive selection on key loci associated with spermatogenesis, especially during the recent peripatric divergence of the Galápagos penguin from the Humboldt penguin. High temperatures in tropical habitats may have favored selection on loci associated with spermatogenesis to maintain sperm viability, leading to reproductive isolation among young species. Our results suggest that genome-wide selection on loci associated with molecular pathways that underpin thermoregulation, osmoregulation, hypoxia, and social behavior appear to have been crucial in local adaptation of banded penguins. Overall, these results contribute to our understanding of how the complexity of biotic, but especially abiotic, factors, along with the high dispersal capabilities of these marine species, may promote both neutral and adaptive lineage divergence even in the presence of gene flow.


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

May 2024

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120 Reads

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1 Citation

Genome Biology and Evolution

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.


Highly Pathogenic Avian Influenza A (H5N1) Suspected in penguins and shags on the Antarctic Peninsula and West Antarctic Coast

March 2024

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128 Reads

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8 Citations

Suspected cases of Highly Pathogenic Avian Influenza (H5N1) were detected in Adelie penguins and Antarctic shags at the southernmost latitude so far in Antarctica, at two breeding sites out of 13 visited, using highly specific PCR assay. These first records mark the progression of the H5N1 panzootic into Antarctica.


Figure 1. Distribution of gentoo penguins around the Southern Ocean. The figure shows the sample locations (colored circles): northern gentoo: Martillo and Falkland/Malvinas I.; southern gentoo: Signy Island, O'Higgins base, Stranger Point and Gabriel Gonzalez Videla base; southeastern gentoo: Courbet Peninsula, Kerguelen I.; eastern gentoo: Marion and Crozet I. and open circles represent areas with unsampled colonies. Map images provided by Shutterstock database and edited in Adobe Illustrator.
(a) Haplotype distribution of gentoo penguin lineages around the Southern Ocean; (b) Distribution of haplotypes translated into amino acid sequences. Map images provided by Shutterstock database and edited in Adobe Illustrator.
Figure 3. Bayesian phylogenetic reconstruction obtained from partitions of 13 protein coding genes (11,170 bp). On the phylogenies, stars, circles, and squares represent codons under selection obtained using different approaches. Stars and circles represent codons with positive selection signals obtained from only TreeSAAP or only codeml analyses, respectively. Squares represent sites under selection using both programs. Abbreviations on the map: APF (Antarctic Polar Front) and STF (Sub-Tropical Front). All nodes were supported by PP = 1.0. Map images provided by Shutterstock database and edited in Adobe Illustrator.
Mito-nuclear discordance between topologies of gentoo penguins. Left: Genomic phylogeny (SNAPP) generated using 4429 SNPs in Pertierra et al. (2020). Right: Bayesian phylogeny from 13 mitochondrial protein coding genes (11,170 bp).
Estimation ΔLRT of M1a/M2a and M7/M8 nested codeml site models (*p < 0.05) to detect genes candidates of positive selection.
Positive selection over the mitochondrial genome and its role in the diversification of gentoo penguins in response to adaptation in isolation

March 2022

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723 Reads

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21 Citations

Although mitochondrial DNA has been widely used in phylogeography, evidence has emerged that factors such as climate, food availability, and environmental pressures that produce high levels of stress can exert a strong influence on mitochondrial genomes, to the point of promoting the persistence of certain genotypes in order to compensate for the metabolic requirements of the local environment. As recently discovered, the gentoo penguins (Pygoscelis papua) comprise four highly divergent lineages across their distribution spanning the Antarctic and sub-Antarctic regions. Gentoo penguins therefore represent a suitable animal model to study adaptive processes across divergent environments. Based on 62 mitogenomes that we obtained from nine locations spanning all four gentoo penguin lineages, we demonstrated lineage-specific nucleotide substitutions for various genes, but only lineage-specific amino acid replacements for the ND1 and ND5 protein-coding genes. Purifying selection (dN/dS < 1) is the main driving force in the protein-coding genes that shape the diversity of mitogenomes in gentoo penguins. Positive selection (dN/dS > 1) was mostly present in codons of the Complex I (NADH genes), supported by two different codon-based methods at the ND1 and ND4 in the most divergent lineages, the eastern gentoo penguin from Crozet and Marion Islands and the southern gentoo penguin from Antarctica respectively. Additionally, ND5 and ATP6 were under selection in the branches of the phylogeny involving all gentoo penguins except the eastern lineage. Our study suggests that local adaptation of gentoo penguins has emerged as a response to environmental variability promoting the fixation of mitochondrial haplotypes in a non-random manner. Mitogenome adaptation is thus likely to have been associated with gentoo penguin diversification across the Southern Ocean and to have promoted their survival in extreme OPEN

Citations (4)


... Our mitochondrial DNA results indicated that Z. c. australis diverged from the other subspecies within lineage B around 400,000 years ago based on a 2.1% divergence per million years rate (Weir & Schluter, 2008), suggesting a potential role of Pleistocene glaciations in the evolution of Z. capensis in Patagonia. This was previously suggested by Lougheed et al., (2013) for Z. capensis and is also apparent in other Neotropical birds (Kopuchian et al., 2016;Acosta et al., 2020;Bukowski et al., 2024;Balza et al., 2025). One possibility is that glaciations isolated southern populations of Z. capensis in Patagonia, congruent with the "selection-in-allopatry" model. ...

Reference:

Selection on a single locus drives plumage differentiation in the Rufous-collared Sparrow (Zonotrichia capensis)
Glacial History and Ecological Restrictions Shape Island‐Scale Genetic Structure and Demography in the Southernmost Bird of Prey

... Adaptation for the conditions of high mountain altitudes [12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29]. Adaptation to the conditions of the high mountain altitudes was characterized by higher levels of ionized radiation (solar, galactic, etc.) and oxygen deficiency (causing hypoxia) [17][18][19]. ...

History of Diversification and Adaptation from North to South Revealed by Genomic Data: Guanacos from the Desert to Sub-Antarctica
  • Citing Article
  • May 2024

Genome Biology and Evolution

... By December 2023, beach surveys along the southern Brazilian coast documented 271 SASL, of which 82.6% were found dead (de Lima et al. 2024). The HPAI H5N1 virus was also detected in South Georgia in October 2023 (Government of South Georgia and the South Sandwich Islands 2023), the Falkland/Malvinas Islands in November 2023 (Falkland/ Malvinas Islands Government 2023), and mainland Antarctica in February 2024 (León et al. 2024). ...

Highly Pathogenic Avian Influenza A (H5N1) Suspected in penguins and shags on the Antarctic Peninsula and West Antarctic Coast
  • Citing Preprint
  • March 2024

... Protein-coding mitochondrial genes, responsible for oxidative phosphorylation and energy production, may be involved in environmental adaptation (Lubawy et al. 2022). While the order and sequence of these genes is relatively conserved, it has been demonstrated that mitogenomes of conspecific arthropod and other metazoan lineages may be subject to selective pressure, particularly driven by climatic stress (Camus et al. 2017;Li et al. 2018;Noll et al. 2022). We searched for potential targets of selection commensurate with diversification of major ALT lineages within our mitochondrial genomes and identified nad4L (NADHubiquinone oxidoreductase chain 4 L; electron transport from NADH to the respiratory chain) and nad1 (NADH-ubiquinone oxidoreductase chain 1) as having potentially relevant amino acid substitutions in the parthenogenetic and H1 lineages, respectively. ...

Positive selection over the mitochondrial genome and its role in the diversification of gentoo penguins in response to adaptation in isolation