Biology Issue Three | 2014 News www.biology.ox.ac.uk

Department of Sciences Department of Zoology 2 Biology News, University of Oxford I Issue Three I 2014

Liam Dolan Head of Department of Plant Sciences Trees loom large in the highlights of the Department this year

represents a commitment by the Depart- allow policy makers to prioritise species and ment and University to forest science and regions of forest for conservation. Adoption

John Baker has been enabled by the kind generosity of of his recommendations in Ghana have been Sir Martin and Lady Audrey Wood, and the the basis for laws enacted in the late 1990s to Patsy Wood Trust. protect the sustainability of forestry activities and underpinned the adoption of a bilateral David Boshier was central to the develop- agreement for the licensing of timber for ment of “A Future with Broadleaved Trees”, export from Ghana to the European Union a strategy for the improvement of broad- which came into effect in 2013. This demon- leaved trees in Britain and Ireland until strates the contribution of scientific knowl- 2035. This represents the first comprehen- edge to the development of policies that can sive attempt to develop an integrated strat- safeguard forests for future generations. egy for the delivery of resources required to conserve and develop broad leaved trees Trees will be an important part of the in the face of invasive diseases and climate future of the Department. We look change. It builds on the local collaboration forward to developing this theme with with the Earth Trust, which is based at Lit- the collaboration of our extensive network tle Wittenham, and founded by ex-members of partners. of the Department more than 30 years ago. As we were going to press, we were very sad- Liam Dolan As part of the assessment of research in dened by news of the death of Professor Lor- UK universities (Research Excellence na Casselton, who had been Foreign Secretary John MacKay is the inaugural Wood Chair Framework) the Department submitted an and Vice President of the Royal Society until in Forest Science and joined the Depart- Impact Case based on William Hawthorne’s 2011 and taught first year genetics practicals ment in October 2013. John has made groundbreaking research on forest bio- until a few weeks before her death. Lorna enormous contributions to our understand- diversity. William has been on a campaign wrote an article for Biology News outlining ing the genetic diversity of conifers and to map and rate centres of biological some of her contributions to fungal genetics was one of the lead authors on the publica- diversity around the world. As part of this and it can be found on page 6. tion that reported the sequence of program he has developed new protocols the Norway Spruce. John’s appointment for efficiently surveying diversity that

Graduate student projects Diversity in hotspots geometry and morphogenesis Trypanosome pathogens of Cicely Marshall (Merton College) Charlotte Kirchelle (St Cross College) Eleanor Jaskowska (Keble College) The world’s rarest Plant cells are Trypanosomatids plant species are fixed in their are a monophyletic

not distributed John Baker relative position group of unicellular evenly around in the tissue by , found

William Hawthorn the world, but are their surrounding in both free-living

found aggregated rigid cell wall, Olga Sedelnikova Baker and parasitic in regions called and cells in organ forms. Evolved hotspots. While primordia have from a common hotspots are striking polyhedral ancestor, species relatively well geometries. of trypanosomatid characterised at the species level, we Changes in cell geometry and growth have cause pathologies in hosts from crocodiles know little about their genetic signatures. to be coordinated to give rise to organs to cassava. Despite being discovered My research examines genetic diversity of defined shape. RAB-A5c is a regulatory in plants over 100 years ago we know in hotspots to ask whether hotspots are component involved in membrane almost nothing about their biology. My promoting novel diversity. I am trafficking and identifies geometric edges research is focused on parasite cell surface building community phylogenies and of cells as distinct spatial domains with an which interact with plant species haplotype maps for hotspots apparent function in cell geometry control. immune system. Aside from improving in West Africa to ask what contribution Using a combination of 4D imaging, our knowledge of how these pathogens recent lineage diversification has made genetic, biochemical and biophysical interact with host crops such as coffee and to the biodiversity patterns we observe. techniques, I am testing the hypothesis palm oil, we might also uncover new clues Are hotspots also hotbeds of genetic that RAB-A5c acts through controlling the as to how the ancestral trypanosomatid innovation, or is their high endemism mechanical properties of cellular edges. surface has been adapted to exploit due to harbouring relictual lineages different host environments. now extinct elsewhere? www.biology.ox.ac.uk Biology News, University of Oxford I Issue Three I 2014 3

Peter Holland Head of Department of Zoology Does Zoology have ‘impact’?

