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Forcada, J.

Publications and source records attributed to Forcada, J..

13 recordsLinked to original sources

The crabeater seal reference genome reveals hallmarks of persistently large effective population size and sustained population expansion in the World's most abundant pinniped

Population genetic theory predicts that a species demographic history shapes patterns of genome-wide variation. However, conservation genomic studies have disproportionately focused on small or declining species, where low genetic diversity and inbreeding are major concerns, while highly abundant species have attracted comparatively less attention. Here, we investigate the crabeater seal (Lobodon carcinophaga) which, despite being one of the most numerous large mammals on Earth, remains largely uncharacterised in terms of its genomic diversity and demographic history. We assembled a high-quality crabeater seal reference genome from a combination of Illumina and PacBio HiFi reads, generating a 2.44 Gb assembly spanning 138 scaffolds with high completeness. To evaluate genomic diversity in a comparative context, we whole-genome resequenced 20 crabeater seals alongside 20 individuals each of three Antarctic phocids spanning a population size gradient: the Weddell seal (Leptopnychotes weddellii), leopard seal (Hydrurga leptonyx) and southern elephant seal (Mirounga leonina). Crabeater seals carried 61.5 million SNPs compared to 12-16 million in the other species and exhibited markedly higher nucleotide diversity and negligible genomic inbreeding. We observed an excess of rare alleles, with nearly half of all variants segregating at frequencies below 5%. Demographic reconstruction revealed persistently large effective population sizes over the past million years and sustained population expansion, paralleling inferred increases in Antarctic krill associated with sea-ice expansion during the late Pleistocene. This study provides a new genomic resource and sheds new light on the evolutionary dynamics of the worlds most abundant pinniped.

genomics↗

Early-life environmental conditions shape demographic responses to climate change in male Antarctic fur seals

Climate change intensifies selection, driving population declines and eroding genetic diversity, yet the mechanisms linking environmental perturbations to long-term demographic and evolutionary outcomes remain elusive. In particular, deteriorating early-life environments can have lasting impacts on fitness and population dynamics, but detecting these carry-over effects requires multidecadal, individual-based datasets. Long-term monitoring of Antarctic fur seals at Bird Island, South Georgia, has revealed a decline in breeding female numbers associated with persistent positive phases of the Southern Annular Mode (SAM), when warmer sea surface temperatures reduce local krill abundance. However, male responses remain understudied as their large size and aggressiveness preclude conventional tagging. To investigate male population dynamics, we combined 27 years of field observations of nearly 2,000 individually paint-marked territorial males with genetic recapture analysis of over 11,000 tissue samples, testing for both direct effects of the SAM on male abundance and lagged effects operating through recruitment. Territorial male numbers declined by 61%, yet male abundance was decoupled from the contemporary SAM, reflecting a delayed recruitment strategy that allows resource accumulation over multiple years and buffers short-term environmental variation. By contrast, recruitment probability fell by 59% annually and was strongly linked to natal conditions. Males born during increasingly positive SAM phases were significantly less likely to recruit, whereas heavier and more heterozygous individuals showed higher recruitment success, indicating that adverse natal environments act as selective filters. These findings identify a pathway linking environmental variability to population decline through recruitment dynamics, highlighting the importance of accounting for early-life carry-over effects when predicting the resilience of long-lived species to rapid environmental change.

ecology↗

High population density limits predator access in Antarctic fur seal breeding colonies

Population density can influence individual predation risk in colonial breeders through shared vigilance and predator deterrence. We investigated how predator-prey interactions are shaped by population density at two Antarctic fur seal (Arctocephalus gazella) breeding colonies at Bird Island, South Georgia, which differ four-fold in seal density. By deploying autonomous time-lapse cameras, we captured high-resolution images at one-minute intervals throughout the breeding season. Using a YOLOv8 neural network, we identified fur seal adult males, females and pups, as well as three predator-scavenger bird species: giant petrels (Macronectes spp.), brown skuas (Stercorarius antarcticus) and snowy sheathbills (Chionis alba). Abundance patterns corresponded to the known foraging and breeding behaviours of these species. Differences in seal density between the colonies were mainly driven by adult females and their pups, but not adult males. The ratios of predatory birds to pups were markedly lower at the high-density colony, while scavenger to pup ratios remained similar. Spatial analyses revealed that predators were largely excluded from areas of high seal density, whereas scavengers overlapped extensively with pups in both colonies. This study demonstrates the value of remote observation in resolving predator-prey interactions and illustrates how density can shape predation risk in a colonial breeder.

