Our group is currently working on the following projects:
Heterozygosity and fitness in fur seals
Pinnipeds are challenging to study as they are semi-aquatic, breed in remote and crowded colonies, and can be highly aggressive. Fortunately, a scaffold walkway above a colony of Antarctic fur seals (Arctocephalus gazella) at Bird Island, South Georgia, allows all of the animals that come ashore to be studied with minimal disturbance. In collaboration with Dr Jaume Forcada of the British Antarctic Survey, we have analysed genetic samples collected over two decades to discover the parentage of over a thousand pups. A remarkable picture of breeding behaviour has emerged. The most successful males appear to arrive first in the colony, stay for more days per season and come ashore for more seasons in total. However, although the traditional picture is one in which males fight each other for access to females, the opposite appears to be true; males stay rooted to the spot while females appear to actively choose their partners. We have also shown that heterozygosity correlates with virtually every male fitness trait measurable, including territory-holding ability, body size, reproductive success and even attractiveness. More recently, we found that increasingly frequent adverse climactic events correlated with low food availability have led to profound phenotypic changes in the population, including an 8% decline in pup birth weight since the mid 1980s. In parallel, average breeding female heterozygosity has increased by 17% over the past two decades, consistent with a temporal increase in the strength of viability selection on homozygous offspring. We are now using a high-density single nucleotide polymorphism array to explore this phenomenon in greater detail.
Funded by: the DFG
Niche choice and conformance in fur seals
Population density is an important niche dimension that varies dynamically over both space and time. Consequently, selection should favour plastic responses such as niche choice (individuals selecting niches to which their own phenotypes are a good fit) and niche conformance (individuals altering their behaviour or physiology to fit their niche). These responses could have major implications for individual fitness, ecological and evolutionary dynamics, adaptation to environmental change and evolutionary potential, yet they remain poorly understood in natural populations. In Antarctic fur seals, naturally occurring variation in the density of breeding colonies presents opportunities and challenges to fur seal mothers and their pups, as high-density colonies offer breeding females greater freedom to exercise mate choice but are also associated with increased social stress and offspring mortality. Female niche choice thus determines the social environment of their offspring, leading to the prediction that pups should maximise their fitness by altering their behaviour and physiology accordingly. Together with Dr Jaume Forcada, we are exploiting a “natural experiment” provided by two neighbouring fur seal colonies of high and low density to evaluate the fitness consequences of maternal niche choice and offspring niche conformance. We are using an integrative approach combining fieldwork with hormonal analysis, immune profiling and genomics. This should provide highly detailed and multi-faceted insights into the fitness consequences of maternal niche choice as well as the behavioural, genetic and endocrinological mechanisms by which offspring may cope with variation in their social environment.
Funded by: the DFG (SFB, TRR 212, NC3)
Population genetics of Southern Ocean predators
Many animal populations have been strongly affected by anthropogenic influences and climate change. The amount of genetic variation within a species determines its capacity to respond to selection and hence to adapt to these changing pressures. However, a species’ adaptive potential is also likely to be influenced by its demographic history and by the magnitude of gene flow between populations. Top-trophic high-latitude predators are likely to be among the first to show the impacts of environmental change because their prey are directly affected by bottom-up ecosystem changes. Consequently, it is of interest to understand how genetic variability, historical demography and population structure may interact to shape the future resilience of these species. Together with Dr Andy Lowther and Prof Kit Kovacs, we are using molecular markers to compare and contrast the circumpolar population structures and historical demographies of two key Southern Ocean predators, the Antarctic fur seal (Arctocephalus gazella) and macaroni penguin (Eudyptes chrysolophus). We will also evaluate the ‘krill surplus hypothesis’, which predicts that macaroni penguin populations may be in decline as a consequence of increasing competition for food with other top-predator species, such as the fur seals.
Funded by: the Norwegian Research Council
Pinniped population genetics
We also work collaboratively on a variety of other pinniped species, including grey seals (Halichoerus grypus), South American fur seals (Arctocephalus australis), Southern sea lions (Otaria flavescens), Northern elephant seals (Mirounga angustirostris), Southern elephant seals (Mirounga leonina) and Steller’s sea lions (Eumetopias jubatus). Many of these projects are using molecular genetic approaches to shed light on population structure and demographic histories, both of which may have important implications for conservation. For example, our work on Steller’s sea lions revealed a clear phylogenetic break within the range of this threatened ‘flagship’ species, in support of previous mitochondrial studies revealing two discrete stocks, and in line with the observation that two stocks show opposite growth trajectories.
Mechanisms underlying heterozygosity-fitness correlations
Many important fitness traits including parasite resistance, survivorship and reproductive success often correlate with heterozygosity in natural populations. Such heterozygosity-fitness correlations (HFCs) have the potential to influence interactions between pathogens and their hosts, and the evolution of mate choice. However, HFCs have become the focus of a long-standing debate as most studies use only around ten microsatellite markers. While this number is enough to detect many HFCs, it is too few to elucidate which of two possible mechanisms could be most important. In collaboration with Dr Kanchon Dasmahapatra, we are helping to resolve this question through the application of high-throughput sequencing.