We will always argue that fundamental the future of the Large Blue butterfly in curiosity-driven research is essential, the UK, Alex Rogers’ group has made partly since surely it is important (and major strides in assessing risk to threat- interesting!) to understand how the ened deep-sea habitats, and – amongst world works, but also because some the success stories from our Wildlife far-reaching impacts come in quite Conservation Research Unit – Claudio unexpected ways. Recently, we reviewed Sillero and David Macdonald developed the ‘impacts’ that have come from a novel rabies vaccination strategy that research in the Department of Zool- is safeguarding the Ethiopian wolf. ogy, and I think you will agree that the In welfare, Marian Dawkins’ diversity is impressive. For example, research has transformed the welfare Luke Alphey’s research showed how of commercially-reared poultry and genetic modification could be applied influenced EU Directives and industry to engineer sterile insects for the fight practice (and was recognised by a well- against mosquito-borne diseases; a deserved CBE in the 2014 New Years’ spin-out company (Oxitec) was formed Honours). Most surprisingly of all, who to develop the idea, and the method would have predicted that software is in trials in Brazil and the Cayman technology underpinning blockbuster Islands. Simon Hay’s work creates risk computer games such as Star Wars: maps for malaria and other diseases, The Force Unleashed and Clumsy Ninja Peter Holland which governments and agencies use stemmed from animal movement re- extensively. Oliver Pybus and col- search in the Department of Zoology? One word that is never far from the leagues developed methods for tracking These are just a few examples, and there agenda today is ‘impact’. Increasingly, and predicting the transmission and is much more to come, but hopefully Universities are being challenged to of pathogens; these became even this snapshot shows that funding demonstrate that research, especially part of the official UK response to the research in Zoology, and training the if funded from public funds (Research 2009 H1N1 ‘Swine Flu’ pandemic and next generation of Biological Science Councils and HEFCE), is having are used extensively in other countries undergraduates, really can have impact. positive effects on the health, wealth, too. In the conservation arena, Jeremy or well-being of people and the planet. Thomas’ ecological work has secured

Graduate student projects

Octocoral communities of Mesoamerican Conservation of the Persian leopard Evolution and developmental roles Caribbean reefs Mohammad Farhadinia (Lady Margaret Hall) of microRNAs Vanessa Lovenburg (New College) Shan Quah (Merton College) The Persian leopard Coral reefs are is the largest cat MicroRNAs under threat in west Asia, and (very small RNA from anthropo- is considered to molecules that Peter Holland Jenny Murray genic and natural be endangered do not code for forces such as Taghdisi Mohammad – poaching and proteins) are climate change, habitat degradation known to regulate bleaching events, are thought to be the activity of coral disease, responsible. The , and many over-fishing, rolling mountains play important coastal develop- and high altitudes it favours present roles in embryonic ment and eutrophication. Conservation considerable challenges for scientists, and development. If we can determine how monitoring and systematic understanding it is consequently one of the least known microRNAs evolve, especially how new is essential to inform policy makers for subspecies. I am a DPhil student in the microRNAs arise in evolution, this will the development of sustainable fisheries, WildCRU (Department of Zoology) who has help us understand how development, marine protected areas, and predictive being trying to rectify this. I am exploring and therefore adult morphology, evolves. models for the future of the world’s the fundamental ecology of the population Using next-generation DNA and RNA oceans. I am studying the morphological of Persian leopards, and how these big sequencing and functional assays in cell and molecular diversity of octocoral cats interact with the humans who live culture, I am researching the evolution communities (soft corals and gorgonians) alongside. I am using a variety of modern and developmental roles of microRNAs in on the Mesoamerican Barrier Reef System. technology, including camera traps, to do mammals and Lepidoptera, discovering My fieldwork is carried out with Operation this. new microRNAs and their functions. Wallacea on the Honduran Bay Island I am funded by an A*STAR NSS (PhD) of Utila. Scholarship.

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Navigation over land and sea Many long-distance migrants return journeys become structured by prominent landscape even on remarkably fine spatial each summer to their nesting sites with landscape features – roads, rivers, railway scales. pin-point accuracy after having travelled lines, villages, and even power stations – hundreds or even thousands of kilome- strongly suggesting control by sequences Homing pigeons can be GPS-tracked tres. Carrier pigeons can arrive home of local visual landmark memories. with exquisite precision over short dis- efficiently from distant locations having Nevertheless, despite this “pilotage” we tances, but unravelling the truly staggering traversed terrain they have never visited are finding that birds continue to pay journeys of oceanic navigators requires ad- before. Navigation has long fascinated bi- attention to their time-compensated sun ditional techniques. Combining GPS, dive ologists, but much still remains unknown compass as they orient across the familiar logger, immersion logger and geolocator about the sensory and cognitive basis of the maps and compasses that use to plot these extraordinary journeys.

In the early 2000s, our group became one Zsuzsa Ákos of the first to use the unprecedented preci- sion of miniature GPS tracking devices to study navigational strategies in free-flying birds. Using homing pigeons as our chief study species, we have since uncovered a suite of unexpected phenomena, many of them overturning decades of received wis- dom about the control of avian navigation.

