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Glacial History and Ecological Restrictions Shape Island‐Scale Genetic Structure and Demography in the Southernmost Bird of Prey

Journal of Biogeography

January 2025
52(4)

DOI:10.1111/jbi.15083

Authors:

Ulises Balza

National Scientific and Technical Research Council

Nicolás Alejandro Lois

University of Buenos Aires

Katie J. Harrington

University of Veterinary Medicine Vienna

Show all 7 authorsHide

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.

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.

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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.

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(a) Expected heterozygosity for each Striated Caracara population based on 3546 independent SNPs. (b) Relatedness coefficient based on the same dataset.

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(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.

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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.

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Journal of Biogeography, 2025; 52:e15083

https://doi.org/10.1111/jbi.15083

Journal of Biogeography

RESEARCH ARTICLE

Glacial History and Ecological Restrictions Shape

Island- Scale Genetic Structure and Demography in the

Southernmost Bird of Prey

SantiagoG.Ceballos1,11

1Centro Austral de Investigaciones Científicas (CADIC- CONICET), Ushuaia, Argentina | 2Instituto de Ecologia Genetica y Evolucion de Buenos

Aires (IEGEBA- CONICET), Buenos Aires, Argentina | 3Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires,

Argentina | 4Comparative Cognition Unit, Messerli Research Institute, University of Veterinary Medicine Vienna, Vienna, Austria | 5Acopian Center

for Conservation Learning, Hawk Mountain Sanctuar y, Orwigsburg, Pennsylvania, USA | 6Facultad de Ciencias Biológicas, Departamento de Ecología,

Instituto Para el Desarrollo Sustentable, Pontificia Universidad Católica de Chile, Santiago, Chile | 7Millennium Institute Center for Genome Regulation,

Santiago, Chile | 8Millennium Institute of Biodiversity of Antarctic and Subantarctic Ecosystems, Santiago, Chile | 9Millennium Nucleus of Patagonian

Limit of Life, Santiago, Chile | 10Antarctic Research Trust, Bremer vörde, Germany | 11Instituto de Ciencias Polares, Ambiente y Recursos Naturales

(ICPA), Universidad Nacional de Tierra del Fuego, Ushuaia, Argentina | 12Wildlife Conservation Society, Buenos Aires, Argentina

Correspondence: Nicolás A. L ois (nlois@ege.fcen.uba.ar)

Received: 22 August 2024 | Revised: 18 December 2024 | Accepted: 26 December 2024

Funding: This work was supported by Wildlife Conservation Society Argentina, Agencia Nacional de Promoción Científica y Tecnológica, Hawk Mountain

Sanctuary Association, A ntarctic Research Tr ust.

ABSTRACT

Aim: To understand the influence of Andean uplifts and glacial cycles on South American biodiversity, we delve into the popu-

lation 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 hy pothesis- 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 pe-

riod (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.

Selection on a single locus drives plumage differentiation in the Rufous-collared Sparrow (Zonotrichia capensis)

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Apr 2025
EVOLUTION

The Rufous-collared Sparrow (Zonotrichia capensis) shows phenotypic variation throughout its distribution. In particular, the Patagonian subspecies Z. c. australis is strikingly distinct from all other subspecies, lacking the black crown stripes that characterize the species, with a uniformly grey head and overall paler plumage. We sequenced whole genomes of 18 individuals (nine Z. c. australis and nine from other subspecies from northern Argentina) to explore the genomic basis of these color differences and to investigate how they may have evolved. We detected a single ~465-kb divergence peak on chromosome 5 that contrasted with a background of low genomic differentiation and contains the ST5 gene. ST5 regulates RAB9A, which is required for melanosome biogenesis and melanocyte pigmentation in mammals, making it a strong candidate gene for the melanic plumage polymorphism within Z. capensis. This genomic island of differentiation may have emerged because of selection acting on allopatric populations or against gene flow on populations in physical and genetic contact. Mitochondrial DNA indicated that Z. c. australis diverged from other subspecies ~400,000 years ago, suggesting a putative role of Pleistocene glaciations. Phenotypic differences are consistent with Gloger’s rule, which predicts lighter colored individuals in colder and drier climates like that of Patagonia.