ecology↗

Fine-scale spatiotemporal predator-prey interactions in an Antarctic fur seal colony

Density is a major determinant of population dynamics, with high densities exacerbating intraspecific competition and disease transmission, while low densities increase predation risk. To investigate spatiotemporal density patterns and predator-prey interactions in a breeding colony of Antarctic fur seals (Arctocephalus gazella), we deployed an autonomous camera capturing minute-by-minute, high-resolution images throughout a breeding season. Using a YOLO-based neural network, we identified adult males, females and pups, as well as three avian predator-scavengers: giant petrels (Macronectes spp.), brown skuas (Stercorarius antarcticus) and snowy sheathbills (Chionis alba). Analysis of 4.1 million automated detections from over 10,000 high-quality images revealed spatiotemporal abundance patterns corresponding with the known breeding and foraging behaviours of these species. Strong temporal associations emerged between the abundance of pups and two avian species, while fine-scale spatial analyses showed that pups grouped together with other pups and adult females but avoided avian predators and territorial males. Notably, proximity to adult fur seals of both sexes reduced pup predation risk, defined as the distance between the pup and the nearest bird, whereas proximity to other pups did not. Overall, this study provides a framework for quantifying density-dependent interactions in wild populations and emphasises the value of remote observation in ecological research.

ecology↗

Semi-Automated Seal Detection on the Western Antarctic Peninsula: An Unsupervised Machine Learning Approach for Detecting Ice Seals in Aerial Survey Data

Over the past 25 years, the Western Antarctic Peninsula (WAP) has experienced dramatic shifts in sea ice extent. This change has coincided with rapid alterations in ice-dependent ecosystems, including those supporting crabeater seals - the most abundant Antarctic seal and one of the largest mammalian consumers of krill. Despite their ecological importance, population estimates for ice seals remain scarce due to the difficulty of surveying large-scale, remote, ice-covered habitats. In 2023, during an abnormally low sea ice year, we conducted aerial surveys over Crystal Sound and Marguerite Bay during the end of the breeding season, flying over 1,000 km of transects. Seals were extremely sparse in the resulting imagery - occupying less than 1% of the surveyed area. This posed a significant challenge for both manual annotation and automated detection. Here we present a semi-automated, rules-based image analysis pipeline to substantially reduce human annotation time. Our method leverages hierarchical clustering with just two tunable parameters, avoiding the computational burden and opacity of deep learning models. Using this method, we identified 758 seals within a [~]350 km2 survey subset, achieving a test recall of 82%. In the absence of concurrent tagging data to estimate haul-out corrections, we refrain from extrapolating to a population estimate. However, the low observed densities highlight the urgent need for continued monitoring. Our improved data processing pipeline is a key step in facilitating the large-scale analysis required to inform conservation strategies for this key species.

ecology↗

Skin but not gut microbial communities in Antarctic fur seals vary with social density

Comparative studies of microbial communities occupying different body sites in wild vertebrates are scarce, but they are crucial for advancing our understanding of the ecological and evolutionary factors shaping animal microbiomes. We therefore used a "natural experiment" comprising mother-offspring pairs from two adjacent Antarctic fur seal breeding colonies that differ in social density to investigate differences between skin and gut microbial communities in relation to host-specific and environmental factors. Using 16S rRNA amplicon sequencing, we uncovered a strong influence of colony on the diversity and composition of skin but not gut microbial communities. Specifically, we observed a suppressive effect of high social density on skin microbial alpha diversity as well as an overabundance of phyla associated with diseases and bite wounds in the high-density colony. Our findings suggest that skin microbial communities may be more sensitive to external factors, whereas gut communities are more tightly regulated by the host. Overall, this study highlights the importance of considering multiple body sites and their distinct microbial communities to develop a more comprehensive understanding of the factors shaping microbial diversity and composition in marine mammals.

microbiology↗

Sustainability in the laboratory: evaluating the reuseability of microtiter plates for PCR and fragment detection