Pigeons rarely home directly “as the crow flies”. Instead they quickly settle on individually preferred, idiosyncratic homing routes, which are often inef- ficient, and which they faithfully repeat with little deviation – much like us taking a preferred route to work each day. Their Pigeon routes: Repeated homing flights of a pigeon, showing idiosyncratic route choice

Undergraduate student projects Elemental defence and plant-mediated Nitrogen assimilation in land plants The effects of disturbance on butter- interactions between herbivore guilds Rebecca Watkins (Somerville College) fly diversity on Buton island, Indonesia José Waterton (St Hugh’s College) Emma Crookenden (Pembroke College) I worked in Herbivores Liam Dolan’s lab I studied the effects

Anon can improve investigating of disturbance on

the feeding Caroline Trude the genetic butterflies in Sulawesi performance basis of nitrogen with Operation of others. assimilation Wallacea. A modified Edward Crookenden Edward Hyperaccumulating in Marchantia Pollard walk method plants sequester polymorpha. was used at varying high concen- The liverwort levels of disturbance. trations of metals is interesting Abundance and in their tissues; the ‘elemental defence’ to study because of its early diverging richness were hypothesis proposes that these metals position in land plant phylogeny. I similar at different disturbance levels, protect against herbivore attack. I examined conducted genetic and size analysis but population composition varied the effect that hyperaccumulation had of plants grown in different nutrient significantly. Endemic butterfly trends on such plant-mediated, facilitative conditions, and ran a mutant screen were different to the observed for interactions between herbivores. By using growing approximately 65,000 transgenic generalist species, and the importance herbivore feeding experiments in the plants on media containing chlorate. I of focusing research on species with greenhouse, I found that aphids improve identified three mutants that will now be the highest conservation value was the feeding performance of Lepidoptera used for further research into the genes highlighted. Fruit-baited traps were larvae on the hyperaccumulator Noccaea responsible for nitrogen assimilation and set to consider vertical stratification of caerulescens. This facilitative effect utilisation. I found working alongside a populations. Stratification was evident, appeared reduced on high zinc treatments; large group of researchers and students with a number of species new to the study therefore, further research is required to really helped me challenge myself, found only in the canopy. This implies that confirm whether this might be an added especially at lab meetings to dissect each certain species may be misrepresented in advantage of elemental defences. project. Pollard walk surveys.

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Recently, we have be- come interested in how birds make navigational Zsuzsa Ákos decisions within groups. Zsuzsa Ákos Birds in a flock travelling together face a problem that is ubiquitous among group- living species: how to resolve differences of opin- ion and remain cohesive. Humans can solve these problems democratically, Homing pigeon carrying miniature GPS logger by voting, or by appointing leaders whom others follow. In collabora- data we have been tracking the foraging tion with statistical physicists, and using excursions and annual migration routes high-resolution GPS data from flocks of the ocean-wandering seabirds (such of pigeons, we have identified a subtle as shearwaters and puffins) breeding on hierarchical arrangement that lies some- islands off Britain’s western coasts. Novel where between democracy and despotism: machine learning techniques allow us to go each member of the flock can have some beyond simply reconstructing routes, and input into the navigational decisions of pinpoint areas where birds stop-over to the flock, but some members’ “votes” Annual migration route of a Manx shearwater feed, dive, or rest – critical data for inform- carry more weight than those of others. ing global marine conservation efforts. Interestingly, birds near the top of this leadership in flight – is the subject of our Tracking repeat individual migrations leadership hierarchy are not necessarily ongoing research aimed at understanding also shows us that, like pigeons, seabirds more dominant socially, suggesting that how evolution has shaped animals to deal have individually idiosyncratic routes and hierarchies within the same collective are with the challenges and opportunities that destinations, confirming that the role of rearranged according to context. Why and group living offers. learning and memory extends to very long how this happens – for example whether distance oceanic navigation too. those best at navigating get to assume Dora Biro & Tim Guilford

Undergraduate student projects Modelling the interaction between Molecular characterisation of the T-Cell receptor repertoire in T cell Plasmodium falciparum var genes bacterial of two subsets during and the human sickle cell trait SWIR gastropods Kirstie McLoughlin (Brasenose College) Susan Hawkins (St Catherine’s College) Jack Howe (Hertford College) My undergraduate My project was The scaly- dissertation

with Sunetra foot Any Hong investigated Gupta, where gastropod the relationship Sally Le Page

Barry Hawkins Barry I studied the is found at between T-cell strain dynamics deep-sea clonality and of malaria and its vents in function using coevolutionary the Indian T-cell receptor interactions Ocean. As (TCR) repertoire with the human with other vent fauna, it is sustained analysis. I focused sickle cell . by a bacterial that can on the relationship between regulatory Through making harness the energetic chemistry of the and conventional T-cells using their TCR mathematical models, I discovered vent-plumes. I investigated the symbiotic sequences to track distribution of clones strain behaviours that had never been of this snail, alongside a second in these subsets. The different T-cell seen before, and it was the first time species novel to science, from a vent field subsets shared sequences (and thus clonal the effect of a haemoglobin disorder on near South Africa, to determine how they history) which indicated the potential malarial strain dynamics had ever been compared to each other and to species for using TCR repertoire as a method investigated. It was an enjoyable project from other vents. Surprisingly, the novel to explore immune responses. I really to learn how to write models, and be snail harboured at least three distinct enjoyed lab work, the success and the the first to explore malaria and sickle symbionts, and, while the scaly-foot challenges, especially developing strong cell coevolution in this way. I am now gastropod contained only one symbiont, problem-solving skills that were needed continuing this research as a DPhil the bacteria showed some divergence to to generate good data. The laboratory student, through funding from the ERC symbionts of this species collected from I worked in (Dr Adrian Smith’s) was and Clarendon Scholarship. another site. incredibly welcoming and supportive.