Impacts of Quaternary glaciation, geological history and geography on animal species history in continental East Asia: A phylogeographic review

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MOL ECOL

Continental East Asia has a mild Pleistocene climate and a complex recent geological history. Phylogeographic studies of animals over the last 30 years have produced several distinctive patterns. Glaciation refugia are numerous and are not restricted to any particular regions. Most of them are localized and species‐specific, although several large refugia, for example the mountains of SW China, are shared by multiple species and have refugia‐within‐refugia. Furthermore, postglaciation range expansion events vary greatly in time, scale and direction. Large‐scale south‐to‐north post‐LGM expansions are few and mostly occurred in the northern regions. Additionally, several unique geographic features, including the three‐step terrain of China and the northern arid belt, have significant impacts on many species histories. Overall, the impacts of Pleistocene glaciations, particularly the LGM, on species history vary drastically from nondetectable to significant. The impacts are the least for species from the southwestern region and are most dominant for species from the north. Geological events play a more significant role in shaping species history than Pleistocene climatic changes. Phylogeographic patterns among animals species are highly consistent with those of plants. Future phylogeographic endeavour in East Asia should be hypothesis‐driven and seek processes that underlie common patterns. The wide use of genomic data allow accurate estimates of historical population processes and exploration of older history beyond the Pleistocene.

Status of breeding birds at Observatorio and Goffré Islands, Argentina

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POLAR BIOL

Continental islands are often sites of low diversity and endemism, as well as important areas for the protection of bird populations, especially seabirds. On Isla Observatorio and the Año Nuevo Islands, in the Southwestern Atlantic, the latest assessment of avifauna dates from more than 20 years ago. In this study, we use a combination of methods to update the status of the main seabird colonies and the most abundant avian terrestrial predator at Observatorio and Goffré Islands during the breeding season. In only 4.5 km², the islands would harbour ~ 90,000 breeding seabirds. Seabird colonies occupied different areas of the islands and varied in their population status, with Imperial Shags (Leucocarbo atriceps) showing an increase and Southern Giant Petrels (Macronectes giganteus) a decrease according to the last surveys. Magellanic Penguin (Spheniscus magellanicus) population estimations also suggest a decrease but the last survey was based on total, and not on occupied nest sites. We recorded and assessed one new breeding species: The globally near-threatened Striated Caracara (Phalcoboenus australis), which has an important breeding population of around 15 territorial pairs at Observatorio Island. These islands appear to be an important regional bird site and future studies would determine their trends and threats, especially those related with invasive species.

fastsimcoal2 : demographic inference under complex evolutionary scenarios

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Motivation fastsimcoal2 extends fastsimcoal, a continuous time coalescent-based genetic simulation program, by enabling the estimation of demographic parameters under very complex scenarios from the site frequency spectrum under a maximum-likelihood framework. Results Other improvements include multi-threading, handling of population inbreeding, extended input file syntax facilitating the description of complex demographic scenarios, and more efficient simulations of sparsely structured populations and of large chromosomes. Availability fastsimcoal2 is freely available on http://cmpg.unibe.ch/software/fastsimcoal2/. It includes console versions for Linux, Windows and MacOS, additional scripts for the analysis and visualization of simulated and estimated scenarios, as well as a detailed documentation and ready-to-use examples.

