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Biology subjects

Hoffman, J. I.

Publications and source records attributed to Hoffman, J. I..

At least 19 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↗

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↗

Can the marginal male hypothesis explain spatial density variation in pinnipeds?

The marginal male hypothesis is a mechanism proposed to explain gregariousness, for example in pinnipeds. Here, we explore whether this mechanism, combined with density-dependent pup survival, can also account for heterogeneity in density across colonies, as observed for example in Antarctic fur seals (Arctocephalus gazella). We build a discrete-time matrix model inspired by the Antarctic fur seal to investigate how differences in density between two colonies can emerge through mate choice and density-dependent pup mortality. Our model assumes a heritable male colony preference that is coupled to competitive ability, i.e. a local siring advantage. Female colony preference is modelled as an independent trait that is allowed to evolve separately. Pup survival decreases with local density. Based on numerical analysis of the model, we find slight differences in density between the colonies at equilibrium. When siring advantage is high, and the survival penalty for males with siring advantage is low, the colony that is preferred by the high-quality males actually becomes the less dense colony. Our model serves as a proof of concept that such density differences can emerge. We expect that by including additional environmental factors, future models will explain a larger part of the observed variation in density.

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↗

Sex-dependent influence of major histocompatibility complex diversity on fitness in a social mammal

Parasite infections affect males and females differently across a wide range of species, often due to differences in immune responses. Generally, females tend to have stronger immune defenses and lower parasite loads than males. The major histocompatibility complex (MHC) plays a crucial role in the adaptive immune response, and extensive research has explored how variation in this region influences infection and fitness outcomes. However, studies of sex-specific relationships between MHC variation and infection are scarce, perhaps because MHC genes are located on the autosomes, which are shared by both sexes. Here, we provide evidence of sexually antagonistic selection in a wild, group-living mammal--the banded mongoose. Using genetic and life history data collected from over 300 individuals across 25 years, we found that particularly MHC class I (MHC-I) but also MHC class II (MHC-II) diversity influence lifetime reproductive success differently in males and females. Specifically, higher MHC diversity is linked to increased fitness in males but decreased fitness in females. Furthermore, MHC diversity did not differ between the sexes, indicating an unresolved genetic sexual conflict. Our findings demonstrate that sexually antagonistic selection acts on the MHC and may operate across both MHC classes but differently. This study contributes to the growing body of evidence that sex is a significant factor in shaping host immunity and fitness.

evolutionary biology↗

A haplotype-resolved chromosomal reference genome for the porcini mushroom Boletus edulis

Haplotype-resolved chromosomal reference genomes are increasingly available for many fungi, offering insights into the evolution of pathogenic and symbiotic lifestyles. However, these resources remain scarce for ectomycorrhizal fungi (EMF), which play crucial roles in forest ecosystems. Here, we used a combination of chromatin conformation capture (Hi-C) and PacBio sequencing to construct a haplotype-resolved chromosomal genome assembly for Boletus edulis, an emerging model for EMF research and a prized edible fungus. Our new reference assembly, "BolEdBiel_h2", derives from a sporocarp sampled in Bielefeld, Germany. The genome assembly spans 41.8 Mb, with a scaffold N50 of 4.1 Mb, and includes 11 chromosome-level scaffolds, achieving near telomere-to-telomere coverage across multiple chromosomes. We annotated 15,406 genes, with a Benchmarking Universal Single-Copy Orthologs (BUSCO) score of 96.2%. Key genomic features such as mating loci, CAZymes, and effector proteins, were mapped across the assembly. As a first application of this new genomic resource, we mapped whole genome resequencing data from 49 genets to investigate the population structure and genetic diversity of the European lineage of B. edulis. We identified five distinct genetic clusters and found that high-latitude populations from Iceland and Fennoscandia exhibited greater nucleotide diversity than populations from the United Kingdom and central Europe. Additionally, we discovered a 0.4 Mb inversion on chromosome three and identified several regions of locally elevated nucleotide diversity, which may represent candidates for ecological adaptation. This genomic resource will facilitate a deeper understanding of this ecologically and commercially important wild fungus.