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Gene – the key to tracing how sex evolved in fungi evolution played an cell and are partitioned accurately by the unexpected trick. formation of a clamp. In ascomycetes the

John Baker dikaryophase is restricted within a short- Filamentous ascomy- lived fruiting body but in basidiomycetes cete fungi such as the it is the predominant stage and exists in bread mould Neurospora the soil indefinitely, constantly giving rise crassa, and basidi- to complex dikaryotic-celled fruiting bod- omycete fungi such as ies (to the delight of fungal foragers). the ink cap mushroom Coprinus cinereus have Long before cloning, it was rec- been favourite genetic ognised that genes at the MAT loci had tools for studying the essential roles in establishing and main- eukaryotic cell for over taining the dikaryophase. In unicellular 70 years. Ascomycetes basidiomycetes (such as the corn smut and basidiomycetes Ustilago maydis) secreted phero- form the Dikarya, a mones are needed for mate recognition group in which most but in filamentous forms mate attraction Coprinus spp, ink cap species are self-sterile has become superfluous and vegeta- One of the important themes of research and must mate in order to complete their tive cell fusion is sufficient to determine in the Plant Sciences Department is how cycle and produce sexual spores. whether mates are compatible. If fusion developmental pathways have evolved Mating is achieved through action of the occurs, pheromone signalling is activated during land plant evolution. Over the last MAT locus with compatible mates having intracellularly to promote migration of 25 years, the study of sex in multicellular different genes at their MAT loci. The full the incoming nucleus. These same events fungi has also provided key insights into complement of genes necessary for sexual (pheromone secretion, intracellular phero- how evolution has tweaked gene function development is only present when cells of mone signalling, nuclear migration, clamp and regulation in response to the acquisi- the two mates fuse. cell formation and fusion) can also clearly tion of different life styles and develop- be seen in the development of ascomycete mental complexity. Fungal sex genes were The name Dikarya derives from the fact hyphae. first identified in the unicellular budding that compatible cell fusion does not im- yeast Saccharomyces cerevisiae, and this mediately lead to nuclear fusion. Instead Given the shared developmental processes species was long considered a paradigm there is a prolonged mycelial stage, known that occur during sex in both ascomycetes for understanding how they work, but in as the dikaryophase, in which the two dif- and basidiomycetes, and regulation in generating the mating type (MAT) locus, ferent nuclei divide in synchrony in each both groups by the MAT loci, it was long

description of its flock every 15 minutes. Chickens on camera: health, Remarkably, these four numbers allow us to detect flocks in which there is, or will be, a welfare issue. For example, welfare and efficient farming flocks made up of healthy birds that walk easily can be distinguished from People across the world want to eat more producers, more efficient farming may flocks containing a larger proportion meat while livestock agriculture is under actually improve animal welfare. This is of poor walkers with damaged legs and pressure to reduce greenhouse gas emis- because some of the greatest improve- feet. The smartphones are able to pre- sions and to use less water and land. ments in both efficiency and welfare dict these health problems in chicks as Production, therefore, must become come from reducing mortality and waste young as three days old, long before they more efficient and more ‘sustainably and improving resistance to disease. show any clinical symptoms. We now intensive’. But what does ‘more efficient’ want to know whether the smartphones mean for food animals themselves? Does In collaboration with Stephen Roberts can detect which flocks are carrying more ‘sustainably intensive’ mean that in the Department of Engineering Sci- specific diseases. Working with Martin pigs, chickens and cattle will have even ence, we are developing smartphone Maiden, Frances Colles and Adrian less space, less food and less water than software to help farmers manage their Smith in the Department of Zoology, we they have now? Is animal welfare on a flocks more effectively. The cameras on are looking at how our four indicator collision course with human food secu- the phones monitor the movements of numbers vary with flocks with different rity and tackling climate change? chicken flocks and the images are ana- levels and genotypes of Campylobacter, lyzed on the spot. The cameras do not Salmonella, Clostridium and Coccidia. Our research on the welfare of broiler track the movements of individual birds (meat) chickens shows that such a clash (that would be quite overwhelming in a Of course, a smartphone camera does is not inevitable and that, by work- house of 30,000 or more chickens) but not replace good human observation, ing closely with commercial poultry each phone simply delivers a 4-number but it does provide an extra eye for when