Mapping our knowledge on birds of prey population genetics

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The current and rapid anthropogenic environmental changes could disproportionately impact ecosystems, particularly when they affect species with critical roles in ecosystem integrity. As top predators, raptors provide critical top-down ecosystem services and structure food webs. Yet, many avian predators are currently experiencing global population declines and some are threatened with extinction. The dire conservation status of numerous raptor species warrants urgent action, and detailed ecological data are needed to guide management strategy, including empirical knowledge regarding genetic structure. To that end, we compiled published studies investigating population genetic structure in raptors. Out of a total of 83 publications on 50 raptors species published, we identified a lack of empirical genetic studies for species from the Southern Hemisphere and species with a high level of extinction risk according to IUCN Red List criteria. Only 24% of the species studied are considered “threatened” (i.e., with the “Vulnerable”, “Endangered”, or “Critically Endangered” status). We found a significant signal of genetic differentiation in 41 species (82%) at the study-specific population. Isolation-by-Distance is a common pattern of genetic differentiation in raptors. Future steps in raptor conservation could prioritize facilitating genetic studies on species located in the Southern Hemisphere and on species with a conservation status. A better inclusion of some key genetic metrics (e.g., Ne, Ne/Nc, genetic diversity) in published studies will further help management and conservation across various species and ecosystems.

Extreme philopatry and genetic diversification at unprecedented scales in a seabird

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Effective conservation requires maintenance of the processes underlying species divergence, as well as understanding species’ responses to episodic disturbances and long-term change. We explored genetic population structure at a previously unrecognized spatial scale in seabirds, focusing on fine-scale isolation between colonies, and identified two distinct genetic clusters of Barau’s Petrels ( Pterodroma baraui ) on Réunion Island (Indian Ocean) corresponding to the sampled breeding colonies separated by 5 km. This unexpected result was supported by long-term banding and was clearly linked to the species’ extreme philopatric tendencies, emphasizing the importance of philopatry as an intrinsic barrier to gene flow. This implies that loss of a single colony could result in the loss of genetic variation, impairing the species’ ability to adapt to threats in the long term. We anticipate that these findings will have a pivotal influence on seabird research and population management, focusing attention below the species level of taxonomic organization.

Genetic Diversity and Demographic History of the Shaggy Soft-Haired Mouse Abrothrix hirta (Cricetidae; Abrotrichini)

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Genetic information on species can inform decision making regarding conservation of biodiversity since the response of organisms to changing environments depend, in part, on their genetic makeup. Territories of central-southern Chile and Argentina have undergone a varying degree of impact during the Quaternary, where the response of local fauna and flora was rather species-specific. Here, we focus on the sigmodontine rodent Abrothrix hirta, distributed from 35° S in Chile and Argentina to northern Tierra del Fuego. Based on 119,226 transcriptome-derived SNP loci from 46 individuals of A. hirta, we described the geographic distribution of the genetic diversity of this species using a maximum likelihood tree, principal component and admixture analyses. We also addressed the demographic history of the main intraspecific lineages of A. hirta using GADMA. We found that A. hirta exhibited four allopatric intraspecific lineages. Three main genetic groups were identified by a Principal Component Analysis and by Ancestry analysis. The demographic history of A. hirta was characterized by recent population stability for populations at the northernmost part of the range, while southern populations experienced a recent population expansion.

Winter bird gets the worm: consumption of earthworms (Lumbricidae) by striated caracaras (Phalcoboenus australis) in invasive Yorkshire fog (Holcus lanatus) in the Falkland Islands (Malvinas)

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Biological invasions can drive ecosystem change and alter predator ecology by providing trophic subsidies that mitigate the effects of seasonally pulsed resources. Striated Caracaras (Phalcoboenus australis) are near threatened, non-migratory falconids who inhabit the southern coasts of South America and the Falkland Islands (Malvinas) and feed on seasonally migratory colonial seabirds. Here we report the first multi-day observation of caracaras foraging extensively for earthworms (Lumbricidae) and beetle larvae (Coleoptera) in introduced Yorkshire fog (Holcus lanatus) on New Island, Falkland Islands. Our results suggest that invertebrates may be a more important winter resource than previously thought, and that caracaras benefit indirectly from introduced grasses in the Falklands, a relationship that merits special consideration when identifying ecological restoration plans.