evolutionary biology↗

The gut microbiota-immune-brain axis in a wild vertebrate: dynamic interactions and health impacts

The gut microbiota-immune-brain axis is a feedback network which influences diverse physiological processes and plays a pivotal role in overall health and well-being. Although research in humans and laboratory mice has shed light into the associations and mechanisms governing this communication network, evidence of such interactions in wild, especially in young animals, is lacking. We therefore investigated these interactions during early development in a population of common buzzards (Buteo buteo) and their effects on individual condition. In a longitudinal study, we used a multi-marker approach to establish potential links between the bacterial and eukaryotic gut microbiota, a panel of immune assays and feather corticosterone measurements as a proxy for long-term stress. Using Bayesian structural equation modelling, we found no support for feedback between gut microbial diversity and immune or stress parameters. However, we did find strong relationships in the feedback network. Immunity was negatively correlated with corticosterone levels, and microbial diversity was positively associated with nestling body condition. Furthermore, corticosterone levels and eukaryotic microbiota diversity decreased with age while immune activity increased. The absence of conclusive support for the microbiota-immune-brain axis in common buzzard nestlings, coupled with the evidence for stress mediated immunosuppression, suggests a dominating role of stress-dominated maturation of the immune system during early development. Confounding factors inherent to wild systems and developing animals might override associations known from adult laboratory model subjects. The positive association between microbial diversity and body condition indicates the potential health benefits of possessing a diverse and stable microbiota.

microbiology↗

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↗

From populations to pan-genomes: investigating the role of ecology and genomic architecture in maintaining species boundaries in the porcini mushroom, Boletus edulis

Hybridization among diverged species is common across all domains of eukaryotic life, but appears to be particularly common in fungi. However, some fungi exhibit a greater tendency for hybridization than others and it is unclear what mechanisms facilitate or prevent hybridization. Here, we generated 253 whole genome sequences and 22 reference genomes within the globally distributed ectomycorrhizal species complex Boletus edulis Bull. and use a multi-faceted genomic approach to identify patterns of ongoing hybridization and determine whether hybridization is mediated by changes in genome structure, ecology, or both. We found that hybridization is common among species of B. edulis despite 2.1 million years of divergence. However, not all lineages that hybridize today exhibit patterns of introgression, indicating the presence of strong reproductive boundaries among some species. Using a pan-genomic approach we find that genome structural variation is abundant within B. edulis, but that the presence of ongoing introgression does not correlate with genome structural similarity or overall gene content. Instead, we find that the composition of ecologically relevant gene families more accurately predicts the presence of introgression among lineages and B. edulis as a group may specialize on chitin decomposition. Altogether, we show that ecological preferences are likely the primary driver of reproductive barriers in B. edulis.

evolutionary biology↗

Genetic diversity and demographic history of the leopard seal: a Southern Ocean top predator

Leopard seals (Hydrurga leptonyx) are top predators that can exert substantial top-down control of their Antarctic prey species. However, population trends and genetic diversity of leopard seals remain understudied, limiting our understanding of their ecological role. We investigated the genetic diversity, effective population size and demographic history of leopard seals to provide fundamental data that contextualizes their predatory influence on Antarctic ecosystems. Ninety leopard seals were sampled in the northern Antarctic Peninsula, during the austral summers of 2008-2019 and a 405bp region of the mitochondrial control region was sequenced for each individual. We uncovered moderate levels of nucleotide ({pi} = 0.013) and haplotype (Hd = 0.96) diversity, and the effective population size was estimated at around 24,000 individuals (NE = 24,376; range 16,876 - 33,126). Consistent with findings from other ice-breeding pinnipeds, Bayesian skyline analysis also revealed evidence for population expansion during the last glacial maximum, suggesting that historical population growth may have been boosted by an increase in the abundance of sea ice. Although leopard seals can be found in warmer, sub-Antarctic locations, the species core habitat is centered around the Antarctic, making it inherently vulnerable to the loss of sea ice habitat due to climate change. Therefore, detailed assessments of past and present leopard seal population trends are needed to inform policies for Antarctic ecosystems.