www.biology.ox.ac.uk Biology News, University of Oxford I Issue Three I 2014 7 assumed that regulatory gene function types but in basidiomycetes there are unicellular yeasts where there is no di- first identified in the yeast S. cerevisiae thousands of mating types and as such the karyophase because cell fusion is followed would be conserved in other dikaryons. pheromone and other critical sex genes immediately by nuclear fusion? In the most But evolution can be more sophisticated have to be regulated differently. ancient forms of the yeast MAT loci (as seen than that, and ascomycete and basidiomy- in Candida albicans), one locus has a gene cete MAT loci harbour unrelated genes. The essential genes for mate recognition encoding the typical ascomycete HMG- In ascomycetes there are only two mating and sexual development in basidiomy- domain factor linked to an types (a/alpha, plus/minus) and one MAT cetes reside in two MAT loci. One locus HD2 gene, and the other locus has a gene locus; in its simplest form (found in fila- contains the structural genes encoding encoding the alpha-domain transcription mentous ascomycetes) the two alternative different allelic forms of the all important factor linked to an HD1 gene. Importantly forms of MAT contain different genes sex pheromones and receptors and the there are telltale signs that these genes have with one encoding an HMG-domain other locus contains different allelic forms been brought together by rear- transcription factor and the other encod- of a pair of homeodomain transcription rangement. It is therefore hypothesised that ing an alpha-domain transcription factor. factors (HD1 and HD2). Compatible cell the forms of MAT (a and alpha) that were In combination, the two transcription fusion only occurs when different allelic first identified in S. cerevisiae were derived factors induce the synthesis of mating forms of these HD proteins heterodimer- from an ancestral HD1-HD2 gene pair. The type specific sex pheromones and of the ise (HD1/HD2) to form a transcription MAT a locus retained the HD2 gene and an corresponding receptors. Pheromones are factor unique to mated cells. Homologues inactivated HD1 gene, while the MAT alpha secreted as attractants leading to fusion of of HD1 and HD2 genes have yet to be locus retained the HD1 gene and recombined compatible cells. This type of regulation identified in filamentous ascomycetes but with an alpha-domain transcription factor works well when there are just two mating for such a conserved developmental path- that replaced the HD2 gene. The gene encod- way, evolution is unlikely ing the expected HMG domain transcription to have invented other pro- factor was lost from the a locus and so the teins to enable dikaryosis. pheromone and receptor genes it would have John Baker Most likely the two genes induced are now expressed constitutively encoding these proteins are and must be repressed in MAT alpha haploid another subset, along with cells, a new function for the HD1 in the pheromone and recep- addition to its function as a heterodimer in tor genes, that are regulated mated cells. Importantly this scenario could differentially in the two not have been envisaged without a compara- mating types by the HMG tive approach that focused on gene homol- or alpha-domain transcrip- ogy. Such approaches allow us to trace how tion factors encoded at the evolution has adapted the tools at its disposal MAT loci. to promote new life styles and the develop- mental complexity that accompanies this. So how do these discov- eries relate back to our Lorna A. Casselton understanding of sex in Coprinus cinereus on petri dish

no-one can be present. Our ultimate aim is a phone app that famers can carry around and then be warned when the cameras detect something unusual that would suggest an incipient health or welfare issue. Globally, 58 billion chick- ens are killed each year for food (nearly

U.S. Department of Agriculture 1 billion in the UK), more individual animals than any other species. For the welfare of these animals to be taken seriously as part of the efficient farm- ing of the future, welfare needs to be firmly linked to human food security, animal and human health and financial competitiveness. We hope that an easy to use smartphone app will go some way to forging these links and improving the lot of our commonest food animal.

Marian Stamp Dawkins

Most Broiler (meat) chickens are kept in large groups of up to 50,000 birds.

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Mathematical ecology parent (or parents) but ensures a parent get its

genes into future genera- Oxitec Ltd.

Francesca Lock tions. However, parents often cannibalise off- spring. Our theoretical work on the evolution of parental care (with Hope Klug at the University of Tennessee) emphasizes the ecological condi- tions under which care or cannibalism might evolve. Some key find- ings are that ecological resource competition plays an important role. Mouse blastocyst Care is more likely to evolve when adult life-spans are short: Mathematical approaches play an ever- individuals have more to lose if their growing role in biology. Research work capacity to reproduce is curtailed, and in the Department of Zoology has a rich parental investment in just increasing history of the use and application of offspring survival through the vulnerable mathematical approaches. This tradition life stages can evolve as the only benefit of Aedes aegypti, the mosquito vector of dengue continues today, with research spanning care (without any other benefits such as fever, taking a blood meal the hierarchy of complexity in the life sci- the need for sustained provisioning). ences. At the centre of our work is a desire Through competitive funding from BB- to understand how diversity in life evolves GM Insects SRC, we have recently completed a major and is organised; how do deterministic For almost 10 years now we have been project with Oxitec exploring the interface and perceivably more random processes working with Oxitec, a spin out company between insect ecology, genetics and GM interact to affect biological complexity? from Zoology, that has developed novel technologies. A new BBSRC supported genetic-based technologies for the control project with Oxitec and Imperial College Theoretical Developmental Biology insect pests and vectors. These technolo- aims to understand how these genetically- The organisation of early mammalian gies work very much like the sterile insect modified insects can be used to manage embryos is a venerable problem (and has technique in aiming to reduce the size of insect resistance. This work will focus on had a research focus in Zoology for almost pest (or vector) populations and, in recent the diamondback moth which is a major 50 years). For example, how do cells in the field trials, Oxitec have proven achieve- pest of crucifer crops around the world. early embryo organize themselves, and ments in the reduction of both agricul- Conventional methods of control focus does predetermined patterning exist? In tural pests and human disease vectors. on the use of microbial and chemical work with Chris Graham (and colleagues pesticides yet diamondback moth has rap- from the Maths Institute in Oxford) we idly evolved resistance to these controls. have shown how simple rule-based deci- Modelling work by Nina Alphey in the sions of cell organisation can explain the group has shown that the introduction of increasing array of experimental pat- Allen Moore genetically-modified insects will not only terns in early mammalian embryos. More reduce pest population size but should recently, our theoretical models are being drive up susceptibility to conventional put to work (with colleagues at Southamp- control methods by introgressing wildtype ton) to explore cell allocation decisions (not resistant) strains. The details matter in the blastocyst (the ball of cells which is and our new research project will build on made up a group of ‘inside’ and a group of this idea but also focus on specific applied ‘outside’ cells). Allocation to outside cells issues like when and where is it optimal (trophectoderm) and inside cells (inner to undertake genetic-based methods of cell mass) is predicted to be controlled, control to manage insect resistance. amongst other things, by variability in cell cycle times between these two different The future groups of cells. The future looks bright. Research in mathematical biology is highly collabora- Evolution of Parental Care tive, well placed to make conceptual and How and why parental care evolved applied advances in the life sciences and and how it is maintained draws on both as such it is really an exciting and vibrant evolutionary and ecological theory. Care time to be involved in this sort of research is expected to increase offspring survival, in Oxford. be costly (in an evolutionary sense) to the Female burying beetle provisioning her larvae Michael Bonsall