1.Single-use plastics (SUPs) are indispensable in laboratory research, but their disposal contributes substantially to environmental pollution. Consequently, reusing common SUP items such as microtiter plates represents a promising strategy for improving laboratory sustainability. However, the key challenge lies in determining whether SUP reuse can be implemented without sacrificing data quality. To investigate this, we conducted a simple experiment to assess the impact of reusing microtiter plates on microsatellite genotyping accuracy. Plates previously used for PCR and fragment detection were cleaned opting for an environmentally friendly approach using regular soap and then reused. Our results indicate that, while reusing PCR plates significantly increases genotyping error rates due to residual DNA contamination, detection plates can be reused without compromising data quality. Our approach offers laboratories a practical and sustainable option for reducing SUP waste and costs while maintaining research integrity.

molecular biology↗

Little evidence for inbreeding depression for birth mass, survival and growth in Antarctic fur seal pups

Inbreeding depression, the loss of offspring fitness due to consanguineous mating, is generally detrimental for individual performance and population viability. We therefore investigated inbreeding effects in a declining population of Antarctic fur seals at Bird Island, South Georgia. Here, localised warming has reduced the availability of the seals staple diet, Antarctic krill, leading to a temporal increase in the strength of viability selection against inbred offspring, which are increasingly failing to recruit into the adult breeding population. However, it remains unclear whether viability selection operates before or after nutritional independence at weaning. We therefore used microsatellite data from 884 pups and their mothers, and SNP array data from 100 mother-offspring pairs, to quantify the effects of individual and maternal inbreeding on three important neonatal fitness traits: birth mass, survival and growth. We did not find any clear or consistent effects of inbreeding on any of these traits. This suggests that viability selection filters inbred individuals out of the population as juveniles during the time window between weaning and recruitment. Our study brings into focus a poorly understood life-history stage and emphasises the importance of understanding the ecology and threats facing juvenile pinnipeds.

evolutionary biology↗

Low heritability and high phenotypic plasticity of salivary cortisol in response to environmental heterogeneity in fur seals

Individuals are unique in how they interact with and respond to their environment. Correspondingly, unpredictable challenges or environmental stressors often produce an individualized response of the hypothalamic-pituitary-adrenal axis and its downstream effector cortisol. We used a fully crossed, repeated measures design to investigate the factors shaping individual variation in baseline cortisol in Antarctic fur seal pups and their mothers. Saliva samples were collected from focal individuals at two breeding colonies, one with low and the other with high density, during two consecutive years of contrasting food availability. Mothers and pups were sampled concurrently at birth and shortly before weaning, while pups were additionally sampled every 20 days. We found that heritability was low for baseline cortisol, while within-individual repeatability and among-individual variability were high. A substantial proportion of the variation in baseline cortisol could be explained in pups and mothers by a combination of intrinsic and extrinsic factors including sex, weight, day, season, and colony of birth. Our findings provide detailed insights into the individualization of endocrine phenotypes and their genetic and environmental drivers in a wild pinniped. Furthermore, the strong associations between cortisol and life history traits that we report in fur seals could have important implications for understanding the population dynamics of species impacted by environmental change.

ecology↗

Movement patterns and activity levels are shaped by the neonatal environment in Antarctic fur seal pups

Tracking studies of juveniles are rare compared to those of adults, and consequently little is known about the influence of intrinsic and extrinsic factors on activity during this critical life stage. We used hourly GPS data, collected from 66 Antarctic fur seal pups from birth until moulting, to investigate the explanatory power of multiple individual-based and environmental variables on activity levels. Pups were sampled from two nearby breeding colonies of contrasting density during two subsequent years, and a two-state hidden Markov model was used to identify modalities in their movement behaviour, specifically active and inactive states. We found that movement was typified by central place exploration, with active movement away from and subsequent return to a location of inactivity. The probability of such directed exploration was unaffected by several factors known to influence marine mammal movement including sex, body condition, and temperature. Compared to pups born at the high-density colony, pups at low-density were more active, increased their activity with age, and transitioned earlier into the tussock grass, which offers protection from predators and extreme weather. Our study illustrates the importance of extrinsic factors, such as colony of birth, to early-life activity patterns and highlights the adaptive potential of movement.

animal behavior and cognition↗

Chemical patterns of colony membership and mother-offspring similarity in Antarctic fur seals are reproducible over time