Sea lion speciation genomics
One hundred and fifty years after Charles Darwin’s seminal work On the Origin of Species, the quest for the mechanistic underpinnings of speciation has begun in earnest. Among the most promising systems to reveal the evolutionary processes that control adaptation and govern the early steps of speciation are evolutionary young lineages diverging along strong environmental gradients. In particular, marine species provide ideal systems in which to test whether ecologically divergent selection in the absence of physical barriers to gene flow can lead to heterogeneous genomic divergence. Sea lions from the Galápagos provide just such a system. The species has a tiny geographic range relative to its dispersal capability but occupies a steep environmental cline between the nutrient-rich grounds around the young western islands and the islands on the shallow central shelf of the archipelago. These environmental contrasts translate into marked differences in morphology, diet and the underlying genetics. In collaboration with Prof Jochen Wolf, we are using whole-genome resequencing to quantify patterns of genomic divergence at base-pair resolution between ecologically and genetically divergent sea lion populations.
Funded by: the DFG
Olfactory communication in pinnipeds
Olfactory communication underpins virtually all aspects vertebrate social life, from mother-offspring communication through kin recognition to mate choice. In particular, odour seems to be an important pathway for signalling complex information about an individual’s genetic makeup, such as heterozygosity and relatedness. However, the extreme complexity of vertebrate odours has largely precluded a mechanistic understanding of the link between odour and genotype. Antarctic fur seals provide an ideal model system for studying olfactory communication in a free-ranging marine mammal. In this species, olfaction is important for the close-range recognition of pups and breeding females also show mate choice for partners who are heterozygous and unrelated, implying that genotype could be encoded in scent. Together with Prof Barbara Caspers, we are combining gas chromatography-mass spectrometry (GC-MS) with microbiome sequencing and genetic analysis to shed light on the molecular mechanisms underlying chemical communication.
The costs and benefits of inbreeding
Although inbreeding is usually detrimental to fitness, theory predicts that it could have a substantial positive effect on inclusive fitness by increasing the benefits of cooperation. In collaboration with Prof Mike Cant and Dr Hazel Nichols, we are exploring the causes and consequences of inbreeding using rich, multigenerational data from a long-term study of a cooperatively breeding mammal, the banded mongoose (Mungos mungo).
Funded by: the DFG
Sexual trait expression in black grouse
Since Darwin first coined the term “sexual selection” to explain the evolution of exaggerated male traits, we have come to understand the complex interrelationships among these traits, the information they encode and the life histories of the animals they are embedded into. Sexual selection is built on the idea that individual quality is signaled by the expression of these traits, yet a clear mechanistic understanding of the genetic architectures of sexual traits and the mechanisms regulating sexual trait expression remains elusive. Together with Dr Carl Soulsbury and Prof Kees van Oers, we are combining the genomic inference of inbreeding with genome-wide methylation analysis to investigate the genetic and epigenetic mechanisms affecting sexual trait expression and reproductive success in a classical lek model system, the black grouse, Lyrurus tetrix.
Funded by: the DFG
Shorebird ecology and conservation
Sex ratio biases are widespread in nature and represent a fundamental component of sexual selection. They can also have a strong influence on population viability and persistence. Small plovers (Charadrius spp.) exhibit diverse mating systems, ranging from monogamy to polygyny. Consequently, in collaboration with Prof Oliver Krüger, Prof Tamás Székely and Dr Nayden Chakarov, we are studying sympatric populations of three species in Madagascar, using a combination of molecular genetic and demographic modelling approaches, to identify the underlying factors that drive adult sex ratio variation.
Funded by: the DFG
Seascape genetics in the cold
The persistence of a species within a changing environment depends on a number of factors. Arguably the most important of these is the ability of local populations to acclimate to changing conditions, but population genetic connectivity is also crucial as this determines the extent to which beneficial alleles can spread among populations. However, the factors that affect genetic connectivity are still poorly understood, particularly in the marine realm where intrinsic factors such as life history may interact with multiple physical variables including ocean currents, sea bed topology and substrate type. Together with Prof Lloyd Peck and Prof Melody Clark of the British Antarctic Survey, we are using an unusually large collection of samples of a brooding Antarctic marine mollusc Margarella antarctica to elucidate how various factors shape the population genetic structure of a dispersal-restricted marine invertebrate over multiple geographic scales, from hundreds of kilometres down to as little as one metre. We will use a spatially explicit modelling framework incorporating genetic data from over a hundred locations on the Western Antarctic Peninsula, one of the fastest-warming regions of the planet. There is an imperative to understand and predict how the endemic, slowly evolving, cold-adapted fauna of this region will cope with ongoing climate change.