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Paleovirology: ancient and modern in animal information contained that viruses of all known genome types in DNA sequences. and replication strategies can form EVEs. To circumvent these This includes viruses with DNA and RNA

Thomas Lersch Thomas obstacles, we turn to the genomes, double and single stranded genomes of the organ- varieties of both forms, with dates of inte- isms that viruses infect. gration stretching back to the Cretaceous. This diverse set of ancient viral forms The genomes of animals is a gold mine of evolutionary informa- are riddled with frag- tion, and is referred to as the ‘viral ments of viruses that record’. The analysis of EVEs has greatly hold the key to under- facilitated the study of , and standing viral evolution- has led to the recently established field of ary history. They are palaeovirology. known as endogenous viral elements (EVEs), Not all viruses in animal genomes are and result from the passive relics however. Occasionally integration of viral DNA endogenous that are nor- into the genome of the mally silent can be re-activated and this hosts’ reproductive can have serious consequences for their cells. When this occurs, host. A replicating can reinsert the is usually no into new genomic locations, potentially longer functional, but its inactivating or altering the expression of Chimpanzee, Pan troglodytes DNA can be passed on a host gene. The inactivation of a tumour to the offspring, behaving like any other suppressor gene, for example, could lead The fossil record has contributed greatly host allele, capable of spreading within the to cancer. We know that some endogenous to our understanding of the evolution population and potentially persisting for retroviruses can be more active in patients of animal life. Viruses do not have such millions of years. Remarkably, EVEs that with several diseases such as cancer, a physical fossil record as they do not originate from retroviruses in humans autoimmune disorders or those with HIV/ persist for long outside an , and make up approximately 5% of the genome, AIDS. However, it is currently unclear as a result, the long-term evolutionary compared to only about 1.5% that codes whether this upregulation is a cause or a biology of viruses has until recently been for our own protein-coding genes. consequence of disease. In collaboration poorly understood. Another way to study with Gkikas Magiorkinis, we are looking evolution is to use analytical techniques Once an EVE is formed, the rate of evolu- into the of the upregulation of en- to reconstruct evolutionary history from tion of the viral sequence slows down by dogenous retroviruses in human disease contemporary DNA sequence data. This several orders of magnitude to the host in order to shed light on this connection, approach is also limited when it comes to neutral rate, preserving information about potentially leading to novel therapy tar- viruses, particularly for events that have the virus’ past for much longer. Retrovirus gets in future. occurred millions of years ago, because EVEs were identified in the late 1960s, rapid rates of viral evolution erode the and more recently we have demonstrated Aris Katzourakis Amr Aswad

An endogenous viral element that integrated in the common ancestor of chimpanzees and humans, but not orangutans. Coloured blocks indicate genes – viral genes are in green and purple.