genetics↗

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↗

Where are the beachmasters? Unexpectedly weak polygyny among southern elephant seals on a South Shetland Island

Intraspecific variation in animal mating systems can have important implications for ecological, evolutionary and demographic processes in wild populations. For example, patterns of mating can impact social structure, dispersal, effective population size and inbreeding. However, few species have been studied in sufficient detail to elucidate mating system plasticity and its dependence on ecological and demographic factors. Southern elephant seals (Mirounga leonina) have long been regarded as a textbook example of a polygynous mating system, with dominant beachmaster males controlling harems of up to several hundred females. However, behavioural and genetic studies have uncovered appreciable geographic variation in the strength of polygyny among elephant seal populations. We therefore used molecular parentage analysis to investigate patterns of parentage in a small satellite colony of elephant seals at the South Shetland Islands. We hypothesised that dominant males would be able to successfully monopolise the relatively small numbers of females present in the colony, leading to relatively high levels of polygyny. A total of 424 individuals (comprising 33 adult males, 101 adult females and 290 pups) sampled over eight years were genotyped at 20 microsatellites and reproductive success was analysed by genetically assigning parents. Paternity could only be assigned to 31 out of 290 pups (10.7%), despite our panel of genetic markers being highly informative and the genotyping error rate being very low. The strength of inferred polygyny was weak in comparison to previous genetic studies of the same species, with the most successful male fathering only seven pups over the entire course of the study. Our results show that, even in a species long regarded as a model for extreme polygyny, male reproductive skew can vary substantially among populations.

animal behavior and cognition↗

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↗

Early sexual dimorphism in the developing gut microbiome of northern elephant seals

The gut microbiome is an integral part of a species ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals during a critical developmental window of six weeks after weaning, when the pups stay ashore without feeding. We show that the early-life gut microbiome is already substantially different in male and female pups, even though males and females cannot yet be distinguished morphologically. Sex and age both explain around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual show high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity is explained by health status, but healthy individuals have a greater microbial alpha diversity than their non-healthy peers. Across the post-weaning period, the elephant seal gut microbiome is highly dynamic. We found evidence for several colonisation and extinction events as well as a decline in Bacteriodes and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness is correlated with gut microbiome similarity in males but not females, again reflecting substantial early sex-differences. Our study represents a naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.

molecular biology↗

Recent demographic histories and genetic diversity across pinnipeds are shaped by anthropogenic interactions and mediated by ecology and life-history

A central paradigm in conservation biology is that population bottlenecks reduce genetic diversity and negatively impact population viability and adaptive potential. In an era of unprecedented biodiversity loss and climate change, understanding both the determinants and consequences of bottlenecks in wild populations is therefore an increasingly important challenge. However, as most studies have focused on single species, the multitude of potential drivers and the consequences of bottlenecks remain elusive. Here, we used a comparative approach by integrating genetic data from over 11,000 individuals of 30 pinniped species with demographic, ecological and life history data to elucidate the consequences of large-scale commercial exploitation by 18th and 19th century sealers. We show that around one third of these species exhibit strong genetic signatures of recent population declines, with estimated bottleneck effective population sizes reflecting just a few tens of surviving individuals in the most extreme cases. Bottleneck strength was strongly associated with both breeding habitat and mating system variation, and together with global abundance explained a large proportion of the variation in genetic diversity across species. Overall, there was no relationship between bottleneck intensity and IUCN status, although three of the four most heavily bottlenecked species are currently endangered. Our study reveals an unforeseen interplay between anthropogenic exploitation, ecology, life history and demographic declines, sheds new light on the determinants of genetic diversity, and is consistent with the notion that both genetic and demographic factors influence population viability.

evolutionary biology↗