Funded by: the DFG
Phenotypic plasticity, local adaptation and climate change responses
One of the most topical questions in science and one of the issues of greatest concern to society is how life on earth will respond to climate change. This is particularly important for species living in polar areas where the most rapid and profound changes are occurring. However, predicting species responses requires a detailed understanding of the genetic basis of variation in individual fitness. Our recent study in Nature has shown that climate change is exerting increasingly strong viability selection on an Antarctic fur seal population, specifically against relatively homozygous offspring. However, it is actually marine invertebrates that are at the greatest risk under future climate change scenarios due to the warming and acidification of the World’s oceans. Consequently, together with Prof Lloyd Peck and Prof Melody Clark of the British Antarctic Survey, we have begun to apply genomic tools to elucidate the mechanisms by which Antarctic marine invertebrates may respond to environmental change. For example, we recently used reciprocal transplant experiments together with transcriptome sequencing to investigate the molecular basis of phenotypic plasticity in an Antarctic limpet, Nacella concinna. We are also using a novel approach based on heated settlement panels to assess the in situ effects of warming on marine encrusting communities in polar seas. We recently reported in Nature Communications that Antarctic encrusting communities fail to acclimate to 18 months of localised warming to either +1 °C or +2 °C above ambient temperature.
Funded by: Natural Environment Research Council
Population dynamics, dispersal and adaptation in Porcini mushrooms
Ectomycorrhizal fungi are critical components of terrestrial ecosystems that play essential roles in nutrient recycling. Consequently, there is a pressing need to study their population dynamics and life histories so as to better understand how ecosystems function and persist. In particular, we need to learn how these fungi disperse, colonise new habitats, persist, adapt to their hosts and, in the longer term, speciate. Together with Prof Bill Amos, Dr Kanchon Dasmahapatra and Prof Bryn Dentinger, we are studying the population genetics of the iconic edible mushroom, Boletus edulis, known variously as the penny bun, cèpe de Bordeaux, porcino or Steinpilz. We are currently using microsatellites to genotype a large collection of B. edulis samples that have been systematically gathered from sites in Germany and the UK over the last ten years. We hope to use whole-genome sequencing to unravel genome-wide patterns of divergence in relation to geography and host species.
In alphabetical order
Prof Karina Acevedo-whitehouse, Autonomous University of Queretaro, Mexico
Prof William Amos, University of Cambridge, UK
Dr Alastair Baylis, Macquarie University, Sydney
Prof Pierre Boudry, Institut français de recherche pour l’exploitation de la mer, France
Prof Mike Cant, University of Exeter, UK
Prof Barbara Caspers, Bielefeld University, Germany
Dr Francisco Ceballos, Middle East Technical University, Turkey
Dr Nayden Chakarov, Bielefeld University, Germany
Dr Greg Charrier, Université de Bretagne Occidentale, France
Prof Melody Clark, British Antarctic Survey, UK
Dr Kanchon Dasmahapatra, University of York, UK
Prof Patrice David, Centre d’Ecologie Fonctionnelle et Evolutive, France
Dr Bryn Dentinger, Natural History Museum of Utah, USA
Dr Farnon Elwood, University of the West of England, UK
Dr Jaume Forcada, British Antarctic Survey, UK
Dr Mike Goebel, National Oceaninc and Atmospheric Administration, USA
Prof Liz Harper, Cambridge University, UK
Dr Marty Kardos, National Oceanic and Atmospheric Administration, USA
Prof Kit Kovacs, Norwegian Polar Institute, Norway
Prof Oliver Kruger, Bielefeld University, Germany
Dr Kim Last, Scottish Association for Marine Science, UK
Dr Florian Leese, Ruhr Universität Bochum, Germany
Dr Andy Lowther, Norwegian Polar Institute, Norway
Dr Aurelio Malo, Universidad de Alcalá, Spain, and Oxford University, UK
Dr Frank Melzner, GEOMAR, Germany
Prof Caroline Müller, Bielefeld University, Germany
Dr Hazel Nichols, Swansea University, UK
Prof Lloyd Peck, British Antarctic Survey, UK
Dr Larissa Rosa de Oliveira, Universidade do Vale do Rio dos Sinos, Brazil
Prof Jon Slate, Sheffield University, UK
Dr Carl Soulsbury, University of Lincoln, UK
Dr Iain Staniland, British Antarctic Survey, UK
Prof Tamás Székely, University of Bath, UK
Prof Kees van Oers, Netherlands Institute of Ecology and Wageningen University, the Netherlands
Dr Tom Wilding, Scottish Association for Marine Science, UK
Prof Mary Wisz, World Maritime University, Sweden
Prof Jochen Wolf, Ludwig Maximilian University of Munich, Germany
Dr Sama Zefania, University of Toliary, Madagascar