www.biology.ox.ac.uk 10 Biology News, University of Oxford I Issue Three I 2014

Inbreeding modifies species interactions likely to fluctuate more than host-plant In line with previous findings this research populations, but they are also likely to be demonstrates that inbreeding reduces plant more connected due to migration between resistance to herbivores: inbred plants were Anne Muola Anne populations. A small plant population is consumed more and inbreeding also altered not necessarily always associated with a the defensive chemistry in the leaves. This small herbivore population and vice versa. negative effect of inbreeding on resistance This means that plants in inbred popula- was, however, reduced when inbred plants tions can interact with inbred or outbred were eaten by inbred herbivores. Outbred herbivores, which can hugely influence herbivores were, in turn, able to take advan- how inbreeding affects their interactions. tage of the altered chemistry and nutrient content in inbred plants and, therefore, out- For over a decade my research group has bred herbivores were able to consume more Abrostola asclepiadis feeding on Vincetoxicum investigated the interactions between of the inbred plants. In other words, nega- hirundinaria (left) the long-lived perennial Swallow-wort tive effects of inbreeding on plant resistance Investigating the impact of inbreeding in a (Vincetoxicum hirundinaria) and its were more prominent when herbivores were greenhouse experiment (right) specialist insect herbivores in a naturally outbred. When investigating the impact of fragmented archipelago landscape in herbivore inbreeding on their performance Today many plant species occur in small SW Finland. We have been particularly we found that inbreeding resulted in re- and fragmented populations where indi- interested in understanding how frag- duced performance, but that this inbreed- viduals mate with relatives or in extreme mentation influences the evolution or ing depression was more pronounced when cases with themselves. This inbreeding coevolution of these interactions. Our herbivores were fed on inbred plants that has long been known to reduce plant research has been motivated by the idea are likely to be of poorer quality and, thus, fitness and population viability. More that understanding how fragmentation a more stressful environment for the her- recently research has demonstrated that affects coevolution, a process responsible bivores. Inbreeding depression is generally inbreeding can also influence the interac- for creating and maintaining diversity, greater under stressful environments. This tions between plants and other organ- improves our ability to understand and research provides the first evidence show- isms by, for example, resulting in lower predict its impact on diversity. Recently ing that the impact of inbreeding on traits resistance to herbivores. This research Aino Kalske, a PhD student in the group, central for species interactions depends has, however, been unrealistic in ignoring wanted to understand better how inbreed- on the level of inbreeding in both of the the impact of fragmentation on interact- ing influences the interaction between the interacting species. Focusing on the effects ing species. In nature populations and Swallow-wort and the leaf feeding special- of inbreeding on only one species at a time communities of interacting species often ist Abrostola asclepiadis depending on the is likely to provide an unrealistic picture of decline together, especially if the interac- level of inbreeding or outbreeding in both its impact. tions are very specialized. In interactions of the interacting species and not only between insect herbivores and long-lived in one of the species as had been done in Roosa Leimu host plants herbivore populations are previous studies.

From spiders’ silks to medical devices The spider’s web is a marvel of engineer- comprehensive biological understand- ing: gossamer threads combine to form ing as well as the application of the fullest a structure that can barely be seen, only possible range of state-of-the-art tools glimpsed, but that nevertheless can stop and techniques developed in the polymer Vollrath Fritz (and hold) a bumblebee in full flight. In the sciences. web of the garden cross spider the mecha- nisms involved range from, self-assembling In silks, water is the solvent and long- micro-scale windlasses and electrostatic chain proteins are the main structural charging in glue droplets, to nano-scale components. Protein and water molecules molecular arrangements. are interlaced in such a way that they can easily separate during ‘spinning’. This de- As we all know, the threads of spider hydration denaturation ushers the protein webs are silks. Not identical, but also not molecules to refold, combine and interlink very different from the silks made by the into a very tough and lasting material. mulberry silkmoth used in commercial Some spider silks, such as the frame and textiles. But because of the way they are radial threads of a typical orb web, demon- spun, the silks of spiders are more eas- strate the superb mechanical performance ily studied than those of silkmoths, and that can be achieved with this process. they have opened the door to new insights Molecular order, or rather the combina- into the truly remarkable properties of all tion of ordered and disordered regions, silks. Importantly, silk research provides a determines strength and stretchiness. And truly trans-disciplinary field for it requires exquisite spinning technology guarantees Web of a sector spider, Zygiella x-notata, Oxford

www.biology.ox.ac.uk Biology News, University of Oxford I Issue Three I 2014 1 1

Plants delivered by UPS In plants, photosynthesis takes place Actually, are just within subcellular structures (organelles) one member of a broader fam- called chloroplasts. A photosynthetic leaf ily of structurally and func- cell typically contains ~100 chloroplasts, tionally diverse organelles each one approximately 5 micrometres in called ; other family