SambaR: An R package for fast, easy and reproducible population‐genetic analyses of biallelic SNP data sets

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SNP data sets can be used to infer a wealth of information about natural populations, including information about their structure, genetic diversity, and the presence of loci under selection. However, SNP data analysis can be a time‐consuming and challenging process, not in the least because at present many different software packages are needed to execute and depict the wide variety of mainstream population‐genetic analyses. Here, we present SambaR, an integrative and user‐friendly R package which automates and simplifies quality control and population‐genetic analyses of biallelic SNP data sets. SambaR allows users to perform mainstream population‐genetic analyses and to generate a wide variety of ready to publish graphs with a minimum number of commands (less than 10). These wrapper commands call functions of existing packages (including adegenet, ape, LEA, poppr, pcadapt and StAMPP) as well as new tools uniquely implemented in SambaR. We tested SambaR on online available SNP data sets and found that SambaR can process data sets of over 100,000 SNPs and hundreds of individuals within hours, given sufficient computing power. Newly developed tools implemented in SambaR facilitate optimization of filter settings, objective interpretation of ordination analyses, enhance comparability of diversity estimates from reduced representation library SNP data sets, and generate reduced SNP panels and structure‐like plots with Bayesian population assignment probabilities. SambaR facilitates rapid population genetic analyses on biallelic SNP data sets by removing three major time sinks: file handling, software learning, and data plotting. In addition, SambaR provides a convenient platform for SNP data storage and management, as well as several new utilities, including guidance in setting appropriate data filters. The SambaR source script, manual and example data set are distributed through GitHub: https://github.com/mennodejong1986/SambaR.

Conservation and the Genomics of Populations

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Feb 2022

Loss of biodiversity is among the greatest problems facing the world today. Conservation and the Genomics of Populations gives a comprehensive overview of the essential background, concepts, and tools needed to understand how genetic information can be used to conserve species threatened with extinction, and to manage species of ecological or commercial importance. New molecular techniques, statistical methods, and computer programs, genetic principles, and methods are becoming increasingly useful in the conservation of biological diversity. Using a balance of data and theory, coupled with basic and applied research examples, this book examines genetic and phenotypic variation in natural populations, the principles and mechanisms of evolutionary change, the interpretation of genetic data from natural populations, and how these can be applied to conservation. The book includes examples from plants, animals, and microbes in wild and captive populations. This third edition has been thoroughly revised to include advances in genomics and contains new chapters on population genomics, genetic monitoring, and conservation genetics in practice, as well as new sections on climate change, emerging diseases, metagenomics, and more. More than one-third of the references in this edition were published after the previous edition. Each of the 24 chapters and the Appendix end with a Guest Box written by an expert who provides an example of the principles presented in the chapter from their own work. This book is essential for advanced undergraduate and graduate students of conservation genetics, natural resource management, and conservation biology, as well as professional conservation biologists and policy-makers working for wildlife and habitat management agencies. Much of the book will also interest nonprofessionals who are curious about the role of genetics in conservation and management of wild and captive populations.

Phylogeography of Otaria flavescens (Carnivora: Pinnipedia): unravelling genetic connectivity at the southernmost limit of its distribution

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The Pleistocene glacial period shaped the current genetic structure of numerous species. The last glacial dynamics has been proposed to have split the South American sea lion, Otaria flavescens, into two Evolutionarily Significant Units (ESUs), one on each side of the continent. However, previous studies have not provided genetic information on colonies found along 3000 km of coastline of the southernmost limit of the species distribution, where gene flow could occur. We conducted an exhaustive phylogeographical analysis of O. flavescens using a mtDNA marker, including, for the first time, data from colonies living south of latitude 45° S, in the Argentinian provinces of Santa Cruz and Tierra del Fuego. Our results indicated the presence of five Conservation Units across the distribution range of O. flavescens and suggest that the Patagonian population must have expanded about 150 000 BP. We found evidence for gene flow across the entire species range, supporting a scenario of secondary contact in Tierra del Fuego where representatives of the oldest lineages coexist. The presence of gene flow between oceans leads us to reject the assumption of complete reciprocal monophyly for mtDNA between the presumed ESUs, suggesting that the species constitutes a single Evolutionarily Significant Unit.

Glacial History and Ecological Restrictions Shape Island‐Scale Genetic Structure and Demography in the Southernmost Bird of Prey

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