Replication studies are essential for assessing the validity of previous research findings and for probing their generality. However, it has proven challenging to reproduce the results of ecological and evolutionary studies, partly because of the complexity and lability of many of the phenomena being investigated, but also due to small sample sizes, low statistical power and publication bias. Additionally, replication is often considered too difficult in field settings where many factors are beyond the investigators control and where spatial and temporal dependencies may be strong. We investigated the feasibility of reproducing original research findings in the field of chemical ecology by attempting to replicate a previous study by our team on Antarctic fur seals (Arctocephalus gazella). In the original study, skin swabs from 41 mother-offspring pairs from two adjacent breeding colonies on Bird Island, South Georgia, were analysed using gas chromatography-mass spectrometry. Seals from the two colonies differed significantly in their chemical fingerprints, suggesting that colony membership may be chemically encoded, and mothers were also chemically similar to their pups, implying that phenotype matching may be involved in mother-offspring recognition. Here, we generated and analysed comparable chemical data from a non-overlapping sample of 50 mother-offspring pairs from the same two colonies five years later. The original results were corroborated in both hypothesis testing and estimation contexts, with p-values remaining highly significant and effect sizes, standardized between studies by bootstrapping the chemical data over individuals, being of comparable magnitude. We furthermore expanded the geographic coverage of our study to include pups from a total of six colonies around Bird Island. Significant chemical differences were observed in the majority of pairwise comparisons, indicating not only that patterns of colony membership persist over time, but also that chemical signatures are colony-specific in general. Our study systematically confirms and extends our previous findings, while also implying that temporal and spatial heterogeneity need not necessarily negate the reproduction and generalization of ecological research findings.

ecology↗

A 90K SNP array uncovers inbreeding and cryptic relatedness in an Antarctic fur seal breeding colony

High density single nucleotide polymorphism (SNP) arrays allow large numbers of individuals to be rapidly and cost-effectively genotyped at large numbers of genetic markers. However, despite being widely used in studies of humans and domesticated plants and animals, SNP arrays are lacking for most wild organisms. We developed a custom 90K Affymetrix Axiom array for an intensively studied pinniped, the Antarctic fur seal (Arctocephalus gazella). SNPs were discovered from a combination of genomic and transcriptomic resources and filtered according to strict criteria. Out of a total of 85,359 SNPs tiled on the array, 75,601 (88.6%) successfully converted and were polymorphic in 274 animals from a breeding colony at Bird Island in South Georgia. Evidence was found for inbreeding, with three genomic inbreeding coefficients being strongly intercorrelated and the proportion of the genome in ROH being non-zero in all individuals. Furthermore, analysis of genomic relatedness coefficients identified multiple second and third order relatives among a sample of ostensibly unrelated individuals. Such "cryptic relatedness" within fur seal breeding colonies may increase the likelihood of consanguinous matings and could therefore have implications for understanding fitness variation and mate choice. Finally, we demonstrate the cross-amplification potential of the array in three related species. Overall, our SNP array will facilitate future studies of Antarctic fur seals and has the potential to serve as a more general resource for the wider pinniped research community.

evolutionary biology↗

RAD sequencing and a hybrid Antarctic fur seal genome assembly reveal rapidly decaying linkage disequilibrium, global population structure and evidence for inbreeding

Recent advances in high throughput sequencing have transformed the study of wild organisms by facilitating the generation of high quality genome assemblies and dense genetic marker datasets. These resources have the potential to significantly advance our understanding of diverse phenomena at the level of species, populations and individuals, ranging from patterns of synteny through rates of linkage disequilibrium (LD) decay and population structure to individual inbreeding. Consequently, we used PacBio sequencing to refine an existing Antarctic fur seal (Arctocephalus gazella) genome assembly and genotyped 83 individuals from six populations using restriction site associated DNA (RAD) sequencing. The resulting hybrid genome comprised 6,169 scaffolds with an N50 of 6.21 Mb and provided clear evidence for the conservation of large chromosomal segments between the fur seal and dog (Canis lupus familiaris). Focusing on the most extensively sampled population of South Georgia, we found that LD decayed rapidly, reaching the background level of r2 = 0.09 by around 26 kb, consistent with other vertebrates but at odds with the notion that fur seals experienced a strong historical bottleneck. We also found evidence for population structuring, with four main Antarctic island groups being resolved. Finally, appreciable variance in individual inbreeding could be detected, reflecting the strong polygyny and site fidelity of the species. Overall, our study contributes important resources for future genomic studies of fur seals and other pinnipeds while also providing a clear example of how high throughput sequencing can generate diverse biological insights at multiple levels of organisation.

evolutionary biology↗