diameter. Chloroplasts contain large quan- Qihua Ling & Paul Jarvis members are etioplasts in tities of the green pigment chlorophyll, dark-grown plants, chromo- which enables light absorption for photo- plasts in ripe fruit and flow- synthesis, and as many as 3000 different ers, and amyloplasts in roots, types of protein. Although chloroplasts tubers and seeds. Different retain a functional genome of their own types interconvert in (an indicator of their evolutionary origin response to developmental as free-living photosynthetic bacteria), the and environmental cues. For vast majority of proteins are example, etioplasts quickly encoded in the nucleus and synthesized differentiate into chloroplasts in the cytosol. These nucleus-encoded as etiolated seedlings emerge proteins must then be imported by chloro- into the light, to enable rapid plasts, and this is achieved by sophisticated photosynthetic establish- import machinery in the envelope mem- ment. During fruit ripening branes that surround each organelle. Images, taken using a transmission electron microscope, in tomato, bell pepper and of typical chloroplasts in three different genotypes of citrus, chloroplasts transform Using a genetic screening approach, we re- Arabidopsis thaliana, superimposed on a photograph showing into that syn- cently identified a new gene called SP1 that the appearance of the corresponding plants. Mutant plants thesize and accumulate red, regulates the chloroplast protein import with defects in chloroplast protein import (bottom) are orange or yellow carotenoid machinery. The SP1 gene encodes a type of considerably smaller and paler than wild-type plants (top). pigments (which have dietary enzyme (a ubiquitin E3 ligase) that targets Differences in chloroplast development between the geno- significance as provitamin A unwanted proteins for proteolytic removal types at the bottom left and bottom right are entirely due and as antioxidants). These by the cytosolic ubiquitin-proteasome to altered activity of the SP1 gene. plastid type interconversions system (UPS) – a major proteolytic system are linked to reorganization in eukaryotes that had not previously to regulate which proteins are imported by of the organellar proteome, a process in been linked to chloroplast development. chloroplasts. Because imported proteins which we believe SP1 plays a critical role. The SP1 protein is embedded in the outer define the organellar proteome to a large envelope membrane of chloroplasts, where extent, and are largely responsible for We have shown that SP1 (which or- it acts to specifically control the abun- the functions of chloroplasts, SP1 is very chestrates UPS activity) is essential for dance of key components of the protein influential. chloroplast development from etioplasts import machinery. In this way, SP1 is able in seedlings of the model plant Arabidop- sis thaliana (thale cress); in fact, mutant plants lacking SP1 are unable to de-etiolate efficiently, and die as a result. We believe flawless filaments ranging in thickness bio-compatibility combined with that SP1 will prove to be important during from a few microns to a few tens of resorption in the human body. Some other developmental processes under- nanometers. silks integrate faster into the body than pinned by plastid type interconversions, others and this feature can be modified and, therefore, that SP1 will find applica- Fundamentally, moth silks are all of chemically in order to tune a medical tions in crops. For example, by manipulat- one basic design-type, while spider silks device, for example. Silk threads can ing the activity of the SP1 gene, it may be cover a wide range of types. Moreover, also be rendered chemically down to possible to speed up or slow down fruit a silkmoth larva has only one set of their molecules and then rebuild into ripening; doing so might help to prolong glands while a spider produces several forms other than threads. In this way the shelf-life of certain fruits, reduc- and rather different silk types each one of our spin-out (so sorry) compa- ing waste, or enable farmers to expedite originating in a dedicated gland. Impor- nies has developed a silk-based menis- ripening when time is limiting. Alter- tantly, the ability to collect the silk un- cal implant, hard and tough and with natively, the SP1 technology may enable der highly controlled conditions makes sponge-like holes to accommodate modification of amyloplast development some spider silks excellent model ma- cell ingrowth. Funded largely by the in the grain of field crops such as wheat terials in the pursuit of understanding Wellcome Trust, this implant is about to and rice, or alteration of the rate at which animal silks. And there are important go into clinical trials. If successful, then leaves age (a process characterized by the lessons to be learned, as we are finding this would be the first silk-based medi- degeneration of chloroplasts into geronto- out, about potentially transformational cal device on the market, other than, of plasts), keeping crops green for longer and manufacturing technology for tough, course, the age-old silk suture threads potentially improving yields. These and sustainable, bio-inspired polymers fit still going strong. However this may other exciting possibilities for the practical for 21st century applications. be, the hopes for silks in regenerative application of our research in crops medicine are very high all round. are currently being investigated. There are also novel applications for the silks themselves. An interesting Fritz Vollrath Paul Jarvis feature of some silks is the excellent

www.biology.ox.ac.uk NEWSLETTER FOR BIOLOGY ALUMNI AND FRIENDS

Do visit our website (www.biology.ox.ac.uk/alumni), and email us on [email protected]

Other websites: www.alumni.ox.ac.uk; www.plants.ox.ac.uk; www.zoo.ox.ac.uk Martin Speight Martin Speight Martin OXFORD UNIVERSITY ALUMNI WEEKEND SEPTEMBER 2014

The Departments of Plant Sciences & Zoology invite you, your family and your friends to our Open Day in the Department of Zoology

SATURDAY 20TH SEPTEMBER 2014 12.30 PM TO 5.00 PM

Attractions will include TALKS: Prof Phil Poole – ‘Addressing the Global Nitrogen Crisis’

Dr Lindsay Turnbull – ‘Looking Up and Looking Down: How to Integrate Ecology into the Rest of Biology’

Prof Peter Holland – ‘Ecology, Evolution & Eccentricity: A History of Zoology at Oxford’

Dr Ashleigh Griffin – ‘Evolutionary Biology: From Birds to Bacteria’

TOURS AND DISPLAYS: Oxford University Herbaria, Department of Plant Sciences Research & Teaching Exhibits, Department of Zoology

Refreshments will be served

TO REGISTER PLACES, PLEASE EMAIL [email protected] Martin Speight Martin

Front cover Graphics: Máté Nagy Photos: Zsuzsa Ákos, Simon Walker